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Abstract

Objectives

Individual studies in the Eastern Mediterranean Region (EMR) have shown the high prevalence of diabetic retinopathy. We conducted a meta-analysis to yield an estimate of the prevalence of diabetic (type 1 and 2) retinopathy in the EMR. Additionally, we explored its potential modulators.

Methods

Two-step screening of relevant articles published from 1 January 2000 to 13 December 2019 was carried out. An estimation of summary proportions, subgroup analysis, meta-regression, and publication bias assessment were performed.

Results

One hundred nine articles were included in the meta-analysis, involving 280,566 patients. The prevalence of diabetic retinopathy was 31% (95% confidence interval [CI] = 28, 33). The highest and lowest diabetic retinopathy prevalence rates were observed in low human development index (HDI) countries (63.6; 95% CI = 52.4, 74.0) and very high HDI countries 22.6 (95% CI = 20.5, 24.7), respectively.

Conclusions

The prevalence of diabetic retinopathy is high in the EMR. Our results provide important information for diverse healthcare surveillance systems in the EMR to implement the modifiable risk factors, diabetes screening to decrease undiagnosed diabetes, early detection of retinopathy, and proper diabetes care to decrease untreated diabetes.

Keywords

Prevalence epidemiology meta-analysis diabetic retinopathy diabetes mellitus diabetes complication diabetic angiopathy vascular disease Eastern Mediterranean Region systematic review

Introduction

Diabetes mellitus is one of the most prevalent metabolic disorders that has reached epidemic proportions worldwide, exerting a substantial burden on healthcare services. Based on International Diabetes Federation (IDF) reports, approximately 537 million people had diabetes in 2021, and this rate is projected to increase to 643 million people by 2030 and 783 million by 2045.¹ Approximately 87.5% of people with undiagnosed diabetes live in low- and middle- income countries. Countries with a high prevalence of undiagnosed diabetes show an increased incidence of diabetic complications.¹ Undiagnosed or untreated complications will inevitably affect the patients’ quality of life and become a burden for the health system.²

Diabetic retinopathy is a chronic diabetic complication and a leading cause of blindness and vision disabilities worldwide.³ This complication develops in almost all patients with type 1 by two decades after diagnosis and approximately 80% of those with type 2 diabetes.⁴ Different risk factors are associated with retinopathy in patients with diabetes; the most important factors are age, duration of diabetes, high blood pressure, high body mass index, hyperglycemia, and hypercholesterolemia.^6–9

The Eastern Mediterranean Region (EMR) is a sub-community of the World Health Organization (WHO) with countries located in southwest Asia, Western Asia, and North Africa, including a range of low-, middle-, and high-income countries.^10–12 There is an increasing trend in the prevalence of type 2 diabetes in middle- and low-income countries.¹³ As the WHO stated, the EMR has the highest prevalence of diabetes worldwide, with 43 million people living with the disease in 2014 (14% versus 9% global prevalence among people aged ≥ 18 years).¹⁰ Additionally, several regional studies indicated a wide range of diabetes prevalence rates in the EMR, such as 14.1% in Iran¹² and 32.8% in Saudi Arabia.¹⁵ Similarly, the prevalence of diabetes complications is dramatically increasing in the EMR.¹⁶ In a systematic review from Pakistan, the prevalence of diabetic retinopathy was 28%, ranging from 10.6% to 91.3%.¹⁷ A meta-analysis from Iran showed an overall prevalence of diabetic retinopathy of 37.8%.¹⁸ In addition, several studies from Saudi Arabia,^19,20 Kuwait,²¹ and Jordan²² reported that diabetic retinopathy is highly prevalent (27.8% to 36.4%, 50%, and 48.4%, respectively).

One mission of surveillance services in decreasing the burden of retinopathy on the health system and patients is to provide information regarding the prevalence of diabetic retinopathy for healthcare policymaking.²³ Systematic epidemiologic data are vital for government health legislation to implement early detection and efficient intervention; however, to the best of our knowledge, no study has evaluated the prevalence of diabetic retinopathy in the EMR. Therefore, we conducted a systematic review and meta-analysis of relevant studies published since 2000 to estimate the incidence of diabetic (type 1 and 2) retinopathy in the EMR.

Materials and methods

We followed the Preferred Reporting Items for Systematic reviews and Meta-Analyses (PRISMA) 2020 guideline and checklist.²⁴ We did not prospectively register this trial but registered it retrospectively at Research Registry (registration number: reviewregistry1362; registered on 18 May 2022). The study protocol was approved by the Ethics Committee of Shiraz University of Medical Sciences (code: IR.SUMS.REC.1398.818). Because this meta-analysis used the results of published studies, which did not contain individual data, informed consent was not applicable.

Search strategy

This meta-analysis of effect estimates was designed and conducted in January 2020 to estimate the prevalence of retinopathy in patients with both type 1 and type 2 diabetes in the EMR. We searched for the relevant keywords in the title and abstract of articles from Medline/PubMed, Scopus, Embase, Web of knowledge, and Google Scholar (gray literature) to identify the target studies published from 1 January 2000 to 13 December 2019. The keywords list is provided in Appendix 1. Additionally, the references of systematic reviews and meta-analyses were manually searched to include all relevant articles. The articles list was collected in EndNote X9.

Selection criteria

The first screening was conducted based on the title, abstract, and quality assessment by two independent researchers (S.D-KH and P.A-CH). The second screening was performed by scanning the entire manuscript. An article was included if it studied the prevalence of retinopathy among patients with diabetes in a normal population. In cases of conflict, a third researcher (A.H) made the final decision whether to include or exclude an article. The Joanna Briggs Institute checklist for systematic reviews was used for methodological quality assessment (possibility of bias in design, conduct, and analysis) of included studies.²⁵ The result of the quality assessment is presented in Appendix 2.

Data extraction

All targeted statistics were entered into a checklist prepared as a spreadsheet. This checklist included the first author’s name, publication year, recruitment time span, country, sample size, proportion (%) and upper and lower 95% confidence intervals (CIs) of retinopathy, range of participants’ age, mean duration of diabetes, and method of diagnosis.

Statistical analysis

Statistical analysis was carried out by R (v3.4.1, www.r-project.org) using metafor²⁶ and meta²⁷ packages. We followed a recently published paper for the meta-analysis of proportions.²⁸ Our codes are provided in Appendix 3.

For calculating the summary effect size, we applied the random-effects model because both between-study variance (tau;² true effect sizes related to population characteristics) and within-study variance (due to the random sampling error) exist in most series of observational studies on a specific topic. Additionally, results obtained by the random-effects model are more generalizable. The random-effects model was carried out using the restricted maximum likelihood method. Moreover, we applied the double-arcsine transformation method to make the included studies follow a normal distribution to obtain more accurate estimates of summary proportions and statistical analyses.

Heterogeneity consists of two distinct components: the between-study variance (tau;² real variation) and the within-study variance (sampling error). Because a considerable variation (heterogeneity) in the summary proportion usually exists, we visually inspected the output forest plot (studies with 95% CIs non-overlapping with the 95% CIs of the summary effect), performed X² tests (general heterogeneity), and calculated I² statistics (the proportion of heterogeneity refers to the between-study variance). It is worth noting that our estimated I² was 99.77% (95% CI = 99.70, 99.83), which means that approximately all heterogeneity could be attributed to the between-study variance. Therefore, we carried out subgroup analyses or meta-regression to explore different potential mediators of this heterogeneity of the effect sizes, including the Human Development Index (HDI; a relative measure of the living standards in human societies)²⁹, publication year, and mean duration of diagnosed diabetes. For subgroup analysis, the random-effects model was used to obtain summary effect sizes within each subgroup, and then a fixed-effects model was used to test whether these effects differed significantly from each other.

To visualize studies’ effects and their CIs, we generated a forest plot. It is worth noting that by visual inspection of another forest plot (Appendix 4) that sorted the studies according to their precisions (using standard error), the nine largest studies were considered outliers, which confirmed the high overall heterogeneity. However, we performed a quantitative test to determine if the outlying studies were truly outliers. It was carried out by externally studentized residuals, which consider a study as an outlier if its absolute value is larger than 3, and leave-one-out estimates for the amount of heterogeneity, which consider a study as an outlier if its exclusion leads to a considerable influence on the summary proportion. In the externally studentized residuals test, we did not find any study with an absolute value of larger than 3 (Appendix 5). Moreover, the leave-one-out diagnostic test did not find any influential outlier (Appendix 6–9).

We generated a funnel plot and carried out objective tests for publication bias, including Egger’s regression test and the rank correlation test, which are powerful for large meta-analyses involving more than 75 studies. However, it should be noticed that in epidemiology studies, papers reporting either low proportions or high proportions are likely to be published. Therefore, exploring the publication bias might not be applicable in meta-analyses of observational studies. p < 0.05 was considered statistically significant.

Results

Search results

We initially identified 4096 citations. After discarding duplicates (automatic: 930; manually: 198) and publications before 2000, 2974 studies were screened based on the title and abstract, which resulted in 153 articles for the second round of screening. In addition, 43 studies were manually added. After reading 196 full texts, 87 papers were discarded, and 109 remaining articles were entered into the meta-analysis. The reasons for excluding the 87 articles were: (1) studies outside of the EMR (n = 21), not normal population (n = 9), not reporting the prevalence of retinopathy (n = 6), reporting the incidence of retinopathy (n = 3), review or meta-analysis study (n = 13), non-English papers (n = 7), full text unavailable (n = 5), unclear results (n = 5), and irrelevant papers (n = 18). The flowchart of data retrieval is shown in Figure 1.

Figure 1.

Flowchart of search and screening results (PRISMA-2020-Flow-Diagram).

Description of the included studies

The basic characteristics of the included studies in the meta-analysis are shown in Table 1. Our dataset consisted of 109 studies that were published from 2000 to 2019 and contained population-based or secondary- or tertiary-care-based data on the prevalence of retinopathy in patients with diabetes in the EMR. The sample sizes of the included studies ranged from 51 to 64,351 patients, with a combined total of 280,566 patients. Twelve (11.01%) studies included undiagnosed subjects with type 2 diabetes, while the remaining studies were only conducted on known cases of type 2 and/or type 1 diabetes. The prevalence of diabetic retinopathy was reported for only patients with type 1 diabetes in three (2.75%) studies, only patients with type 2 diabetes in 61 (55.96%) studies, and both type 1 and 2 diabetes separately in 11 (10.09%) studies. Additionally, in 27 (24.77) studies, the prevalence of diabetic retinopathy was not provided for each type of diabetes separately, even though the study had been conducted on both types. Judgement for the remaining seven (6.42%) studies was not feasible. Furthermore, 13 (11.93%) and 7 (6.42%) studies provided the classified prevalence of diabetic retinopathy according to the stage (i.e., non-proliferative diabetic retinopathy and proliferative diabetic retinopathy) and the presence of macular edema in addition to the stage of diabetic retinopathy, respectively.

Table 1.

Basic characteristics of the studies included in the review.

#	Author, Year	Country, HDI	Time period	UDDM included	Diabetes type	N	PDR (%)	Age (year)	Mean duration	Diagnosis tool	Stage of DR (N)
#	Author, Year	Country, HDI	Time period	UDDM included	Diabetes type	N	PDR (%)	Age (year)	Mean duration	Diagnosis tool	Mild NPDR	Moderate NPDR	Severe NPDR	PDR	ME
1	Khanedkar, 2005²⁹	Oman, VH	2002	–	1 & 2 [Y]	2,520	14	NA	NA	C1,3	NA	NA	NA	NA	NA
2	Din, 2006³⁰	Pakistan, M	2002	–	1 & 2 [Y]	108	15.7	30–70	NA	C1	6	5	2	1	3
3	Humera Ishaq, 2016³¹	Pakistan, M	2013–2014	–	2	154	42.86	50.59 ± 10.24	NA	C1	NA	NA	NA	NA	NA
4	Taleb, 2008³²	Lebanon, H	2005–2007	–	2	235	33	57.7 ± 10.6	8.2 ± 6.6	C1	NA	NA	NA	NA	NA
5	Harb, 2018³³	Lebanon, H	2006–2016	–	2	484	24.6	NA	8.3 ± SD?	C1	30	32	14	43	81
6	Shaikh, 2008³⁴	Pakistan, M	2003	+	NA	660	15.3	≥30	NA	C1	NA	NA	NA	NA	NA
7	Alaboud, 2016³⁵	Saudi Arabia, VH	2014	–	2	748	14.7	25–97	NA	NA	NA	NA	NA	NA	NA
8	Al-Agha, 2015³⁶	Saudi Arabia, VH	2013–2014	–	1	228	4.4	10.99 ± SD?	NA	NA	NA	NA	NA	NA	NA
9	Esteghamati, 2017³⁷	Iran, H	2015–2016	–	1 & 2 [N]	30,202	21.9	≥18	NA	NA	NA	NA	NA	NA	NA
10	Hajar, 2015¹⁸	Saudi Arabia, VH	2011–2012	–	NA	740	27.8	≥50	NA	C1	NA	NA	NA	NA	NA
11	Alvi, 2016³⁸	Pakistan, M	2011–2012	–	1 & 2 [Y]	8,742	20.3	19–102	0.5	C1,2	NA	NA	NA	NA	NA
12	Ali, 2013³⁹	Pakistan, M	2011–2012	+	2	113	24.79	30–70	0.5	C1	NA	NA	NA	NA	NA
13	Memon, 2014⁴⁰	Pakistan, M	2009–2011	–	1 & 2 [Y]	10,768	24.7	53.18 ± SD?	NA	C1,2	1209	386	52	129	852
14	Javanbakht, 2012⁴¹	Iran, H	NA	–	2	3,472	40.4	59.4 ± 11.7	8.08 ± 6.7	NA	NA	NA	NA	NA	NA
15	Hussain, 2013⁴²	Pakistan, M	2011–2012	–	2	300	23.9	49.04 ± 0.69	7.17 ± 0.38	C1	NA	NA	NA	NA	NA
16	Valizadeh, 2016⁴³	Iran, H	2015	–	2	206	45.1	60.4 ± 3	13 ± SD?	NA	NA	NA	NA	NA	NA
17	Janghorbani, 2003⁴⁴	Iran, H	1992–2001	–	NA	549	45.35	45.7 ± 9.3	6.9 ± 5.7	C1	NA	NA	NA	NA	NA
18	Khandekr, 2015⁴⁵	Saudi Arabia, VH	2013–2014	–	1 & 2 [Y]	51	52	24-89	3.6 ± 4.2	NA	NA	NA	NA	5	4
19	Al-Zuabi, 2005⁴⁶	Kuwait, VH	2002–2004	+	2	92	7.6	≥51	0.5	C2	NA	NA	NA	NA	NA
20	Safi, 2019⁴⁷	Iran, H	2018	–	1 & 2 [N]	604	40	53 ± 14	9 ± 7	C1,2	NA	NA	NA	NA	NA
21	Rahman khan, 2010⁴⁸	Saudi Arabia, VH	2007–2009	–	1 & 2 [Y]	473	30	≥18	8.61 ± 5.96	C5	NA	NA	NA	NA	NA
22	Mehhana, 2017⁴⁹	Lebanon, H	2004	–	2	462	39.18	57.27 ± 10.91	8.39 ± 7.38	C1,3,5,6,7	62	18	14	8	NA
23	Katibeh, 2014⁵⁰	Iran, H	2012–2013	–	NA	529	29.5	40-80	NA	C1,2,5	NA	NA	NA	NA	NA
24	Aidenloo, 2016⁵¹	Iran, H	2012–2013	–	2	327	32.6	54.7 ± 8.4	7.3 ± 0.6	C2	NA	NA	NA	NA	NA
25	Jammal, 2013⁵²	Jordan, H	2009–2011	+	2	127	7.9	49.7 ± 10	0.5	C1	NA	NA	NA	NA	NA
26	Alberto, 2016⁵³	Saudi Arabia, VH	2012–2013	–	1 & 2 [N]	126	61	38-87	14.9 ± SD?	NA	NA	NA	NA	NA	NA
27	Ahmed, 2016¹⁹	Saudi Arabia, VH	2008–2013	–	2	401	36.4	54.6 ± 12.3	9.2 ± SD?	C2,3,5	84	29	16	17	NA
28	Ageely, 2019⁵⁴	Saudi Arabia, VH	2017	–	2	281	32.4	≥18	NA	NA	NA	NA	NA	NA	NA
29	Elwali, 2017⁵⁵	Sudan, L	2015	–	1 & 2 [N]	316	82.6	58.7 ± 10.5	NA	C1,5	NA	NA	NA	126	140
30	Abro, 2019⁵⁶	Pakistan, M	2005–2016	–	2	28,601	15.8	52.5 ± 11.3	8.2 ± 7.5	C1,2	NA	NA	NA	NA	NA
31	Sultan, 2019⁵⁷	Pakistan, M	2017	–	2	709	17.5	49.93 ± 12.51	9.01 ± 7.71	C5	NA	NA	NA	NA	NA
32	Zia, 2016⁵⁸	Pakistan, M	2011–2012	–	2	678	0.56	51.81 ± 11.43	7.23 ± 6.75	NA	NA	NA	NA	NA	NA
33	El-Gendi, 2018⁵⁹	Egypt, H	2014–2016	–	1 & 2 [N]	67	62.7	57 ± 12.5	NA	C1,5	NA	NA	NA	NA	NA
		Sudan, L	2014–2016	–	1 & 2 [N]	86	26.7	51.8 ± 11.1	NA	C1,5	NA	NA	NA	NA	NA
		Yemen, L	2014–2016	–	1 & 2 [N]	56	87.5	52.5 ± 12	NA	C1,5	NA	NA	NA	NA	NA
34	Ahsan, 2015⁶⁰	Pakistan, M	2009–2010	–	2	366	27.3	48.5 ± 8.02	9.17 ± 6.51	C2	NA	NA	NA	NA	NA
35	Morsy, 2019⁶¹	Saudi Arabia, VH	2017	–	1 & 2 [N]	234	27.35	12-65	NA	C1	NA	NA	NA	NA	NA
36	Bamashmus, 2009⁶²	Yemen, L	2004	–	1 & 2 [N]	350	55	54.4 ± 11.8	9.9 ± 7.77	C1,5	NA	NA	45	60	77
37	Abdelfattah, 2014⁶³	Egypt, H	2012	–	1 & 2 [N]	71	52.11	54.53 ± 15.03	NA	NA	NA	NA	NA	NA	NA
38	Hyassat, 2014⁶⁴	Jordan, H	2011–2012	–	2	1,105	23	57.1 ± 10.3	5.1 ± SD?	NA	NA	NA	NA	NA	NA
39	Al-Otaiby, 2017⁶⁵	Saudi Arabia, VH	2015–2016	–	1 & 2 [N]	400	48.8	NA	NA	C1	NA	NA	NA	NA	NA
40	Al-Till, 2005⁶⁶	Jordan, H	NA	–	1 & 2 [N]	986	64.1	55.3 ± 12.5	11.9 ± 6.3	C1,2,5,6,7	NA	NA	NA	NA	NA
41	Khandekar, 2009⁶⁷	Oman, VH	2006	–	1 & 2 [N]	418	7.9	52.23 ± 12.51	NA	C5	NA	NA	NA	NA	NA
42	Kamaleldeen, 2018⁶⁸	Egypt, H	2012–2014	–	1	180	1.1	13.82 ± 3.23	6 ± 3.08	C1,2	NA	NA	NA	NA	NA
43	AL-Amir, 2008⁶⁹	Jordan, H	2006–2007	–	2	1,000	34.1	57.8 ± 9.9	9.6 ± 7.6	C1,5	121	71	53	96	78
44	Bamashmus, 2009⁷⁰	Yemen, L	2004	–	1 & 2 [N]	228	51.1	50.01 ± 12.0	NA	C1,5	NA	NA	NA	NA	NA
45	Costanion, 2014⁷¹	Lebanon, H	2008–2009	–	2	187	16.6	44.7 ± 14.9	NA	NA	NA	NA	NA	NA	NA
46	El Samahy, 2015⁷²	Egypt, H	2010–2013	–	1 & 2 [N]	600	1.83	13.29 ± 5.05	6.37 ± 3.64	C1	NA	NA	NA	NA	NA
47	Rahman KHan, 2014⁷³	Saudi Arabia, VH	2012–2013	–	2	506	2.96	57.44 ± SD?	10.2 ± 5.96	C1	6	7	NA	2	NA
48	El-Shafei, 2011⁷⁴	Qatar, VH	2009	–	1 & 2 [N]	540	23.5	≥40	12.88 ± 9.06	C1,2,5	NA	NA	NA	NA	NA
49	Kahloun, 2014⁷⁵	Tunisia, H	2007–2011	–	1 & 2 [N]	2,320	26.3	54.5 ± SD?	7.6 ± SD?	C1,2,5,6,7	530	280	251	156	402
50	Rabiu, 2015²¹	Jordan, H	NA	–	1 & 2 [N]	1,040	48.4	≥50	NA	C1	NA	NA	NA	NA	NA
51	Heydari, 2012⁷⁶	Iran, H	2008–2010	–	1 & 2 [N]	1,022	23.6	55.7 ± 12.2	6.85 ± SD?	C1,5	NA	NA	NA	NA	NA
52	Mehravar, 2016⁷⁷	Iran, H	2014	–	2	562	28.1	61.62 ± 10.49	12.82 ± 6.61	C1	NA	NA	NA	NA	NA
53	Khandekar, 2004⁷⁸	Oman, VH	NA	–	1 & 2 [N]	2,063	15.07	NA	NA	C1,5	NA	NA	NA	NA	NA
54	Rahman, 2011⁷⁹	Pakistan, M	NA	–	1 & 2 [N]	200	51	48.3 ± 13	8.5 ± 5.6	C1,4,5	NA	NA	NA	NA	NA
55	Wahab, 2008⁸⁰	Pakistan, M	2006	+	2	130	15	43.2 ± 10.2	0.5	C1	NA	NA	NA	NA	NA
56	Shera, 2004⁸¹	Pakistan, M	NA	–	2	500	43	55.2 ± 10.6	7 ± SD?	C1	NA	NA	NA	NA	NA
57	Al-Akily, 2011⁸²	Yemen, L	2001–2005	–	1 & 2 [N]	694	53	53.9 ± 11.52	10.3 ± 7.7	C1,3,4,5,6	NA	NA	NA	NA	NA
58	Iqbal, 2009⁸³	Pakistan, M	2005	+	2	100	9	47 ± SD?	0.5	C1	NA	NA	2	1	NA
59	Yasir, 2019⁸⁴	Saudi Arabia, VH	2014-2017	–	1 & 2 [N]	395	33.7	≥40	NA	C1,5,6	NA	NA	NA	NA	NA
60	Al-Rubeaan, 2015⁸⁵	Saudi Arabia, VH	NA	–	2	50,464	19.7	59.7 ± 12.78	13.4 ± 8.24	C1,4	9.1	NA	NA	5367	2880
61	Farasat, 2017⁸⁶	Pakistan, M	2010	+	2	200	33	50.69	0.5	C1	NA	NA	NA	NA	NA
62	Szabo, 2015⁸⁷	UAE, VH	2009–2011	–	2	150	6	58.3 ± 12.2	14.4 ± 7.7	NA	NA	NA	NA	NA	NA
63	Javadi, 2009⁸⁸	Iran, H	2007	–	1 & 2 [N]	634	37	58.16 ± 11.98	NA	C1,5	114	42	19	65	38
64	Al-Maskari, 2007⁸⁹	UAE, VH	2003–2004	–	1 & 2 [Y]	513	19	53.3 ± 13.01	NA	C2,5,7	NA	NA	NA	NA	NA
65	Al Kahtani, 2016⁹⁰	Saudi Arabia, VH	2000–2010	–	1 & 2 [Y]	64,351	17.5	55.92 ± 14.5	13.17 ± 8.05	NA	NA	NA	NA	6146	2914
66	Uddin, 2018⁹¹	Pakistan, M	2015–2016	+	2	891	15.9	47.7 ± 10.6	0.5	C1	NA	NA	NA	NA	NA
67	Khandekar, 2003⁹²	Oman, VH	2000–2001	–	1 & 2 [Y]	2,249	14.39	NA	NA	C1,5,7	NA	NA	NA	67	149
68	Nizamani, 2017⁹³	Pakistan, M	2014–2015	–	1 & 2 [N]	1,6760	17	>15	NA	C1,4	NA	NA	NA	NA	NA
69	Jelinek, 2017⁹⁴	UAE, VH	2014–2015	–	2	490	13.26	60 ± 11.3	NA	NA	NA	NA	NA	NA	NA
70	Akhter, 2017⁹⁵	Pakistan, M	2014–2015	–	1 & 2 [N]	876	7.8	53.1 ± 11.9	7.6 ± 7.1	NA	NA	NA	NA	NA	NA
71	Alfadda, 2006⁹⁶	Saudi Arabia, VH	2001–2003	–	2	99	25.3	56.6 ± 12	11.8 ± 7.7	NA	NA	NA	NA	NA	NA
72	Alwakeel, 2008⁹⁷	Saudi Arabia, VH	1989–2004	–	2	1,952	16.7	58.4 ± 14.2	10.4 ± 7.5	NA	NA	NA	NA	NA	NA
73	Ahmed, 2019⁹⁸	Sudan, L	2015	–	1 & 2 [N]	316	83.3	NA	NA	NA	NA	NA	NA	NA	NA
74	Awadalla, 2017⁹⁹	Sudan, L	NA	–	2	424	72.6	20-75	NA	NA	NA	NA	NA	NA	NA
75	Awadalla, 2017⁹⁹	Sudan, L	NA	–	2	316	51.6	58 ± 10	NA	NA	NA	NA	NA	NA	NA
76	Niroomand, 2016¹⁰⁰	Iran, H	2014	–	2	200	60.5	60.17 ± 13.56	13.06 ± SD?	NA	NA	NA	NA	NA	NA
77	Salti, 2009²²	Lebanon, H	2004–2007	–	2	557	35	56.4 ± 11.7	9.2 ± 6.9	C1,5,7	NA	NA	NA	45	42
78	Azizi-Soleiman, 2015¹⁰¹	Iran, H	2003–2014	–	2	1,429	56.3	NA	NA	C1,5,7	NA	NA	NA	NA	NA
79	Solaymani, 2012¹⁰²	Iran, H	2007–2008	–	2	140	36.42	53.49 ± 9.72	8.88 ± 6.06	C1,5,7	NA	NA	NA	8	35
80	Al-Ghamdi, 2012¹⁰³	Saudi Arabia, VH	NA	–	2	852	34.5	63.3 ± SD?	NA	C1,2	NA	NA	NA	NA	NA
81	Saadi, 2007¹⁰⁴	UAE, VH	2005–2006	–	2	245	54.2	>18	NA	C1	NA	NA	NA	NA	NA
82	Abdolghani, 2018¹⁰⁵	Saudi Arabia, VH	2015–2016	–	2	360	23.3	18-75	NA	NA	NA	NA	NA	NA	NA
83	Ghaem, 2018¹⁰⁶	Iran, H	2015–2016	–	1 & 2 [N]	478	32.8	56.64 ± 12.45	11.37 ± 9	NA	82	44	18	13	NA
84	Basit, 2005¹⁰⁷	Pakistan, M	1996–2001	–	2	2,199	15.9	NA	NA	C1	NA	NA	NA	NA	NA
85	Faghih-Amini, 2005¹⁰⁸	Iran, H	2004	–	1	500	76.4	49.59 ± SD?	NA	NA	NA	NA	NA	NA	NA
86	Shafiqur-Rahman, 2004¹⁰⁹	Pakistan, M	2002	NA	NA	185	55	48.3 ± 13.3	8.5 ± 5.6	C1	NA	NA	NA	NA	NA
87	Afghani, 2007¹¹⁰	Pakistan, M	1997–2001	+	NA	8,227	22.29	≥40	NA	C1	NA	NA	NA	NA	NA
88	Esteghamati, 2007¹¹¹	Iran, H	NA	–	2	66	36.4	57 ± 9.5	14.44 ± 6.78	NA	NA	NA	NA	NA	NA
89	Al-Adsani, 2007¹¹²	Kuwait, VH	2000–2005	–	2	165	40	48.99 ± 10.05	8.03 ± 7.04	C1,2	35	NA	NA	5	17
90	Askarishahi, 2012¹¹³	Iran, H	2008	–	2	459	40.7	55 ± 9.9	10.5 ± 6.4	C1,5	NA	NA	NA	NA	NA
91	Aamir, 2012¹¹⁴	Pakistan, M	2011	–	2	2,123	38.34	57.4 ± 22	NA	C1,2	NA	NA	NA	NA	NA
92	Bonakdaran, 2015¹¹⁵	Iran, H	NA	–	2	235	34.8	54.8 ± 9.4	7.52 ± 6.1	C1	NA	NA	NA	NA	NA
93	Dehghan, 2015¹¹⁶	Iran, H	NA	+	NA	529	29.6	54.11 ± 10.06	NA	C1,2,5	67	52	24	16	25
94	Najafi, 2013¹¹⁷	Iran, H	2011–2012	–	2	243	17.69	55.8 ± 10.33	9.08 ± 7.9	NA	NA	NA	NA	NA	NA
95	Amini, 2008¹¹⁸	Iran, H	2001–2004	+	2	710	9	48.8 ± 9.8	0.5	C1	NA	NA	NA	NA	NA
96	Hosseini, 2014¹¹⁹	Iran, H	2011–2012	–	2	305	35.7	53.9 ± 1	8.2 ± 7.1	C1	NA	NA	NA	NA	NA
97	AlamKhanzada, 2011¹²⁰	Pakistan, M	2009–2010	–	2	244	40.94	45 ± 11.5	13 ± 4.5	C1,4,5	NA	NA	NA	NA	NA
98	Manaviat, 2004¹²¹	Iran, H	2000–2001	–	2	590	39.7	54.9 ± 10.2	10.2 ± 6.6	C1,4,5,6	113	71	16	32	52
99	Manaviat, 2008¹²²	Iran, H	NA	–	2	199	70.35	54.16 ± 11.2	NA	C1,2,5	34	34	22	50	NA
100	Sohail, 2014¹²³	Pakistan, M	2009–2010	–	2	202	56.9	52.9 ± 10.5	8.5 ± 5.1	C1	NA	NA	NA	NA	NA
101	Khalid, 2015¹²⁴	Pakistan, M	2014–2015	–	2	340	17	47.55 ± 9.13	NA	C1,5	23	17	10	7	NA
102	Shaikh, 2010¹²⁵	Pakistan, M	2008–2010	–	2	200	25.5	38-70	NA	C1	NA	NA	NA	NA	NA
103	Hassan, 2010¹²⁶	Pakistan, M	2004–2005	–	2	500	41.4	NA	NA	NA	NA	NA	NA	NA	NA
104	Rasoulinejad, 2015¹²⁷	Iran, H	2006–2010	–	1 & 2 [N]	1,562	64.1	54.6 ± 10.6	9.6 ± 7	C5	NA	NA	NA	NA	NA
105	Macky, 2011¹²⁸	Egypt, H	2007–2008	–	1 & 2 [Y]	1,325	20.5	49 ± 12.9	NA	C1,5,6	NA	NA	NA	NA	NA
106	Hussain, 2011¹²⁹	Pakistan, M	2008–2009	–	1 & 2 [Y]	1,524	12	20–70	NA	C1,3,5,6	NA	NA	NA	NA	NA
107	Janghorbani, 2017¹³⁰	Iran, H	2001–2004	–	2	1,566	36.46	50.6 ± 12.3	7.6 ± 6.9	C1,2	NA	NA	NA	NA	NA
108	Jsnghorbani, 2006¹³¹	Iran, H	2000–2003	–	2	810	33.38	52.7 ± 9.9	8.2 ± 6.8	C2	NA	NA	NA	NA	NA
109	Khazaei, 2010¹³²	Iran, H	2002	+	2	200	11	NA	NA	C1	NA	NA	NA	NA	NA

Codes [1]: VH (very high); H (high); M (medium); L (low).

Codes [2]: C1 (Dilated fundus examination (ophthalmoscopy)); C2 (Retinal photography); C3 (Digital stereoscopic retinal imaging); C4 (Angiography); C5 (Slit lamp biomicroscopy); C6 (Visual acuity); C7 (Tonometry).

Codes [3]: D (diagnosed diabetes); nD (newly diagnosed diabetes).

Codes [4]: [Y] (P _DR reported for both type I and II diabetes, separately); [N] (P _DR not reported for both type I and II diabetes, separately).

Abbreviations: NPDR, non-proliferative diabetic retinopathy; PDR, proliferative diabetic retinopathy; ME, macular edema; UDDM, undiagnosed diabetes; SD, standard deviation.

Results of the meta-analysis

Heterogeneity

The output of heterogeneity analysis showed that tau² was 0.05 (95% CI = 0.04, 0.06), I² was 99.77% (95% CI = 99.7, 99.83), and the Q-statistic was 13,537.27 (p < 0.0001), all of which suggested a high heterogeneity in the effect sizes. Additionally, the high value of I² indicated that almost all heterogeneity was related to the between-study variance (Figure 2).

Figure 2.

Forest plot of 109 studies.

Figure 2.

Continued.

Prevalence of retinopathy in diabetes

We found that the summary proportion was 0.31 (95% CI = 0.28, 0.33), which represented a 31% prevalence of diabetic retinopathy (Figure 2).

Prevalence of retinopathy in diabetes based on subgroup analysis by HDI

Low HDI countries and very high HDI countries had the highest and lowest diabetic retinopathy prevalence. Moreover, the recalculated prevalence of retinopathy was 0.254 (95% CI = 0.238, 0.270). In subgroup analysis by HDI, the summary effect proportions were 0.636 (95% CI = 0.524, 0.740), 0.240 (95% CI = 0.211, 0.269), 0.339 (95% CI = 0.292, 0.388), and 0.226 (95% CI = 0.205, 0.247) for the four subgroups (low, medium, high, and very high), respectively. As a nature of our analysis (separate random-effects models in each subgroup), within-group estimates of tau² were 0.029 [Q (df = 8) = 280.461, p < 0.001], 0.008 [Q (df = 28) = 2231.918, p < 0.001], 0.029 [Q (df = 43) = 5009.601, p < 0.001], and 0.004 [Q (df = 28) = 1305.489, p < 0.001] for low, medium, high, and very high subgroups, respectively. We found that the difference between the four subgroup summary estimates was significant (QM (df = 3) = 0.45, p < 0.001), and HDI had a moderating effect on the prevalence of diabetic retinopathy and shared effect on the true heterogeneity in the proportion.

Results of the meta-regression

The meta-regression analysis was performed for three different variables, including HDI, publication year, and the mean duration of diagnosed diabetes.

The slope of the estimated regression line suggested that HDI had a significant negative moderating effect on the prevalence of retinopathy in diabetes (results of the test of modulators: [QM (df = 1) = 27.016, p < 0.0001]; slope coefficient: [−0.069, Z = −5.198, p < 0.0001]) (Figure 3).

Figure 3.

The scatter plot of HDI and the effect sizes [Note for interpretation: Each study was represented by a circle with a size proportional to the study size.]

The slope of the estimated regression line for publication year was almost horizontal, suggesting that it was not a significant modulator of the prevalence of retinopathy in diabetes (results of the test of modulators: [QM (df = 1) = 0.184, p = 0.6679]; slope coefficient: [0.001, Z = 0.429, p = 0.668]) (Figure 4).

Figure 4.

The scatter plot of publication year and the effect sizes [Note for interpretation: Each study was represented by a circle with a size proportional to the study size.]

The slope of the estimated regression line for the mean duration of diagnosed diabetes suggested that it had a significant positive moderating effect on the prevalence of retinopathy in diabetes (results of the test of modulators: [QM (df = 1) = 19.752, p < 0.0001]; slope coefficient: [0.019, Z = 4.444, p < 0.0001]) (Figure 5).

Figure 5.

The scatter plot of the mean duration of diagnosed diabetes and the effect sizes [Note for interpretation: Each study was represented by a circle with a size proportional to the study size.]

Importantly, in all meta-regression plots, most studies were outside the 95% CI boundaries, indicating the presence of unknown or missed parameters affecting the prevalence of retinopathy in diabetes. A zero-to-negligible value of R², which represents the amount of between-study heterogeneity explained by a modulator, supported this claim (R²_HDI = 0.00, R²_{publication year} = 1.33%, R²_{mean duration of diagnosed diabetes =}0.00).

Publication bias

Visual inspection of the funnel plot of proportions against sample sizes showed that our data were asymmetrical (Figure 6). Additionally, Egger’s test showed that the funnel plot was significantly asymmetrical (Z = 2.321, p = 0.020). Furthermore, the funnel plot of proportions against sample sizes showed that a small-study effect was present in our meta-analysis (Appendix 10). However, the rank correlation test did not find any association between the sample size and the reported prevalence of diabetic retinopathy of each study (Kendall’s tau = 0.057, p = 0.375).

Figure 6.

The funnel plot of effect size against standard error [Note for interpretation: Each dot denotes a study, the vertical line denotes the summary effect size, and the two limit lines denote the 95% confidence intervals of the summary effect size.]

Discussion

To our knowledge, this is the first meta-analysis on the prevalence of diabetic retinopathy, irrespective of the type of diabetes, in the EMR, including 109 population-based studies. Most studies included in the meta-analysis were from Iran (28 articles) and Pakistan (28 articles), followed by Saudi Arabia (18 articles), while we could not find any publication that matched our inclusion criteria on the prevalence of diabetic retinopathy from Afghanistan, Bahrain, Iraq, Syria, Somalia, Morocco, Palestine, Djibouti, and Libya. Based on the analysis, the high between-study heterogeneity in this study might indicate a regional difference in the prevalence of diabetic retinopathy in the EMR. In other words, the effectiveness of health surveillance and early detection in these countries vary.

On the basis of the data from 109 studies and approximately 280,000 participants with diabetes, the prevalence of diabetic retinopathy was estimated to be 31% in the EMR, which was higher than the global 25.2% estimation reported by IDF in 2019¹³⁴ and the 22.27% reported in another meta-analysis in 2021.¹³⁵ Furthermore, although the regional classifications by WHO (EMR) and IDF (MENA) are different despite a large overlap, our estimation was comparable to the 33.8% and 32.90% in MENA reported by the above-mentioned studies, respectively.^134,135 However, these estimations did not yield a weighted (according to the country population proportions) summary prevalence of diabetic retinopathy and might be underestimated.

Based on subgroup analysis and meta-regression, HDI was negatively correlated with the prevalence of diabetic retinopathy. The very high HDI countries in the EMR, all of which were “Gulf Cooperation Council (GCC)” countries, had the lowest diabetic retinopathy prevalence rate in the EMR of 22.6%, which is similar to the estimations from Europe (18.75%) and the Western Pacific (19.20%), lower than those from North America and the Caribbean (33.30%) and Africa (35.90%), and higher than those from South East Asia (16.99%) and South and Central America (13.37%).¹³⁴ In a low-income developing country with a poor healthcare system (i.e., screening and diabetes care), the risk of retinopathy would be higher in patients with diabetes. Another, perhaps counter-intuitive, point worth mentioning is that the summary proportion in the medium HDI subgroup was higher than that of the high HDI subgroup. One possible explanation may be that Pakistan was the only member in our medium HDI subgroup; therefore, we should consider the situation of the healthcare system and delivery in Pakistan. Public health resources in Pakistan are mostly located in urban regions, which provide a better quality of life in general for their citizens. In addition, owing to the cost associated with poor transportation systems, most of the rural population cannot go to these public health centers.^136,137 Moreover, the majority of included studies sampled the urban community, which may influence the prevalence of diabetic retinopathy obtained for this category.

The results of meta-regression did not show a statistically significant association between the publication year and prevalence of diabetic retinopathy in the EMR. Thus, the year of study was not a cause of variability in the results. Indeed, publication year cannot properly represent the exact prevalence trend.¹³⁸ The regression line is fitted on the pooled data from different countries in each publication year, which can severely introduce selection bias as this is not longitudinal, and the regression line is the result of a sum of data from variable numbers of studies from different sets of countries at each publication year. However, if we consider the publication year as a relative indicator of changes in diabetic retinopathy prevalence in the EMR, one can interpret that this apparently stable trend during the past 20 years in the EMR might imply an interplay between various opposing factors that has ultimately kept the retinopathy rate constant in the EMR. For example, although GCC countries have made progress in recent years and developed their healthcare systems, the rate of diabetes is noticeable because of the several fundamental risk factors of diabetic retinopathy, including rapid industrialization and globalization, sedentary lifestyle, and dramatically decreased physical activity levels.¹³⁹ Additionally, several EMR countries have encountered serious economic and political issues because of warfare, sanctions, and refugees, which have drastically compromised the healthcare system.

Another remarkable and important point is that although the meta-regression plots demonstrated correlations of HDI, publication year, and diabetes duration with diabetic retinopathy, most studies were outside of 95% CI boundaries in all three plots. This result indicated the presence of several unknown and missed parameters that define the prevalence of diabetic retinopathy in a region and could not be considered because of the nature of our study.

It is worth noting that the asymmetry in the publication bias assessment might not necessarily indicate publication bias as other parameters that interfere with the inclusion of small studies may contribute to this asymmetry in observational studies.¹⁴⁰ First, we previously showed a high between-study heterogeneity, and a substantial number of studies fell outside of the two limit lines in the forest plot, which confirmed the high heterogeneity. In other words, this high between-study heterogeneity might be due to particular reasons. Second, we excluded small studies in foreign languages, which may have resulted in the so-called English language bias. Third, irrespective of the sensitive search strategy, gray literature search, and manual search in references for relevant studies, citation bias might have been present.

Several studies in the EMR showed a high prevalence of undiagnosed diabetes.^138,141,142 This is important because when treatment starts immediately, especially in the pre-diabetes stage of type 2 diabetes, the risk of diabetes complications decreases. These have implications for our study. In particular, most of the included studies in this meta-analysis were carried out on different sample populations of known type 2 diabetes cases. Therefore, this meta-analysis might have underestimated the prevalence of diabetic retinopathy in the EMR. Moreover, we showed that the longer the duration of diabetes, the higher the prevalence of diabetic retinopathy. The duration of diabetes is a major risk factor in developing diabetic retinopathy.¹⁴³ Furthermore, the development of diabetic retinopathy is related to uncontrolled conditions, such as glycemic control, systolic hypertension, and dyslipidemia, which are prevalent in the EMR.^144,145 For example, the prevalence of uncontrolled diabetes is high (about 60%) among patients with diabetes in the EMR.^13,146 Taking these challenges into account, addressing the healthcare burden of this group would be difficult. In particular, although diabetic retinopathy is a well-known complication with comprehensive and universal identification and control protocols, financial barriers, insufficient health system services (all three levels), and limited skilled practitioners in most countries of the EMR are obstacles for the active and efficient follow-up of all patient populations and communications and consultations to make patients with diabetes aware of the importance of annual check-ups and follow-up protocols even at asymptomatic phases.

Conclusion

Our study provided the first pooled analysis to estimate the prevalence of diabetic retinopathy in the EMR. On the basis of the data from 109 studies and approximately 280,000 participants with diabetes, the prevalence of diabetic retinopathy was estimated to be high as 31% in the EMR. We showed that a longer duration of diagnosed diabetes and worse healthcare systems (using HDI as its proxy) were correlated with a higher rate of diabetic retinopathy. Our results implicate the importance of diabetes screening, periodic examinations for retinopathy, diabetes care, and risk factor controls.

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Footnotes

Declaration of conflicting interest

The authors declare that they have no known competing financial interests or personal relationships that could have appeared to influence the work reported in this paper.

Funding

The authors disclosed receipt of the following financial support for the research, authorship, and/or publication of this article: The present article was financially supported by the Shiraz University of Medical Sciences [grant number 19293-109-01-97].

Author contributions

All authors conceived the study and were responsible for designing the protocol. AH, MA, and AM designed the study. SS performed the literature search and, together with SPA and SD, selected the studies and extracted the relevant information. All authors synthesized the data. AH and SPA wrote the first draft of the paper. AH, AM, and MA provided critical guidance on the analysis and overall direction of the study. All authors critically revised successive drafts of the paper and approved the final version.

ORCID iDs

Alireza Heiran

Seyede Pegah Azarchehry

Mehrdad Afarid

Sonia Shaabani

Alireza Mirahmadizadeh

References

International Diabetes Federation. IDF Diabetes Atlas, 10th edn. Brussels, Belgium: 2021. Available at: https://www.diabetesatlas.org

Chow

Foster

Gonzalez

, et al. The disparate impact of diabetes on racial/ethnic minority populations. Clin Diabetes 2012; 30: 130–133.

Bourne

RRA

Stevens

White

, et al. Causes of vision loss worldwide, 1990-2010: A systematic analysis. Lancet Glob Heal 2013; 1: e339–e349.

Klein

BEK

Moss

, et al. The Wisconsin Epidemiologic Study of Diabetic Retinopathy. II. Prevalence and risk of diabetic retinopathy when age at diagnosis is less than 30 years. Arch Ophthalmol 1984; 102: 520–526.

Klein

BEK

Moss

, 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.

McKay

McCarty

Taylor

HR.

Diabetic retinopathy in Victoria, Australia: the visual impairment project. Br J Ophthalmol 2000; 84: 865–870.

Henricsson

Nyström

Blohmé

, et al. The incidence of retinopathy 10 years after diagnosis in young adult people with diabetes: Results from the nationwide population-based Diabetes Incidence Study in Sweden (DISS). Diabetes Care 2003; 26: 349–354.

Kohner

Aldington

Stratton

, et al. United kingdom prospective diabetes study, 30: Diabetic retinopathy at diagnosis of non-insulin-dependent diabetes mellitus and associated risk factors. Arch Ophthalmol 1998; 116: 297–303.

Gallego

Craig

Hing

, et al. Role of blood pressure in development of early retinopathy in adolescents with type 1 diabetes: Prospective cohort study. Bmj 2008; 337: 497–500.

10.

World Health Organization Regional Office for the Eastern Mediterranean. The Work of WHO in the Eastern Mediterranean Region Annual Report of the Regional Director. 2014. Available from: http://applications.emro.who.int/dsaf/EMROPUB_2016_EN_1817.pdf?ua=1&ua=1

11.

WorldHealthOrganization. VIH/SIDA differences entre hommes et femmes dans la Region de la Mediterranee orientale. 2005.

12.

Kuper

Polack

Limburg

Rapid assessment of avoidable blindness. Community Eye Heal J 2006; 19: 68–69.

13.

Lin

Pan

, et al. Global, regional, and national burden and trend of diabetes in 195 countries and territories: an analysis from 1990 to 2025. Sci Rep 2020; 10; 14790.

14.

Mirzaei

Rahmaninan

Mirzaei

, et al. Epidemiology of diabetes mellitus, pre-diabetes, undiagnosed and uncontrolled diabetes in Central Iran: Results from Yazd health study. BMC Public Health 2020; 20: 166.

15.

Meo

SA.

Prevalence and future prediction of type 2 diabetes mellitus in the kingdom of saudi arabia: A systematic review of published studies. J Pak Med Assoc 2016; 66: 722–725.

16.

Alhyas

McKay

Majeed

Prevalence of type 2 diabetes in the states of the co-operation council for the Arab states of the Gulf: A systematic review. PLoS One 2012; 7: e40948. Epub ahead of print.

17.

Mumtaz

Fahim

Arslan

, et al . Prevalence of diabetic retinopathy in Pakistan: A systematic review. Pakistan J Med Sci 2018; 34: 493–500.

18.

Mohammadi

Raiegani

AAV

Jalali

, et al. The prevalence of retinopathy among type 2 diabetic patients in Iran: A systematic review and meta-analysis. Rev Endocr Metab Disord 2019; 20: 79–88.

19.

Hajar

Hazmi

A Al

Wasli

, et al. Prevalence and causes of blindness and diabetic retinopathy in southern Saudi Arabia. Saudi Med J 2015; 36: 449–455.

20.

Ahmed

Khalil

Al-Qahtani

Diabetic retinopathy and the associated risk factors in diabetes type 2 patients in Abha, Saudi Arabia.

J Fam Community Med 2016; 23: 18–24.

21.

Al-Shammari

Al-meraghi

Nasif

, et al. The prevalence of diabetic retinopathy and associated risk factors in type 2 diabetes mellitus in Al-Naeem area (Kuwait). Middle East J Fam Med 2005; 3: 3.

22.

Rabiu

Al Bdour

Abu Ameerh

, et al. Prevalence of blindness and diabetic retinopathy in northern Jordan. Eur J Ophthalmol 2015; 25: 320–327.

23.

Salti

Nasrallah

Taleb

, et al. Prevalence and determinants of retinopathy in a cohort of Lebanese type II diabetic patients. Can J Ophthalmol 2009; 44: 308–313.

24.

Page

Moher

Bossuyt

, et al. PRISMA 2020 explanation and elaboration: updated guidance and exemplars for reporting systematic reviews. BMJ 2021; 372: n160.

25.

Joanna Briggs Institute. Critical Appraisal Tools: Checklist for Systematic Reviews [Internet]. 2017 [cited 2019 December 15]. Available from: http://joannabriggs.org/assets/docs/critical-appraisal-tools/JBI_Critical_Appraisal-Checklist_for_Systematic_Reviews2017.pdf

26.

Viechtbauer

Conducting meta-analyses in R with the metafor. J Stat Softw 2010; 36: 1–48.

27.

Balduzzi

Rücker

Schwarzer

How to perform a meta-analysis with R: A practical tutorial.

Evid Based Ment Health 2019; 22: 153–160.

28.

Wang

NMA.

How to Conduct a Meta-Analysis of Proportions in R: A Comprehensive Tutorial. Texas, USA: CUNY. Epub ahead of print 2018. DOI: 10.13140/RG.2.2.27199.00161.

29.

UNITEDNATIONSDEVELOPMENTPROGRAMME. Human Development Index (HDI) [Internet]. 2020, http://hdr.undp.org/en/content/human-development-index-hdi (2018, accessed 1 August 2020).

30.

Khandekar

Mohammed

AJ.

Visual disabilities among diabetics in Oman. Saudi Med J 2005; 26: 836–841.

31.

Jamal u

Qureshi

Khan

, et al. Prevalence of diabetic retinopathy among individuals screened positive for diabetes in five community-based eye camps in northern Karachi, Pakistan. J Ayub Med Coll Abbottabad 2006; 18: 40–43.

32.

Ishaq

Ali

Kazmi

, et al. Prevalence of diabetic retinopathy in type II diabetic patients in a health facility in Karachi, Pakistan. Trop J Pharm Res 2016; 15: 1069–1076.

33.

Taleb

Salti

Al-Mokaddam

, et al. Vascular complications of diabetes in Lebanon: Experience at the American University of Beirut. Br J Diabetes Vasc Dis 2008; 8: 80–83.

34.

Harb

Chamoun

, et al. Severity of diabetic retinopathy at the first ophthalmological examination in the Lebanese population. Ther Adv Ophthalmol 2018; 10: 251584141879195.

35.

Shaikh

, et al . Prevalence of diabetic retinopathy and influence factors among newly diagnosed diabetics in rural and urban areas of Pakistan: Data analysis from the Pakistan National Blindness & Visual Impairment Survey 2003. Pakistan J Med Sci 2008; 24: 774–779.

36.

Alaboud

Tourkmani

Alharbi

, et al. Microvascular and macrovascular complications of type 2 diabetic mellitus in Central,Kingdom of Saudi Arabia. Saudi Med J 2016; 37: 1399–1403.

37.

Al-Agha

Alafif

Abd-Elhameed

IA.

Glycemic control, Complications, and associated autoimmune diseases in children and adolescents with type 1 diabetes in Jeddah, Saudi Arabia.

Saudi Med J 2015; 36: 26–31.

38.

Esteghamati

Larijani

Aghajani

, et al. Diabetes in Iran: Prospective analysis from first nationwide diabetes report of National Program for Prevention and Control of Diabetes (NPPCD-2016). Sci Rep 2017; 7: 13461.

39.

Alvi

Memon

Shera

, et al . Visual outcome of laser treatment in diabetic macular edema: Study from an urban diabetes care center. Pakistan J Med Sci 2016; 32: 1229–1233.

40.

Ali

Iqbal

Taj

, et al. Prevalence of microvascular complications in newly diagnosed patients with type 2 diabetes. Pakistan J Med Sci 2013; 29: 899–902.

41.

Memon

Ahsan

Riaz

, et al. Frequency, severity and risk indicators of retinopathy in patients with diabetes screened by fundus photographs: A study from primary health care. Pakistan J Med Sci 2014; 30: 366–372.

42.

Javanbakht

Abolhasani

Mashayekhi

, et al. Health Related Quality of Life in Patients with Type 2 Diabetes Mellitus in Iran: A National Survey. PLoS One 2012; 7: e44526. Epub ahead of print. DOI: 10.1371/journal.pone.0044526.

43.

Hussain

Qamar

Iqbal

, et al. Risk factors of retinopathy in type 2 diabetes mellitus at a tertiary care hospital, Bahawalpur Pakistan. Pakistan J Med Sci 2013; 29: 536–539. Epub ahead of print. DOI: 10.12669/pjms.292.3066.

44.

Valizadeh

Moosazadeh

Bahaadini

, et al. Determining the Prevalence of Retinopathy and Its Related Factors among Patients with Type 2 Diabetes in Kerman, Iran. Osong Public Heal Res Perspect 2016; 7: 296–300.

45.

Janghorbani

Amini

Ghanbari

, et al. Incidence of and risk factors for diabetic retinopathy in Isfahan, Iran. Ophthalmic Epidemiol 2003; 10: 81–95.

46.

Khandekar

Al Hassan

Al Dhibi

, et al. Magnitude and determinants of diabetic retinopathy among persons with diabetes registered at employee health department of a tertiary Eye Hospital of central Saudi Arabia. Oman J Ophthalmol 2015; 8: 162–165.

47.

Al-Zuabi

Al-Tammar

Al-Moataz

, et al. Retinopathy in newly diagnosed type 2 diabetes mellitus. Med Princ Pract 2005; 14: 293–296.

48.

Safi

Ahmadieh

Katibeh

, et al. Modeling a Telemedicine Screening Program for Diabetic Retinopathy in Iran and Implementing a Pilot Project in Tehran Suburb. J Ophthalmol 2019; 19: 1–8.

49.

Khan

Wiseberg

Lateef

, et al. Prevalence and determinants of diabetic retinopathy in Al Hasa region of Saudi Arabia: primary health care centre based cross-sectional survey, 2007-2009. Middle East Afr J Ophthalmol 2010; 17: 257.

50.

Mehanna

Fattah

Tamim

, et al. Five-year incidence and progression of diabetic retinopathy in patients with type II diabetes in a tertiary care center in Lebanon. J Ophthalmol 2017; 2017: 9805145.

51.

Katibeh, MH. Dehghan, H. Ahmadieh, R, et al. Prevalence and Risk Factors for Diabetic Retinopathy in Yazd, Iran. J Diabetes 2014; 7: 139–41.

52.

Aidenloo

Mehdizadeh

Valizadeh

, et al. Optimal glycemic and hemoglobin a1c thresholds for diagnosing diabetes based on prevalence of retinopathy in an iranian population. Iran Red Crescent Med J 2016; 18: e31254. Epub ahead of print. DOI: 10.5812/ircmj.31254.

53.

Jammal

Khader

Alkhatib

, et al. Diabetic retinopathy in patients with newly diagnosed type 2 diabetes mellitus in Jordan: Prevalence and associated factors. J Diabetes 2013; 5: 172–179.

54.

Galvez-Ruiz

Schatz

Prevalence of Diabetic Retinopathy in a Population of Diabetics From the Middle East With Microvascular Ocular Motor Palsies.

J Neuroophthalmol 2016; 36: 131–133.

55.

Ageely

Long-term diabetes-related severe complications among individuals with T2DM in Jazan, Saudi Arabia. J Acute Dis 2019; 8: 72–77.

56.

Elwali

Almobarak

Hassan

, et al . Frequency of diabetic retinopathy and associated risk factors in Khartoum, Sudan: Population based study. Int J Ophthalmol 2017; 10: 948–954.

57.

Abro

Zafar

Fawwad

, et al. Prevalence of diabetic micro vascular complications at a tertiary care unit of Karachi, Pakistan. Int J Diabetes Dev Ctries 2019; 39: 325–330.

58.

Sultan

Fawwad

Siyal

, et al. Frequency and risk factors of diabetic retinopathy in patients with type 2 diabetes presenting at a tertiary care hospital. Int J Diabetes Dev Ctries 2019; 40; 87–92. Epub ahead of print. DOI: 10.1007/s13410-019-00756-9.

59.

Zia

Bhatti

Jalil

, et al. Prevalence of type 2 diabetes–associated complications in Pakistan. Int J Diabetes Dev Ctries 2016; 36: 179–188.

60.

Samy El Gendy

Abdel-Kader

AA.

Prevalence of Selected Eye Diseases Using Data Harvested from Ophthalmic Checkup Examination of a Cohort of Two Thousand Middle Eastern and North African Subjects. J Ophthalmol 2018; 2018: 8049475.

61.

Ahsan

Basit

Ahmed

, et al. Risk indicators of diabetic retinopathy in patients with type 2 diabetes screened by fundus photographs: a study from Pakistan. Int J Diabetes Dev Ctries 2015; 35: 333–338.

62.

Elmorsy

Posterior segment eye diseases: prevalence, pattern, and attribution to visual impairment among adult saudi population. Ann Clin Anal Med 2019; 10: 505–509.

63.

Bamashmus

Gunaid

Khandekar

Diabetic retinopathy, visual impairment and ocular status among patients with diabetes mellitus in Yemen: A hospital-based study.

Indian J Ophthalmol 2009; 57: 293–298.

64.

Abdelfattah

Amgad

Salama

, et al. Development of an Arabic version of the National Eye Institute Visual Function Questionnaire as a tool to study eye diseases patients in Egypt. Int J Ophthalmol 2014; 7: 891–897.

65.

Hyassat

Al Sitri

Batieha

, et al. Prevalence of hypomagnesaemia among obese type 2 diabetic patients attending the National Center for Diabetes, Endocrinology and Genetics (NCDEG). Int J Endocrinol Metab 2014; 12: e17796. Epub ahead of print. DOI: 10.5812/ijem.17796.

66.

Al-Otaibi

Khandekar

, et al. Validity, usefulness and cost of RETeval system for diabetic retinopathy screening. Transl Vis Sci Technol 2017; 6: 3. Epub ahead of print. DOI: 10.1167/tvst.6.3.3.

67.

Al-Till

Al-Bdour

Ajlouni

KM.

Prevalence of blindness and visual impairment among Jordanian diabetics.

Eur J Ophthalmol 2005; 15: 62–68.

68.

Khandekar

Tirumurthy

Al-Harby

, et al. Diabetic retinopathy and ocular co-morbidities among persons with diabetes at sumail hospital of Oman. Diabetes Technol Ther 2009; 11: 675–679.

69.

Kamaleldeen

Mohammad

Mohamed

, et al. Microvascular complications in children and adolescents with type 1 diabetes mellitus in Assiut governorate, Egypt. Egypt Pediatr Assoc Gaz 2018; 66: 85–90.

70.

Al-Amer

Khader

Malas

, et al. Prevalence and risk factors of diabetic retinopathy among Jordanian patients with type 2 diabetes. Digit J Ophthalmol 2008; 14: 42–49.

71.

Bamashmus

Gunaid

Khandekar

Regular visits to a diabetes clinic were associated with lower magnitude of visual disability and diabetic retinopathy - A hospital-based historical cohort study in Yemen.

Diabetes Technol Ther 2009; 11: 45–50.

72.

Costanian

Bennett

Hwalla

, et al. Prevalence, correlates and management of type 2 diabetes mellitus in Lebanon: Findings from a national population-based study. Diabetes Res Clin Pract 2014; 105: 408–415.

73.

El Samahy

Elbarbary

Elmorsi

HM.

Current status of diabetes management, glycemic control and complications in children and adolescents with diabetes in Egypt. Where do we stand now? And where do we go from here?

Diabetes Res Clin Pract 2015; 107: 370–376.

74.

Khan

Al Abdul Lateef

Fatima

, et al. Prevalence of chronic complication among type 2 diabetics attending primary health care centers of Al Ahsa district of Saudi Arabia: a cross sectional survey. Glob J Health Sci 2014; 6: 245–253.

75.

Elshafei

Gamra

Khandekar

, et al. Prevalence and determinants of diabetic retinopathy among persons ≥40 years of age with diabetes in Qatar: A community-based survey. Eur J Ophthalmol 2011; 21: 39–47.

76.

Kahloun

Jelliti

Zaouali

, et al. Prevalence and causes of visual impairment in diabetic patients in Tunisia, North Africa. Eye 2014; 28: 986–991.

77.

Heydari

Yaghoubi

, et al. Prevalence and risk factors for diabetic retinopathy: An Iranian eye study. Eur J Ophthalmol 2012; 22: 393–397.

78.

Mehravar

Mansournia

Holakouie-Naieni

, et al. Associations between diabetes self-management and microvascular complications in patients with type 2 diabetes. Epidemiol Health 2016; 38: e2016004.

79.

Khandekar

Zutshi

Glaucoma among Omani diabetic patients: A cross-sectional descriptive study (Oman Diabetic Eye Study 2002). Eur J Ophthalmol 2004; 14: 19–25.

80.

Rahman

Nawaz

Khan

, et al . Frequency of diabetic retinopathy in hypertensive diabetic patients in a tertiary care hospital of Peshawar, Pakistan. J Ayub Med Coll Abbottabad 2011; 23: 133–135.

81.

Wahab

Mahmood

Shaikh

, et al. Frequency of retinopathy in newly diagnosed type 2 diabetes patients. J Pak Med Assoc 2008; 58: 557–561.

82.

Shera

Jawad

Maqsood

, et al. Prevalence of Chronic Complications and Associated Factors in Type 2 Diabetes. J Pak Med Assoc 2004; 54: 54–59.

83.

Al-Akily

Bamashmus

Gunaid

AA.

Causes of visual impairment and blindness among Yemenis with diabetes: A hospital-based study.

East Mediterr Heal J 2011; 17: 831–837.

84.

Iqbal

Zafar

Frequency of retinopathy in newly diagnosed type 2 diabetes mellitus. Rawal Med J 2009; 34: 167–169.

85.

Yasir

Hassan

Rajiv

Diabetic retinopathy (DR) among 40 years and older Saudi population with diabetes in Riyadh governorate, Saudi Arabia – A population based survey. Saudi J Ophthalmol 2019; 33: 363–368.

86.

Al-Rubeaan

Abu El-Asrar

Youssef

, et al. Diabetic retinopathy and its risk factors in a society with a type 2 diabetes epidemic: A Saudi National Diabetes Registry-based study. Acta Ophthalmol 2015; 93: e140–e147.

87.

Farasat

Sharif

Manzoor

, et al. Prevalence of retinopathy detected by fundoscopy among newly diagnosed type 2 diabetic patients visiting a local hospital in Lahore. Pak J Zool 2017; 49: 367–372.

88.

Szabo

Osenenko

Qatami

, et al. Quality of care for patients with type 2 diabetes mellitus in Dubai: A HEDIS-like assessment. Int J Endocrinol 2015; 2015: 1–8.

89.

Javadi

Katibeh

Rafati

, et al. Prevalence of diabetic retinopathy in Tehran province: A population-based study. BMC Ophthalmol 2009; 9: 12–19.

90.

Al-Maskari

El-Sadig

Prevalence of diabetic retinopathy in the United Arab Emirates: A cross-sectional survey. BMC Ophthalmol 2007; 7: 11–18.

91.

Al Kahtani

Khandekar

Al-Rubeaan

, et al. Assessment of the prevalence and risk factors of ophthalmoplegia among diabetic patients in a large national diabetes registry cohort. BMC Ophthalmol; 16. Epub ahead of print 2016. DOI: 10.1186/s12886-016-0272-7.

92.

Uddin

Ali

Junaid

Prevalence Of Diabetic Complications In Newly Diagnosed Type 2 Diabetes Patients In Pakistan: Findings From National Registry. J Ayub Med Coll Abbottabad 2018; 30: S652–S658.

93.

Khandekar

Lawatii

J Al

Mohammed

, et al. Diabetic retinopathy in Oman: A hospital based study. Br J Ophthalmol 2003; 87: 1061–1064.

94.

Nizamani

Talpur

Awan

, et al. Results of a community-based screening programme for diabetic retinopathy and childhood blindness in district Hyderabad, Pakistan. BMJ Open Ophthalmol 2017; 2: e000099.

95.

Jelinek

Osman

Khandoker

, et al. Clinical profiles, comorbidities and complications of type 2 diabetes mellitus in patients from United Arab Emirates. BMJ Open Diabetes Res Care 2017; 5: e000427. Epub ahead of print. DOI: 10.1136/bmjdrc-2017-000427.

96.

Akhter

Ahmed

Mawani

, et al. Patterns, control and complications of diabetes from a hospital based registry established in a low income country. BMC Endocr Disord 2017; 17: 30. Epub ahead of print. DOI: 10.1186/s12902-017-0179-1.

97.

Alfadda

Abdulrahman

KB.

Assessment of care for type 2 diabetic patients at the primary care clinics of a referral hospital. J Family Community Med 2006; 13: 13–138.

98.

Alwakeel

Sulimani

Al-Asaad

, et al. Diabetes complications in 1952 type 2 diabetes mellitus patients managed in a single institution. Ann Saudi Med 2008; 28: 260–266.

99.

Ahmed

Awadalla

Osman

, et al. Ethnicity and diabetes complications in Sudanese population: The need for further genetic population testing. Diabetes Metab Syndr Clin Res Rev 2019; 13: 430–433.

100.

Awadalla

Noor

Elmadhoun

, et al. Diabetes complications in Sudanese individuals with type 2 diabetes: Overlooked problems in sub-Saharan Africa? Diabetes Metab Syndr Clin Res Rev 2017; 11: S1047–S1051.

101.

Niroomand

Ghasemi

Karimi-Sari

, et al. Diabetes knowledge, attitude and practice (KAP) study among Iranian in-patients with type-2 diabetes: A cross-sectional study. Diabetes Metab Syndr Clin Res Rev 2016; 10: S114–S119.

102.

Azizi-Soleiman

Heidari-Beni

Ambler

, et al. Iranian Risk Model as a Predictive Tool for Retinopathy in Patients with Type 2 Diabetes. Can J Diabetes 2015; 39: 358–363.

103.

Soleymani

Moazezi

Gorjizadeh

Frequency of ophthalmic complications on 140 cases of type II diabetes mellitus, Babol, Iran. Iran Red Crescent Med J 2012; 14: 704–706.

104.

Al Ghamdi

Rabiu

Hajar

, et al. Rapid assessment of avoidable blindness and diabetic retinopathy in Taif, Saudi Arabia. Br J Ophthalmol 2012; 96: 1168–1172.

105.

Saadi

Carruthers

Nagelkerke

, et al. Prevalence of diabetes mellitus and its complications in a population-based sample in Al Ain, United Arab Emirates. Diabetes Res Clin Pract 2007; 78: 369–377.

106.

Abdulghani

AlRajeh

AlSalman

, et al. Prevalence of diabetic comorbidities and knowledge and practices of foot care among diabetic patients: A cross-sectional study. Diabetes, Metab Syndr Obes Targets Ther 2018; 11: 417–425.

107.

Ghaem

Daneshi

Riahi

, et al. The prevalence and risk factors for diabetic retinopathy in Shiraz, Southern Iran. Diabetes Metab J 2018; 42: 538–543.

108.

Basit

Hydrie

MZI

Hakeem

, et al. Glycemic control, hypertension and chronic complications in type 2 diabetic subjects attending a tertiary care centre. J Ayub Med Coll Abbottabad 2005; 17: 63–68.

109.

Faghihi-Amini

Amini

Adibi

Silent ischemia in type I diabetic patients: a study of EKG changes. Aria J 2005; 1: 89–93.

110.

Shafiqur-Rahman

IZ.

Prevalence of microvascular complications among diabetic patients. Pakistan J Med Res 2004; 43: 1–3.

111.

Afghani

Qureshi

Chaudhry

KSA.

Screening for diabetic retinopathy: a comparative study between hospital and community based screening and between paying and non-paying patients. J Ayub Med Coll Abbottabad 2007; 19: 16–22.

112.

Esteghamati

Rashidi

Nikfallah

, et al. The association between urodynamic findings and microvascular complications in patients with long-term type 2 diabetes but without voiding symptoms. Diabetes Res Clin Pract 2007; 78: 42–50.

113.

Al-Adsani

AM.

Risk factors for diabetic retinopathy in Kuwaiti type 2 diabetic patients. Saudi Med J 2007; 28: 579–583.

114.

Askarishahi

Hajizadeh

Afkhami-Ardekani

, et al. Estimate of the diabetic retinopathy hazard rates in type 2 diabetic patients with current status data. Int J Diabetes Dev Ctries 2012; 32: 203–208.

115.

Aamir

Jan

Frequency of diabetic retinopathy in a tertiary care hospital using digital retinal imaging technology. J Postgrad Med Inst 2012; 26: 29–33.

116.

Bonakdaran

Shoeibi

Is there any correlation between vitamin D insufficiency and diabetic retinopathy?

Int J Ophthalmol 2015; 8: 326–331.

117.

Dehghan

Katibeh

Ahmadieh

, et al. Prevalence and risk factors for diabetic retinopathy in the 40 to 80 year-old population in Yazd, Iran: The Yazd Eye Study. J Diabetes 2015; 7: 139–141.

118.

Najafi

Malek

Valojerdi

, et al. Dry eye and its correlation to diabetes microvascular complications in people with type 2 diabetes mellitus. J Diabetes Complications 2013; 27: 459–462.

119.

Amini

Aminorroaya

Safaei

, et al. Prevalence of diabetic retinopathy in newly diagnosed type 2 diabetes patients in Isfahan, Iran. Acta Endocrinol (Copenh) 2008; 4: 415–423.

120.

Hosseini

Rostami

Saadat

, et al. Anemia and microvascular complications in patients with type 2 diabetes mellitus. Nephrourol Mon 2014; 6: 1–7.

121.

Alamkhanzada

Narsani

Shaikh

, et al. Frequency and types of diabetic retinopathy in type II diabetes; a hospital base study. J Liaquat Univ Med Heal Sci 2011; 10: 143–146.

122.

Manaviat

Afkhami

Shoja

MR.

Retinopathy and microalbuminuria in type II diabetic patients. BMC Ophthalmol 2004; 4: 1–4.

123.

Manaviat

Rashidi

Afkhami-Ardekani

, et al. Prevalence of dry eye syndrome and diabetic retinopathy in type 2 diabetic patients. BMC Ophthalmol 2008; 8: 10–14.

124.

Sohail

Prevalence of Diabetic Retinopathy among Type 2 Diabetes Patients in Pakistan Vision Registry. Pakistan J Ophthalmol 2014; 30: 204–212.

125.

Kahlid

Rizwan

Khan

MIN.

Frequency of diabetic retinopathy in type II diabetics presenting at DHQ hospital Sahiwal. Pakistan J Med Heal Sci 2015; 9: 1193–1196.

126.

Shaikh

Gillani

Dur-E-Yakta . Frequency of diabetic retinopathy in patients after ten years of diagnosis of type 2 diabetes mellitus. J Ayub Med Coll Abbottabad 2010; 22: 158–160.

127.

Hassan

Akhtar

Prevalence of retinopathy and its associated factors in type-2 diabetes mellitus patients visiting hospitals and diabetic clinics in Faisalabad, Pakistan. Pak J Zool 2010; 42: 41–46.

128.

Rasoulinejad

Hajian-Tilaki

Mehdipour

Associated factors of diabetic retinopathy in patients that referred to teaching hospitals in Babol. Casp J Intern Med 2015; 6: 224–228.

129.

MacKy

Khater

Al-Zamil

, et al. Epidemiology of diabetic retinopathy in Egypt: A hospital-based study. Ophthalmic Res 2011; 45: 73–78.

130.

Hussain

Arif

Ahmad

The prevalence of diabetic retinopathy in Faisalabad, Pakistan: A population-based study. Turkish J Med Sci 2011; 41: 735–742.

131.

Janghorbani

Amini

Tavassoli

Coronary heart disease in type 2 diabetes mellitus in Isfahan, Iran: prevalence and risk factors. Acta Cardiol 2017; 61: 13–20.

132.

Janghorbani

Rezvanian

Kachooei

, et al. Peripheral neuropathy in type 2 diabetes mellitus in Isfahan, Iran: Prevalence and risk factors. Acta Neurol Scand 2006; 114: 384–391.

133.

Khazai

Zargaran

, et al. Diabetic complications and risk factors in recently diagnosed type II diabetes: a case-control study. ARYA Atheroscler 2006; 2: 79–83.

134.

Thomas

Halim

Gurudas

, et al. IDF Diabetes Atlas: A review of studies utilising retinal photography on the global prevalence of diabetes related retinopathy between 2015 and 2018. Diabetes Res Clin Pract 2019; 157: 107840.

135.

Teo

Tham

, et al. Global Prevalence of Diabetic Retinopathy and Projection of Burden through 2045: Systematic Review and Meta-analysis. Ophthalmology 2021; 128: 1580–1591.

136.

Shaikh

Hatcher

Health seeking behaviour and health service utilization in Pakistan: Challenging the policy makers.

J Public Health (Bangkok) 2005; 27: 49–54.

137.

Shaikh

BT.

Private Sector in Health Care Delivery: a Reality and a Challenge in Pakistan. J Ayub Med Coll Abbottabad 2015; 27: 496–498.

138.

Mirahmadizadeh

Fathalipour

Mokhtari

, et al. The prevalence of undiagnosed type 2 diabetes and prediabetes in Eastern Mediterranean region (EMRO): A systematic review and meta-analysis. Diabetes Res Clin Pract 2020; 160: 107931.

139.

FB.

Globalization of diabetes: The role of diet, lifestyle, and genes.

Diabetes Care 2011; 34: 1249–1257.

140.

Hunter

Saratzis

Sutton

, et al. In meta-analyses of proportion studies, funnel plots were found to be an inaccurate method of assessing publication bias. J Clin Epidemiol 2014; 67: 897–903.

141.

Bener

Zirie

Janahi

, et al. Prevalence of diagnosed and undiagnosed diabetes mellitus and its risk factors in a population-based study of Qatar. Diabetes Res Clin Pract 2009; 84: 99–106.

142.

Hadaegh

Bozorgmanesh

Ghasemi

, et al. High prevalence of undiagnosed diabetes and abnormal glucose tolerance in the Iranian urban population: Tehran Lipid and Glucose Study. BMC Public Health 2008; 8: 176.

143.

Flaxel

Adelman

Bailey

, et al. Diabetic Retinopathy Preferred Practice Pattern®. Ophthalmology 2020; 127: P66–P145.

144.

Shirani

Kelishadi

Sarrafzadegan

, et al. Awareness, treatment and control of hypertension, dyslipidaemia and diabetes mellitus in an Iranian population: The IHHP study. East Mediterr Heal J 2009; 15: 1455–1463.

145.

Mirzaei

Bagheri

, et al. Awareness, treatment, and control of hypertension and related factors in adult Iranian population. BMC Public Health 2020; 20: 1–10.

146.

Alzaheb

Altemani

AH.

The prevalence and determinants of poor glycemic control among adults with type 2 diabetes mellitus in Saudi Arabia.

Diabetes, Metab Syndr Obes Targets Ther 2018; 11: 15–21.

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