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ORIGINAL PAPER
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All patients with DM from Tavush and Armavir A structured questionnaire about participants’ health-
provinces, who were registered in primary health care seeking behavior, and sociodemographic and health
(PHC) facilities, were contacted by their endocrinol- characteristics was administered by trained interview-
ogist via phone and were invited to their PHC facility ers. Two teams, each consisting of a well-trained and
for an ophthalmic examination and an interview. The qualified ophthalmologist, a nurse, and an interviewer,
individuals who agreed to participate in the study were were formed to conduct interviews and ophthalmic
invited to their PHC facility on a specific date and time examinations. The ophthalmologists had more than
for eye screening and an interview. All individuals 10 years of experience in measuring visual acuity and
with DM who did not have speech, hearing, or performing pharmacological dilation, detecting retinal
cognitive disorders were included in the study. diseases, and classifying diabetic retinopathy. The
Overall, 1287 people participated in eye screening average duration of interviews was 10–15 min.
and interviews: 449 out of 3449 from Tavush province The study teams were in contact with the fieldwork
and 838 out of 7117 from Armavir province. Oph- coordinator to discuss challenges related to the
thalmic examination and interviews were conducted fieldwork, including survey administration and oph-
from August 2016 to November 2018. thalmic examination. In addition to the review of the
completed surveys on a daily basis, the study coordi-
Study instrument nator made monitoring field visits to observe teams’
performance and provide feedback if needed.
The study team developed a structured questionnaire After completing the interview, participants were
on patients’ socio-demographic characteristics (age, undergone an ophthalmic examination, which
gender, education, socio-economic status, and included measurement of visual acuity by Golovin-
monthly expenditure), health characteristics (duration Sivtsev chart, intraocular eye pressure, and dilated eye
of diabetes, types of diabetes, family history of fundus examination. VI, blindness, and eye diseases
diabetes, and the presence of chronic non-communi- such as cataract, glaucoma suspect, DR, hypertonic
cable diseases), health-seeking behavior (frequency of retinopathy, and ARMD were defined according to the
visiting ophthalmologist and reasons of not regularly International Classification of Diseases-11 [34]. VI
visiting ophthalmologists), and ocular health (visual was classified as mild (VA worth that 6/12 but equal or
acuity, the presence of refractive errors (RE) and eye better than 6/18), moderate (VA worse than 6/18, but
diseases). equal or better than 6/60), severe (VA worse than 6/60,
but equal or better than 3/60), and blindness (VA
Study variables worse than 3/60) in the better eye with the best
correction. Dilated ophthalmoscopy was used to
The outcome variable of this study was the presence or evaluate DR. Mild non-proliferative diabetic retinopa-
absence of VI (VA \ 6/12). Independent variables thy (NPDR) was diagnosed if only micro-aneurysms
included age (continues), gender (dichotomous), were found, moderate NPDR was diagnosed if micro-
province (dichotomous), education (categorized as aneurysm hard exudates and dot hemorrhages were
‘‘secondary, B 10 years’’, ‘‘college, [ 10–B 13 years’’ found, and severe NPDR was diagnosed if in addition
and ‘‘university/ higher, over 13 years’’, socio-eco- to changes described under mild and moderate NPDR
nomic status (‘‘below average’’, ‘‘average’’, ‘‘above the examination found venous beading, cotton wool
average’’), diabetes duration (continues), hypertension spots, and intraretinal microvascular abnormalities
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(IRMA) in the retina. Pre-proliferative diabetic had university or higher (over 10 years) education. A
retinopathy was diagnosed if new vessels were found total of 48.2, 48.8, and 2.6% of participants had
in the retina and it was not defined as proliferative ‘‘average,’’ ‘‘below or substantially below average,’’
diabetic retinopathy. Proliferative diabetic retinopathy and ‘‘above or substantially above average’’ socio-
was diagnosed if new vessels on the optic disk (NVD) economic status, respectively. The mean duration of
and new vessels elsewhere (NVE) were formed diabetes was 7.4 years. Hypertension was the most
[35, 36]. ARMD was classified into two groups: prevalent chronic non-communicable disease in the
(a) dry or non-neovascular and (b) exudative or study sample (71.0%). A total of 59.6% of participants
neovascular. Dry ARMD was diagnosed if lipid visited an ophthalmologist at least once a year, while
deposits called drusen and retinal pigment epithelium 40.4% of participants reported seldom to no visits. The
(RPE) abnormalities were found, while wet ARMD common barriers for not regularly visiting ophthal-
(neovascular or exudative) was diagnosed if abnormal mologists were ‘‘having no need for visiting ophthal-
blood vessels grow from the choroid toward the mologist’’ (42.4%), ‘‘having limited financial means’’
macula (choroidal neovascularization) which involves (37.0%), and ‘‘was not aware’’ (23.5%). (Supplemen-
the exudation, leakage of fluid or blood from the new tal Table 1).
vessel into the layers of the macula as well scar tissue
formation [37]. Prevalence of VI and other eye diseases
Descriptive statistics, simple and multivariable logis- Logistic regression analysis of factors associated
tic regression models were applied to estimate the with VI
crude and adjusted associations of the independent
variables with VI. The multivariable model included The simple logistic regression analysis showed that
all the variables that were significantly associated with advanced age, low level of education, frequency of
VI (VA \ 6/12) at the p \ 0.25 level in the univariate visiting ophthalmologist, diabetes duration, the pres-
analysis [38]. Data were analyzed using SPSS version ence of glaucoma suspect, cataract, DR, and ARMD
25 (SPSS inc., Chicago, IL, the USA). were associated with VI. In the adjusted analysis, all
variables except the frequency of visiting ophthalmol-
ogists retained their significant association with VI
Results (Table 2).
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prevalence estimates of MSVI in Europe, Asia, and rates reported among individuals with DM in Tunisia
China, but lower than in Tunis and Jordan. In a meta- [27] (22.2%) and Jordan [40] (10.1%). The current
analysis of all population-based studies available study reported that the prevalence of bilateral blind-
worldwide from 1990 to 2010, Leasher et al. [39] ness was 0.9% among patients with DM, which is
found that the prevalence of MSVI due to DR was higher than the rates from studies conducted among
1.9% globally, 2.8% in Central Asia, and 2.5% in patients with DM in Iceland (\ 0.5%) [41] and China
Central Europe. Our study reported the total preva- (0.7%) [24], close to the rates reported in East Asia
lence estimates of VI and blindness, while the (1.1%) [39], and lower than the rates from studies
prevalence estimates from Leasher et al. were based conducted in Jordan (7.4%) [40] and in Tunis (4.4%)
on VI and blindness due to DR only, which makes the [27]. The higher prevalence of VI and blindness in our
direct comparison of these estimates challenging. The study sample could be attributable to the high number
Dongguan Eye Study, conducted among people with of untreated cataract. In our study, about two-thirds
DM aged over 40 in China, used the same diagnostic (66.5%) of visually impaired people had cataract,
criteria for VI and blindness as in our study, reporting 50.9% had DR, and 23.4% had ARMD. Low-income
a lower prevalence of MSVI (2.9%) compared to the societies might report high percentages of MSVI and
rates observed in our study [24]. Nevertheless, the blindness due to a high number of unoperated cataract-
prevalence of MSVI in our study was lower than the or undercorrected refractive error-related blindness
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Table 2 Unadjusted and adjusted logistic regression analysis on risk factors of VI (VA \ 6/12)
Simple logistic regression Multivariable logistic regression
OR (95% CI) p value Adjusted OR (95% CI) p value
Age 1.09 (1.07; 1.11) < 0.001 1.08 (1.06; 1.11) < 0.001
Gender
Male 1.00
Female 1.04 (0.73; 1.50) 0.816
Provinces
Armavir 1.00
Tavush 1.06 (0.76; 1.49) 0.722
Education
Secondary (B 10 years) 1.00 1.00
College ([ 10– B 13 years) 0.58 (0.40; 0.85) 0.006 0.69 (0.45; 1.06) 0.086
University or higher ([ 13 years) 0.40 (0.22; 0.75) 0.004 0.37 (0.19; 0.74) 0.005
Socio-economic status
Above or substantially above average 1.00 1.00
Average 1.13 (0.34; 3.82) 0.839 2.42 (0.57; 10.3) 0.232
Below or substantially below average 2.04 (0.61; 6.81) 0.245 2.99 (0.71; 12.7) 0.136
Frequency of visiting OPa
Seldom/never 1.00 1.00
Each year/several times a year 1.50 (1.06; 2.11) 0.022 1.08 (0.72; 1.61) 0.716
Hypertension
No 1.00
Yes 0.94 (0.66; 1.35) 0.750
Diabetes duration (in years)
No 1.00
Yes 1.10 (1.07; 1.13) < 0.001 1.05 (1.02; 1.08) 0.001
Glaucoma suspect
No 1.00
Yes 2.82 (1.67; 4.75) < 0.001 2.32 (1.25; 4.30) 0.008
Cataract
No 1.00
Yes 3.53 (2.51; 4.98) < 0.001 2.45 (1.66; 3.63) < 0.001
Diabetic retinopathy
No 1.00
Yes 4.69 (3.34; 6.59) < 0.001 3.61 (2.38; 5.46) < 0.001
Age-related macular degeneration
No 1.00
Yes 2.90 (1.93; 4.38) < 0.001 1.88 (1.15; 3.05) 0.011
a
OP Ophthalmologist
and MSVI, which could partly be attributable to poor Armenia. The prevalence estimate of DR in this
access to eye care services. [39]. population was lower than the worldwide prevalence
This study showed that the prevalence of DR was rate but relatively comparable with the rates of Asian
22.4% among people with DM in two provinces of studies. A large meta-analysis, which reviewed the
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data from 32 studies for the period of 2015 to 2019, diabetes ([ 10 years) could indicate more severe
reported that the global prevalence of any type of DR visual complications due to diabetes and double the
was 27% [14]. Ruta et al. [42] in a review of 72 studies risk of VI [27]. The studies reported that the duration
from 33 developed and developing countries reported of diabetes increases the risk of developing DR, which
that the prevalence of any diabetic retinopathy ranged in turn can affect visual acuity [25, 27]. In our study,
from 22 to 37%. The prevalence estimate of DR in our the effect of diabetes duration on VI was present even
study population was also lower than the prevalence of after controlling for DR. The association between
DR in the US (28.5) [30] and in Europe (25.7%) [43], diabetes duration and VI in the present study might be
while it is comparable with the prevalence rates of explained by the presence of other eye diseases such as
Asian studies (21%) [44] and higher than the preva- diabetic macular edema and diabetic neuropathy,
lence rates in China (18.2%) [24] and in Saudi Arabia which were not controlled in our adjusted analysis.
(19.7%) [25]. The low prevalence rate of DR in The present study found that eye diseases such as
Armenia might be explained by the poor participation DR, cataract, ARMD, and glaucoma suspect were
rates of individuals with more complicated diabetes. associated with VI in the adjusted analysis. Several
The other possible explanation for having a low rate of epidemiological studies reported a positive associa-
DR could be the relatively lower life expectancy of tion between sight-threatening eye diseases and VI in
patients with DM in developing countries. In regions patients with DM [19, 20, 27]. Kahloun et al. [27] In a
with poor diabetes control, people with DM might not cross-sectional study of 2320 patients with DM,
live long enough to experience DR, which can reduce Kahloun et al. [27] reported that cataract, DR, diabetic
the number of patients with DR [39]. macular edema, open-angle glaucoma, intravitreal
Consistent with the previous studies [19, 20, 24], hemorrhage, and retinal detachment were significantly
we also found that advanced age was one of the factors associated with VI. Similarly, Kumari et al [19] found
associated with VI (VA \ 6/12) among patients with that the most common cause of VI was cataract and
DM. For instance, the Sankara Nethralaya Diabetic that the presence of sight-threatening DR, neuropathy,
Retinopathy Epidemiology and Molecular Genetic and nuclear sclerosis were significantly associated
Study (SN-DREAMS) conducted among the Indian with VI.
population aged over 40 found that the people with Our study has several limitations. First, the preva-
DM over 60 had almost 5 times higher adjusted odds lence estimates of VI, blindness, and eye diseases were
of VI compared to those aged less than 60 [19]. from the sample of patients with DM who agreed to
Similarly, the diabetic retinopathy in various ethnic participate in the study. People who refused or were
groups in the UK (DRIVE UK) study with a sample of unable to participate might be different from those
57,144 people with DM showed that the risk of VI who participated in terms of their vision status and
increased with increasing age in both moderate and ophthalmic health. This study did not collect any
severe VI groups [20]. information about those who refused to participate in
We found that secondary (B 10 years of) education the study or did not respond to the phone calls. Second,
was the strongest risk factor for VI (VA \ 6/12), a this study could not objectively assess the main cause
finding that is consistent with other studies of VI and blindness in patients with two or more eye
[24, 45, 46]. For instance, Cui et al. [24] in a study diseases in the same eye. Therefore, we provide
of individuals with DM from China reported that prevalence estimates of eye diseases among visually
educational level was significantly associated with VI impaired people instead of comparing them with the
in the adjusted model (OR = 3.21; CI: 1.63; 6.29). rates of other studies that reported the main causes of
Similarly, Robinson et al. [45] in a sample of people VI. Third, we could not assess the association between
aged 40 years and older found that those with primary types of diabetes and VI as the majority of our study
education had higher odds of distance and near VI participants (63.1%) did not know their type of
compared to those with university education. diabetes.
The duration of diabetes in our study was associated In conclusion, this study found that VI was
with VI (OR = 1.05; CI: 1.02; 1.08), a finding that is associated with advanced age, low level of education,
consistent with several other studies [22, 24, 25, 27]. diabetes duration, and the presence of eye diseases
Existing evidence suggests that a longer duration of such as cataract, glaucoma suspect, DR, and ARMD
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among people with DM in Armenia. Cataract and DR National Academies Press (US). https://www.ncbi.nlm.nih.
were the most prevalent eye diseases in individuals gov/books/NBK385157/.
3. Coyne KS, Margolis MK, Kennedy-Martin T, Baker TM,
with VI. Thus, there is a need for regular eye screening Klein R, Paul MD et al (2004) The impact of diabetic
and diabetes prevention programs in the country for retinopathy: perspectives from patient focus groups. Fam
early detection and prevention of sight-threatening eye Pract 21(4):447–453. https://doi.org/10.1093/fampra/
diseases among high-risk populations. Continuous cmh417
4. Bourne RRA, Flaxman SR, Braithwaite T, Cicinelli MV,
educational programs on diabetes self-management Das A, Jonas JB et al (2017) Magnitude, temporal trends,
among patients with DM can decrease complications and projections of the global prevalence of blindness and
of diabetes and reduce vision loss due to diabetes. The distance and near vision impairment: a systematic review
findings of this study can inform interventions to and meta-analysis. Lancet Glob Heal 5(9):e888–e897.
https://doi.org/10.1016/S2214-109X(17)30293-0
reduce the substantial burden of diabetes and its 5. World Health Organization. Blindness and vision impair-
complications. Implementation of programs for early ment. https://www.who.int/news-room/fact-sheets/detail/
detection and treatment of DR and timely cataract blindness-and-visual-impairment. Updated October 8,
surgery could lower the risk of blindness and VI in 2019. Accessed 9 March 2020.
6. Narayan KMV, Gregg EW, Fagot-Campagna A, Engelgau
such high-risk populations. MM, Vinicor F (2000) Diabetes—A common, growing,
serious, costly, and potentially preventable public health
Acknowledgements We are thankful to the study participants problem. Diabetes Res Clin Pract 50(SUPPL. 2):S77–S84.
for their support during the implementation of the study. https://doi.org/10.1016/S0168-8227(00)00183-2
7. American Diabetes Association (2009) Diagnosis and
Authors contributions All authors contributed to the study’s classification of diabetes mellitus. Diabetes Care
conception and design. Material preparation, data collection, 32(SUPPL. 1):S62–S67. https://doi.org/10.2337/dc09-S062
and analysis were performed by [AG], [DM], [VK]. The first 8. Lloyd A, Sawyer W, Hopkinson P (2001) Impact of long-
draft of the manuscript was written by [AG] and all authors term complications on quality of life in patients with type 2
commented on previous versions of the manuscript. All authors diabetes not using insulin. Value Health 4(5):392–400.
read and approved the final manuscript. https://doi.org/10.1046/j.1524-4733.2001.45029.x
9. Cheloni R, Gandolfi SA, Signorelli C, Odone A (2019)
Funding None. Global prevalence of diabetic retinopathy: protocol for a
systematic review and meta-analysis. BMJ Open 9:22188.
Declarations https://doi.org/10.1136/bmjopen-2018-022188
10. NCD Risk Factor Collaboration (NCD-RisC) (2016)
Conflict of interest The authors declare that they have no Worldwide trends in diabetes since 1980: a pooled analysis
conflict of interest. of 751 population-based studies with 44 million partici-
pants. Lancet. 387(10027):1513–1530. https://doi.org/10.
Data availability The datasets used and/or analyzed during 1016/S0140-6736(16)00618-8
the current study are available from the corresponding author on 11. Wang W, Lo ACY (2018) Diabetic retinopathy: patho-
reasonable request. physiology and treatments. Int J Mol Sci. https://doi.org/10.
3390/ijms19061816
Ethical approval Approval was obtained from the ethics 12. Cheung N, Mitchell P, Wong TY (2010) Diabetic
committee of The Institutional Review Board of the American retinopathy. Lancet 376(9735):124–136. https://doi.org/10.
University of Armenia. The procedures used in this study adhere 1016/S0140-6736(09)62124-3
to the tenets of the Declaration of Helsinki. 13. Wild S, Roglic G, Green A, Sicree R, King H (2004) Global
prevalence of diabetes: estimates for the year 2000 and
projections for 2030. Diabetes Care 27(5):1047–1053.
Informed consent Informed verbal consent was obtained
https://doi.org/10.2337/diacare.27.5.1047
from all individual participants included in the study.
14. Thomas RL, Halim S, Gurudas S, Sivaprasad S, Owens DR
(2019) IDF Diabetes Atlas: a review of studies utilising
retinal photography on the global prevalence of diabetes
related retinopathy between 2015 and 2018. Diabetes Res
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Publisher’s Note Springer Nature remains neutral with
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regard to jurisdictional claims in published maps and
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