Prevalence and Determinants of Diabetic Retinopathy in Al Hasa Region of Saudi Arabia: Primary Health Care Centre Based Cross-Sectional Survey, 2007–2009

Abstract

Purpose:

To evaluate the prevalence of diabetic retinopathy (DR) in the urban and rural areas of Al Hasa region of Saudi Arabia and to determine risk factors related to DR.

Materials and Methods:

This study was conducted on patient attending primary health care centers between July 2007 and June 2009. A retrospective chart review was conducted on subjects with diabetes mellitus greater than 18 years old. Ophthalmologists examined DR status through dilated pupils by using direct, indirect, and slit lamp bio-microscopy. Frequencies, percentage, and their 95% confidence intervals (CIs) were calculated. Odd’s ratio was used to associate DR with possible risk factors. A P value less than 0.05 was considered statistically significant.

Results:

The prevalence of DR among 473 diabetic subjects was 30% (95% CI: 25.80–34.20). The odd ratios (ORs) of DR among diabetic residing in an urban area was significantly higher than diabetics residing in rural areas [OR = 1.94 (95% CI of OR 0.82–2.89)]. DR was associated to the duration of diabetes (adjusted OR = 1.70), uncontrolled blood sugar level (adjusted OR = 1.96), hyperlipidemia (adjusted OR = 2.04), and hypercholesterolemia (adjusted OR = 2.80).

Conclusions:

DR appears to be a public health problem in the Al Hasa district of Saudi Arabia, and a planned approach is required to avoid severe visual impairment in patients with diabetes mellitus. Primary prevention and early detection could be implemented through primary health centers and non-ophthalmologists.

INTRODUCTION

The World Health Organization (WHO) describes diabetes mellitus (DM) as the most common endocrine disease in the World.¹ Approximately 25% of the population in the Kingdom of Saudi Arabia (Saudi Arabia) has been diagnosed with diabetes.² Over the last decade, there has been an 8% increase in the prevalence of DM in Saudi Arabia.² Previous studies on the Saudi population have reported rural –urban differences in the prevalence of diabetes mellitus.³

The most common complication of DM is diabetic retinopathy (DR).⁴,⁵ Diabetic retinopathy is a leading cause of blindness among the working class populations of both developing and developed countries.⁴,⁵ In Riyadh, Saudi Arabia, 31.3% of diabetics have DR.⁶ To our knowledge, no primary health care-or population-based study has been conducted on the Saudi population to determine the whether the prevalence of DR differs among the rural and urban residents.

To study urban–rural differences, we conducted a study in the Al Hasa district located in the eastern province of Saudi Arabia. This district has a population of 600,000 people residing in 50 villages and 3 cities and spans an area of 120 km² [Figure 1].⁷ Al Hasa is divided into three health sectors: (1) Al Mubarraz with 17 primary health care centers; (2) Al Hofuf with 12 primary health care centers, and (3) Al Omran with 18 primary health care centers. Al Omran is a rural area.⁸ Ophthalmologists routinely screen diabetic patients referred by the general physicians from various primary health care centers of these sectors. The goals of this study were to estimate the prevalence and distribution of DR among diabetics in Al Hasa district and identify the risk factors of DR and propose polices to enhance eye care of diabetic patients in this region.

Figure 1.

Map of Al Hasa (surrounding countries are shown with bullet sign)

MATERIALS AND METHODS

A cross-sectional study was conducted in 2009. A retrospective chart review was conducted on all patients who over 18 years old with registered diabetes mellitus in the health institutions of the district during the period July 2007 to June 2009. Written permission from the health authorities of the Al Hasa district was obtained before conducting this study. As secondary data were collected from patient charts, written consent from study subjects was not required. The identity of all subjects remained confidential for the duration of this study.

Patients and sample size calculation

A total of 2552 patients with diabetes (660 rural residents and 1892 urban residents) were screened by ophthalmologists comprised the study population. Epi Info epidemiologic software (version 6; November, 1993, Centers for Disease Control, Atlanta, USA) was used to calculate a representative sample. For sample calculations, we assumed a prevalence of DR between 11.6% and 14.39% based on previous reports by Al Maskari and El-Sadig⁹ and Khandekar et al¹⁰ The calculated sample size was 527 diabetics based on a 95% confidence level with an additional 20% to compensate for missing data. Stratification of the sample was performed (135 rural and 392 urban) based on the population proportion to the size (PPS) of the screened cases with diabetes in both urban and rural areas. The prevalence of DM in the rural and urban areas of Al Hasa was assumed to be the same as the national prevalence. Data were collected on the status of diabetes (type, duration, and control), blood pressure (BP), age, gender, body mass index (BMI), serum lipid level, serum cholesterol level, three most recent readings of fasting blood sugar (FBS) level, and the results of the ophthalmic examination (specifically, visual acuity and fundus examination results).

Ophthalmic examination and subgroups

The fundus examination findings were based on the direct ophthalmoscopy, indirect ophthalmoscopy, and the retinal examination with a +90 diopter volk lens and Haag Streit Slit lamp (900BQ, Haag Streit AG, Switzerland). All eyes were dilated before funduscopy. All data were collected from the Primary Healthcare Centre (PHC)’s diabetic retinopathy screening records and patients’ chronic disease files and transferred to data collection sheets.

Subjects were divided into five groups based on age (from the patient chart): Group 1 (40 years or less); Group 2 (41–50 years); Group 3 (51–60 years); Group 4 (61–70 years), and Group 5 (greater than 70 years). Duration of diabetes was calculated from the date of the original diagnosis to the date of data evaluation for this study. Duration was rounded to the nearest year and classified as 1 year; 15 years; 6–10 years; 11–20 years, and greater than 20 years. Subjects were considered hypertensive if they were previously diagnosed by a physician or were taking blood pressure lowering medications, and/or had a systolic blood pressure (SBP) greater than 140 mmHg and/or diastolic blood pressure (DBP) greater than 90 Hg measured during last ophthalmic examination. A subject with SBP less than 130 mmHg or DBP less than 85 mmHg was considered normotensive.¹¹ Body mass index (BMI) of subjects with diabetes was categorized based on the American Heart Association criteria.¹² Subjects with three recent fasting blood sugar levels greater than or equal to 140 mg/dL were considered uncontrolled diabetics. Fasting blood sugar between 120 and 139 mg/ dL was considered reasonably controlled. Subjects with fasting blood sugar between 70 and 120 mg/dL had good control.¹³ Subjects with hyperlipidemia had blood lipid levels greater than 200 mg/dL.¹⁴ Diabetic retinopathy was graded according to the International Clinical Diabetic Retinopathy Severity Scale.¹⁵ Visual acuity measurements were performed with the Snellen distance vision chart. Vision was categorized as: normal vision with or without spectacles, e.g., 6/6; defective vision, e.g., subjects with refractive error whose vision did not improve with refraction; partially sighted; and blind.¹⁶

Data analysis

Statistical analyses were carried out using the Statistical Package for Social Sciences (SPSS; Student version 14). Frequencies via descriptive studies were used for categorical variables, whereas means and standard deviation were obtained for continuous variables. Chi-square statistics were used to assess associations between variables. Data were calculated with their respective 95% CI. The data were presented as mean ± SD. A P value less than 0.05 was considered statistically significant.

RESULTS

A total of 527 subjects met the study criteria of which only 473 (90%) patients’ charts were available. Patient charts of 54 subjects were not available due to death of the patients (2 subjects), migration to another part of the country (15 subjects), and routine follow-up at a local newly created diabetic center (37 subjects).

The cohort data comparisons are presented in Table 1. The differences in data indicated that our original estimate of prevalence of DR needed revision.

Table 1.

Demographic and clinical characteristics of the study sample

	Total no. (n = 473)	Percentage
Gender
Male	229	48.4
Female	244	51.8
Age groups (years)
<40	64	13.5
41−50	135	28.5
51−60	147	31.1
61−70	93	19.7
>70	34	7.2
Type of diabetes
Type 1	17	3.6
Type 2	456	96.4
Diabetic control
Uncontrolled	278	58.8
Reasonable control	53	11.2
Good control	142	30.0
Blood pressure
Normotensive	254	53.7
Hypertensive	219	46.3
Blood lipid level
Normal blood lipid	400	84.6
Hyperlipidaemia	68	14.4 *(5 missing data)
Blood cholesterol level
Normal blood cholesterol level	361	76.3
Hypercholesterolaemia	110	23.4

The mean duration of DM in this cohort was 8.61 ± 5.96 years. The mean BMI was 30.63 ± 5.49 kg/m². More than half (52.3%) of the subjects had the DM for 6 years or longer. More than half of diabetics in the cohort had uncontrolled blood sugar levels, 46.3% were hypertensive and 97.8% were obese.

The prevalence of DR by gender, age group, and geography is presented in Table 2 . The overall prevalence of DR was 30% [95% CI: 25.80–34.20]. The age, sex, and area-adjusted prevalence of DR were 29.4% [95% CI: 26.75–32.05]. The prevalence of DR by subgroups is presented in Table 3. The prevalence of DR between males and females was not statistically significant (P > 0.05). The odds of having DR increases one-and-half times in diabetic subjects who lived in an urban area compared to diabetic subjects in the rural setting [OR = 1.94 (95% CI of OR 1.24–2.80)].

Table 2.

Prevalence of diabetic retinopathy by gender, age group, and geography

Characteristics	Study population	DR present	Frequency
Gender
Male	229	73	31.9%
Female	244	69	28.3%
Total	473	142	30.1% (95% CI:
			25.80−34.20)
Age groups (years)
<40	64	8	12.5%
41−50	135	28	20.7%
51−60	147	44	29.9%
61−70	93	46	49.5%
>70	34	16	47.1%
Total	473	142	30.1%
Rural	119	34	28.57% (95% CI: 24.46−32.74)
Urban	354	108	30.50 (CI; 26.27−34.30)
Total	473	142

Table 3.

Prevalence of DR in the subgroups studied (risk factors of DR)

	Total (n = 473)	Prevalence of DR n (%)	P value
Type of DM
Type 1	17	5 (29.4)	= 0.995
Type 2	458	137 (30)	= 0.995
Duration of diabetes (years)			< 0.005
<1	87	10 (11.5)	< 0.005
1-5	138	29 (21.0)	< 0.005
6-10	139	47 (33.8)	< 0.005
11-20	99	50 (50.5)	< 0.005
>20	10	5 (50)	< 0.005
Diabetic control
Uncontrolled	278	101 (36.3)	< 0.005
Reasonable controlled	53	19 (35.8)	< 0.005
Good control	142	21 (14.8)	< 0.005
Blood pressure
No hypertension	254	66 (26.0)	= 0.063
Hypertension present	219	75 (34.2)	= 0.063
Blood lipid level
No hyperlipidemia	361	92 (25.5)	< 0.005
Hyperlipidaemia	110	49 (44.5)	< 0.005
Blood cholesterol level
Normal cholesterol level	361	93 (25.76)	< 0.005
Hypercholesterolaemia	110	49 (44.54)	< 0.005
BMI groups
Normal weight	10	4 (40)	= 0.647
Overweight	219	61 (27.9)
Obesity	205	63 (30.7)
Extreme obesity	39	14 (35.9)

Of the 142 DR cases, 64.8% had mild non-proliferative diabetic retinopathy, 23.9% had moderate non-proliferative diabetic retinopathy, 2.8% had severe non-proliferative diabetic retinopathy, 7.8% had proliferative diabetic retinopathy, and 0.7% had high-risk proliferative diabetic retinopathy. The prevalence of mild non-proliferative diabetic retinopathy was statistically significantly higher in urban areas compared to rural areas (67.6% vs. 55.9%, P = 0.000). However, there was a higher prevalence of more advanced DR such as moderate non-proliferative diabetic retinopathy, proliferative diabetic retinopathy, and high-risk proliferative diabetic retinopathy in rural (P<0.005) areas [Table 4]. Severe non proliferative was more common in subjects who lived in an urban setting (P<0.005).

Table 4.

Prevalence of different stages of DR among the detected DR cases rural vs. urban

	Total No of DR subjects (n = 142)	DR in rural subjects (n = 34), P = 0.000	DR in urban subjects (n = 108), P = 0.000
Mild NPDR	92 (64.8)	19 (55.9)	73 (67.6)
Moderate NPDR	34 (23.9)	10 (29.4)	24 (22.2)
Severe NPDR	4 (2.8)	0 (.0)	4 (3.7)
PDR	11 (7.8 )	4 (11.8)	7 (6.5)
High-risk PDR	1 (0.7)	1 (2.9)	0 (0.0)
Total	142	34	108

Figures in parentheses are in percentage

Multivariate logistic regression analysis suggested that patient’s age (t ratio = 4.1, P = 0.000), duration of DM (t ratio = 4.2, P = 0.000), blood lipid level (t ratio = 2.8, P = 0.006), blood cholesterol level (t ratio = 2.8, P = 0.006) were significantly associated with DR. Gender (t ratio = -0.194, P = 0.846) was not significantly associated with DR.

Visual status in the better eye was compared [Table 5]. Only 21.1% of subjects with DR had normal vision.

Table 5.

Showing relation of visual status with DR

Vision status of subjects	DR present/Percentage n = 331, P = 0.000	No DR/percentage n = 331, P = 0.000
Normal 6/6	30 (21.1)	218 (65.87)
Defective vision	88 (62)	60 (18.12)
Partially sighted	24 (16.9)	53 (16.01)

Figures in parentheses are in percentage

DISCUSSION

The prevalence of DR in our study was 30%, which is higher than that reported in Kuwait (23.5%),⁹,¹⁰ UAE (19%),¹⁷ Oman (14.4%),¹⁰ India (17.6%),¹⁸ and Pakistan (15.7%),¹⁹ yet lower than the prevalence in Egypt (43%),¹⁷ Jordan (34.1%),²⁰ USA (40.3%)²¹ and a specialist center of Southern India (34.2%).²² The prevalence of DR in our study is similar to 31% reported in a study of patients with diabetes for at least 10 years from tertiary centers in Riyadh, Saudi Arabia.¹⁰ This prevalence from the study in Riyadh study may be biased due to the referral of severe cases to tertiary care centers. However, a hospital-based study (2002) in the Aseer region of Saudi Arabia reported a prevalence of 11.3%.²³ The substantial differences in the reported prevalence of DR in previous studies and our study [Table 6] may be attributed to the differences in the study methodology, population, or the differences in the mean age of the study cohort. For example, case selection, DR grading, and detection methods may differ between studies.

Table 6.

Comparison with the prevalence of retinopathy in various countries

Country	Author	Year	Number of subjects	Retinopathy (%)
Saudi Arabia	Al-Khaldi23	2002	203	11.3
Oman	Khandekar10	2003	5564	14.4
India	Mohan Rana37	2005	1529	17.6
India	Rema et al.22	1998	6792	34.2
UAE	Fatma Al-Maskari9	2007	513	19
Kuwait	Al Kharji32	2006	709	23.5
Pakistan	Jamal-Uddin19	2006	912	15.7
Jordan	Al-Amer20	2008	1000	34.1
USA	Kempen21	2004	4440	40.3
Egypt	Fatma Al-Maskar17	2004	500	43
Saudi Arabia	Present study	2009	473	30

To our knowledge, the current study is the first to report the prevalence of diabetic retinopathy based on geographic distribution (urban vs. rural) in Saudi Arabia. The prevalence of DR was greater among subjects residing in urban areas (30.50%, P < 0.005) compared to their rural counterparts (28.57%, P < 0.05). The odds of DR increased to one-and-half times higher among the urban diabetics compared to rural diabetics [OR = 1.94 (95% CI of OR 0.82–2.89)]. This observation is consistent with previous studies in developing countries. A higher prevalence of DR among newly diagnosed diabetics who were urban residents (8.7%) compared to rural residents (6.5%) of Pakistan has been reported by Shaikh et al.²⁴ The difference in urban and rural prevalence of DR may be due to better access to diagnostic facilities among the urban population compared to the rural population. Another contributing factor may be various lifestyles. Urban residents tend to be more sedentary with relatively poor diet habits in comparison to rural residents.

We found that the risk of DR was associated with patients’ age and duration of diabetes, which is consistent with previous findings.⁹,^10–17 A longitudinal study by Aiello et al.²⁵ reported that the prevalence of DR in long-standing diabetics is not dependent on the control of diabetes. Aiello et al.²⁵ found that after 20 years of diabetes almost all patients with Type 1 DM developed DR, while approximately two-third of the patients with Type 2 DM developed DR irrespective of their blood sugar control. In contrast, the United Kingdom Prospective Diabetes Study (UKPDS)²⁶ found that good blood sugar control does reduce the risk of DR as well as does reduce the progression of retinopathy.²⁶ The Diabetes Control and Complications Trial (DCCT),²⁷ Diabetic Retinopathy Study (DRD),²⁷ and Early Treatment of Diabetic Retinopathy Study (ETDRS)²⁷ also support that good glycogenic control is important in the early stage of the diabetes and helps in delaying the onset of retinopathy and halting the rate of progression. Hence, the preponderance of studies do indicate control of blood sugar level is a factor in preventing DR.

We found that hypertension did not play a significant role in the prevalence of DR which is consistent with the results of Rema and Pradeepa.²² A cross-sectional study of type 1 diabetics found an increased prevalence of DR among hypertensive patients.²⁸ A longitudinal study (UKPDS)²⁹ suggested a strong association between the prevalence of DR among the type 2 diabetes and hypertension.²⁹ The outcomes of the Wisconsin Epidemiology Study of Diabetic Retinopathy (WESDR) also suggested that systolic blood pressure was a significant predictor of progression in mild retinopathy to proliferative diabetic retinopathy in patients with type I diabetes for 5–14 years.³⁰ However, the WESDR study did not find an association between blood pressure and DR at baseline, nor between progression of DR in hypertensive people with type 2 diabetes.³⁰

A significant association between the prevalence of DR and blood cholesterol level was noted in this study which is consistent with previous reports. Bajpa et al.³¹ found a significantly higher prevalence of DR among subjects with high blood cholesterol levels. Similarly, Al Kharji et al.³² reported a positive association between serum cholesterol level and the prevalence of DR. The study by Al Kharji et al.³² found that the level of blood cholesterol is significantly related to the presence of any retinopathy (P < 0.000) and the association to severity of DR was also significant (P < 0.001). However, van Leiden³³ did not find any association between the incidence of DR and blood cholesterol level. This study did not find a statistically significant association between BMI and DR.

This study clearly demonstrated a high rate of visual impairment among the DR cases. This outcome may be due to our presumption that the main contributing factor for this vision loss was DR. The possibility does exist that other conditions such as cataract, glaucoma, complications from trachoma, or amblyopia may also be present in subjects with DR that may have contributed to the high rate of visual impairment. However, these conditions were not noted in the subject charts hence we defaulted to DR as the cause of visual morbidity. A high rate of legal blindness among diabetics has been reported in the literature.³⁴,³⁵ One study estimates legal blindness is 50–80 times higher in people with diabetes.³⁴ Among the 37 million blind people worldwide, 4.8% (1.3 million) suffer from DR.³⁵

This is the first time the prevalence of DR has been documented in the Eastern region of Saudi Arabia. The prevalence of DR was related to subject age, disease duration, presence of hypertension, hyperlipidemia, hypercholesterolemia, uncontrolled diabetes, and geographical area. As incidence of blindness due to DR increases, early screening of DR is crucial. Primary Health Centers and General Practitioners (GP) are vital in early detection and primary prevention. As limited a number of ophthalmologists may be available at the Primary Healthcare Centers (PHC), “ophthalmologist led” screening service could be initiated. The screening facilities using easy digital imaging that could be accessible could improve uptake of DR screening. General practitioners, Optometrist, and retinal photographers can be team members for providing such screening. Screening by non ophthalmologists such GPs and paramedical personnel has been shown to be a reliable method in detecting DR.³⁶

This study showed a high prevalence of DR in the Al Hasa district of Saudi Arabia. The incidence of diabetic retinopathy is expected to rise substantially in the coming years due to increasing prevalence of diabetes mellitus. This study also revealed several risk factors and epidemiological determinants such as age, gender, and geographic areas. Similar studies are recommended in other areas of Saudi Arabia in order to determine the scope of this condition nationwide and for the implementation of public health policies.