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avai lab le at www.sc iencedi rec t .com

journa l homepage: ht tp : / /www. int l .e lsev ierhea l th .com/ journa ls /pcd /

riginal research

creening coverage for diabetic retinopathy using ahree-field digital non-mydriatic fundus camera�

nrique Soto-Pedre ∗, Maria C. Hernaez-Ortegauropean Innovative Biomedicine Institute (EIBI), Spain

r t i c l e i n f o

rticle history:

eceived 9 October 2007

eceived in revised form

7 March 2008

ccepted 28 April 2008

ublished on line 4 June 2008

eywords:

iabetes mellitus

iabetic retinopathy

creening

creening coverage

revalence

a b s t r a c t

Aims: Guidelines for regular screening of diabetic retinopathy (DR) have been published in

the Spanish and European literature since 1992, but screening for DR is still in its early stages

in Spain. The aim of this paper is to estimate the prevalence of screening coverage for DR

and prevalence of DR itself using three-field digital non-mydriatic fundus photography to

determine whether these guidelines had been implemented.

Methods: Data on age, gender, diabetes and previous eye examinations were recorded on

a specially designed questionnaire. Three 45◦ digital images per eye were taken using a

three-field digital non-mydriatic fundus camera with two photographic procedures (both

eyes versus the eye with the poorer visual acuity).

Results: A total of 183 patients with diabetes participated. The median age and duration

of diabetes was 63 years and 10 years, respectively. Only six patients (3.3%) could not be

completely graded. Screening coverage for DR was 38.5% in patients with type 2 diabetes

and a duration less than 5 years versus those with longer diabetes duration (P = 0.007); 20.5%

of these patients had DR.

Conclusions: This study highlights the need for heightened awareness of the importance of

screening for retinopathy in people with type 2 diabetes and duration of diabetes under 5

years.

8 Pub

tion of diabetes was a significant predictor for adherence

© 200

. Introduction

ll patients with diabetes mellitus will develop some degree ofetinopathy over time [1,2]. Until now, adequate quality of care

nd regular screening has been the most important measuresor managing this complication [3–7]. Although guidelines foregular screening have been published in the Spanish and

� Presented in part at the Annual Meeting of the Spanish Society of Opward finalist in medical studies (Campaign “Diabetes may have damaational Research Council (CSIC), Madrid, Spain.∗ Corresponding author at: European Innovative Biomedicine Institutepain. Tel.: +34 609409113.

E-mail address: esoto@eibi.es (E. Soto-Pedre).751-9918/$ – see front matter © 2008 Published by Elsevier Ltd on behaoi:10.1016/j.pcd.2008.04.003

lished by Elsevier Ltd on behalf of Primary Care Diabetes Europe.

European literature since 1992 [8–11], and the Wisconsin Epi-demiologic Study of Diabetic Retinopathy [12] and the DiabeticRetinopathy Awareness Program [13] have shown that dura-

hthalmology (SEO), 10 October 2003, Valencia, Spain. 2006 ESTEVEged your eyes”, Cantabria-Spain, 2002), 14 February 2007, Spanish

(EIBI), C/Jardines #2, Apt. 1-G, 39700 Castro-Urdiales (Cantabria),

to vision care guidelines, reports on estimates of screeningcoverage for diabetic retinopathy (SCDR) taking into accountdiabetes duration are still scarce [14].

lf of Primary Care Diabetes Europe.

e t e s

142 p r i m a r y c a r e d i a b

The European Innovative Biomedicine Institute (EIBI) is abiomedical research organisation located in Spain that is com-mitted to promote innovative research in diseases for wherea need for better medical treatments have been identified. InNovember 2002 EIBI launched a campaign in Cantabria (i.e. anautonomous community at the middle-north of Spain) called“Diabetes may have damaged your eyes” close to World DiabetesDay. The announcement had been part of the “EIBI Screeningfor Diabetic Retinopathy Programme”, which promoted screeningfor retinopathy among people with diabetes in Spain in orderto determine if those guidelines were being implemented inpractice. The study had been set up to use a non-mydriaticdigital retinal camera with internal fixation targets to allowfast multiple retinal images on a screen. For the purpose ofthis study, those stored images were graded again by a retinalspecialist in a masked fashion.

The aims of this study were to estimate the prevalenceof SCDR by means of a specially designed questionnaire andthe prevalence of diabetic retinopathy (DR) using three-fielddigital photography with two photographic procedures (botheyes versus the eye with the poorer visual acuity) in a sampleof patients with diabetes mellitus from the middle-north ofSpain.

2. Patients and methods

Consecutive patients with diabetes who volunteered to partic-ipate in the study were screened at the Diabetic Associationof Cantabria (Cantabria, Spain). According to criteria definedbefore the study, patients were excluded from the screeningprogramme for the following reasons: no perception of light;inability to cooperate; and refusal to participate. Informed ver-bal consent was obtained from all study participants prior toscreening and the study was conducted in accordance with the1983 Helsinki Declaration [15]. Data on age, gender, type andduration of diabetes, and diabetes treatment were recorded ona specially designed questionnaire. Information on previouseye examinations was also collected. SCDR was defined as theproportion of patients with diabetes who had been screenedfor DR after diagnosis of diabetes and prior to this study [7].Best stenopeic visual acuity (VA) was measured using a Snellenchart at 6 m in each eye separately, and the eye with the poorerVA was recorded. Diabetes was defined by a self-reported his-tory of physician-diagnosed diabetes mellitus. Depending onage at self-reported diagnosis of diabetes, participants werefurther categorised to younger onset (<30 years of age) or olderonset (≥30 years). Younger-onset participants were consideredto have type 1 diabetes mellitus if they were also receivinginsulin. Type 2 diabetes was considered in participants with anolder-onset in the absence of insulin dependence during thefirst year. The duration of diabetes was defined as the inter-val between the first diagnosis of diabetes by health personneland the present study dates. The total amount of time spentto examine all participants was recorded.

Digital retinal images were taken with a non-mydriatic

TRC-NW100 retinal camera (Topcon® Espana S.A., Barcelona,Spain). The internal fixation targets of the camera allowedrapid capture of three 45◦ colour images per eye: field 1 cen-tred on the macula; field 2 centred on the temporal edge of the

2 ( 2 0 0 8 ) 141–146

optic disc; and field 3 temporal to macula (centre of the maculapositioned half way between the centre and the nasal edge ofthe field). Images were captured by a trained retinal specialist(H-O) using an IBM® Thinkpad notebook with NW100S soft-ware linked to OptiLink® System for image filing and grading.No mydriatic drops were used. The 2.3 million pixel retinalimages were stored in a JPEG (i.e., Joint Photographic ExpertsGroup) file format with a compression of 1:4. Eyes were pho-tographed, both eyes were graded together and the eye withthe poorer VA was also graded apart in order to estimate theagreement between the two photographic procedures (stan-dard practice – both eyes versus study method – eye with thepoorer VA).

For the purpose of this study, stored images were gradedblindly by the same retinal specialist (H-O) and classified intotwo major groups: gradable and ungradable for any reason. Animage was considered ungradable when more than one-halfof it was blurred. Gradable images were classified according tothe following international scale that identifies five levels ofdiabetic retinopathy [16]: (1) no apparent retinopathy, (2) mildnon-proliferative diabetic retinopathy (NPDR), (3) moderateNPDR, (4) severe NPDR, and (5) proliferative diabetic retinopa-thy (PDR). Gradable photographs were also labeled accordingto two major levels of sight threatening diabetic retinopa-thy (STDR): absent or present. STDR was defined as diabeticretinopathy requiring referral to an ophthalmologist accord-ing to the following screening threshold: severe NPDR or moresevere retinopathy and/or suspected macular oedema (hardexudates within one disc diameter of the centre of the foveaassociated with a VA less than 6/9 in the absence of anothercause of reduced vision). Patients who had been photocoag-ulated were not excluded and were classified using the samecriteria as those who had not been photocoagulated.

Data were entered into a Microsoft Access® database.The data-entry screens resembled the original questionnaireto reduce input errors. Logic checks were performed andfrequency distributions for all variables were analysed for out-of-range values. The median and the range of the data weregiven to describe continuous variables. Chi-square tests wereused to compare frequencies among subgroups of patients.Nonparametric methods were used where appropriate [17].The Kappa statistic (k) was used to estimate the amountof agreement corrected with that might have been expectedby chance only (agreement was considered substantial whenk > 0.60 and almost perfect when k > 0.80) [18]. Statistical anal-ysis and determination of statistical significance (P values lessthan 0.05) were determined using the Stata® package [19].

3. Results

One hundred and eighty six patients with diabetes volun-teered to participate in the study, and one hundred and eightythree were invited to participate. Three patients were excludeddue to no perception of light or inability to cooperate. Thepatient characteristics are given in Table 1. Images in 177

patients (96.7%) were all gradable and images in 6 patients(3.3%) could not be completely graded because they had atleast one ungradable fundus field due to significant mediaopacity (Fig. 1), and even though there was not a recall pro-

p r i m a r y c a r e d i a b e t e s 2 ( 2 0 0 8 ) 141–146 143

Table 1 – Characteristics of patients with diabetesmellitus that participated in the study (n = 183)

Characteristic % (n)

Gender (male) 61.2 (112)Age (years)a 63 (9–88)

Diabetes mellitusType I 16.9 (31)Type II 83.1 (152)

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Table 2 – Prevalence of diabetic retinopathy by type ofdiabetes mellitus

Retinopathy Type 1 DM (n = 31) Type 2 DM (n = 152)

No apparentretinopathy

24 (77.4%) 117 (76.9%)

Any DR 7 (22.5%) 35 (23.1%)Mild NPDR 3 (9.7%) 30 (19.7%)Moderate NPDR 1 (3.2%) 4 (2.6%)Severe NPDR 1 (3.2%) 0 (0.0%)PDR 2 (6.5%) 1 (0.7%)

STDR 7 (22.5%) 5 (3.3%)

DM = diabetes mellitus; NPDR = non-proliferative diabetic retinopa-thy; PDR = proliferative diabetic retinopathy; STDR = sight threat-ening diabetic retinopathy. Severe non-proliferative diabeticretinopathy or more severe retinopathy and/or suspected macularoedema (evidenced by the presence of hard exudates within onedisc diameter of the centre of the fovea and associated with a VAless than 6/9 in the absence of another cause of reduced vision).

Table 3 – Prevalence of DR, STDR and SCDR in patientswith type 2 diabetes by duration of diabetes (n = 152)

Duration of diabetes(years)

n DR (%) STDR (%) SCDR (%)

<5 39 20.5 0.0 38.55–10 28 14.3 3.6 60.710–15 31 22.6 6.5 61.3>15 54 29.6 3.7 74.1

DR = any diabetic retinopathy. SCDR = the proportion of patientswith diabetes who had been screened for DR after diagnosis ofdiabetes and before the study. STDR = sight threatening diabeticretinopathy. Severe non-proliferative diabetic retinopathy or moresevere retinopathy and/or suspected macular oedema (evidencedby the presence of hard exudates within one disc diameter of thecentre of the fovea and associated with a VA less than 6/9 in the

Duration of diabetes (years) 10 (1–50)

a Age and duration of diabetes expressed as median (range).

edure for these patients they were all suggested to visit theirphthalmologist to further evaluate their media opacity. Theotal time to examine all participants was 13 h and 45 min; theverage time per patient was 4 min and 30 s.

Forty-two (23.7%) patients with gradable photographs hadome evidence of retinopathy; 33 (18.6%) had mild NPDR, 52.8%) had moderate NPDR, 1 (0.6%) had severe NPDR, and 31.7%) had PDR. Twelve (6.9%) patients had STDR and wereeferred to an ophthalmologist for follow-up or treatment forne or both eyes. Table 2 shows the prevalence of DR and STDRy type of diabetes mellitus (n = 183).

Sixty-eight patients (37.2%) who entered the study reportedhat they had not undergone a fundus examination from diag-osis of diabetes mellitus to the time of this study; 7/31 (22.6%)ype 1 and 61/152 (40.1%) type 2 diabetes (P = 0.065). Table 3hows the prevalence of DR, STDR and SCDR in type 2 diabeticatients stratified by years of duration of diabetes. Screeningoverage was only 38.5% in patients with type 2 diabetes withdiabetes duration under 5 years compared to those with a

onger diabetes duration (P = 0.007). Even though 20.5% of theseatients had evidence of DR, none had STDR. No significantifferences were found based on age and/or gender.

There was substantial agreement for the presence of DRkappa = 0.75) and STDR (kappa = 0.62) when comparing the

tudy method (three fields in the eye with the poorer VA) withtandard practice (the same three fields in both eyes) (n = 177,= 0.001).

Fig. 1 – Flow chart of the data generation process.

absence of another cause of reduced vision).

4. Discussion

Our estimate of prevalence of DR in people with self reporteddiabetes was 23.7%. This estimate was similar to the estimateof 20–20.9% reported on patients with diabetes attending pri-mary care services in Spain [20,21]. Higher estimates (over30%) of DR are found in population-based studies where detec-tion of retinopathy relies on tests with higher sensitivity,such as fluorescein angiography [22]. It was also close tothe prevalence found in population-based studies in othercountries, ranging from 20.6% to 24.8% [23–25]. Differencesin sample size, sampling procedure and distribution of riskfactors in the population might also account for this variabi-lity.

Sixty-eight patients (37.2%) who entered the study reportedthat they had not undergone a fundus examination from diag-nosis of diabetes mellitus to the time of this study (22.6%

type 1 and 40.1% type 2 diabetes mellitus). This is similar toresults found in published population based studies. The Mel-bourne Visual Impairment Project, from Victoria, Australia,examined a population of 239 people aged 42–91 with self

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144 p r i m a r y c a r e d i a b

reported diabetes and found that 36% had never undergone afundus examination [26]. This group has also previously pub-lished a proportion of 31.8% of 157 people with diabetes hadnever visited an ophthalmologist [22]. An overall 30% of peoplewith no previous ophthalmologic examination were reportedby Massin et al. at the conclusion of the first study of screeningfor DR in a primary care setting in France. This cross-sectionalstudy of people with diabetes excluded those with known DR,which may explain their lower estimate [27].

Because of the lack of information in the literature, weinvestigated further the diabetes duration-specific prevalenceof SCDR. This information is vital for quantifying need whenplanning adequate screening services. In our study patientswith type 2 diabetes and a diabetes duration under 5 yearswere clearly under-screened for DR (only 38.5% had receiveda previous fundus examination) compared to those patientswith longer diabetes durations (over 60%) (P = 0.007). We haverecently reported on SCDR among a sample of 217 patientswith type 2 diabetes that were attending a High ResolutionDiabetes Centre in Bilbao (a secondary health care centre,located in a city at the middle-north of Spain, offering anintegrated approach to care of patients with diabetes andproviding diagnosis, education, treatment and complicationscontrol on one site). Fifty percent of those patients haddeveloped some retinopathy within the first 5 years afterdiagnosis of the disease but only 26.1% had undergone a fun-dus examination [14]. Analysis of the Diabetes Control andComplications Trial (DCCT) data in type 1 diabetes suggestedthat patients with retinopathy before 5 years duration hadmore rapid progression of vascular pathology than those withno retinopathy. Early recognition of retinopathy is thereforeimportant as these patients are at higher risk of progressionto STDR [28]. The detection of any new complication of dia-betes such as the development of any retinopathy should leadto optimisation of risk factors and improved medical manage-ment as this has clearly been shown to slow the progressionof retinopathy [29,30].

The use of non-mydriatic retinal cameras is gainingincreasing acceptance for screening programs due to theirability to achieve gradable images without dilating the pupil.Besides, digital images have the advantage of instant avail-ability, ease of archiving/retrieval and remote transmission[31–33]. We used a three-field digital fundus photographysystem with internal fixation targets that allowed rapid acqui-sition of three 45◦ colour digital images per eye. The fixationtargets helped achieve consistent fundus photography. Eventhough images in 3.3% of patients could not be completelygraded because they had at least one ungradable fundusfield, this electronic imaging system reduced by half the per-centage of ungradable images obtained in a previous study(6.6%) utilising one non-mydriatic 45◦ Polaroid® instant filmfundus photograph [34]. Reports of ungradable image ratesfor non-mydriatic photography vary between 3.2% and 36%[35]. The reasons for so few ungradable images in this studymay be the fact that retinal images were taken by thesame highly experienced retinal specialist (H-O), and that

the instant availability of the image conferred the advan-tage that if there was a problem with quality a furtherphotograph could be taken. Besides, having a non-mydriaticretinal camera with an internal fixation device seems also

2 ( 2 0 0 8 ) 141–146

to be helpful in reducing the proportion of ungradable pho-tographs.

The present study did not specifically validate a three-fielddigital imaging modality for diagnosis of DR or STDR, but con-sidering that size of the examined fundus image has a positiveeffect on the validity of the imaging modality [36–38], it doesnot seem hard to assume that this three-field digital imagingmodality should be at least as good as our previous validatedsingle-field screening modality that revealed an overall sensi-tivity of 91.1% and a specificity of 89.7% [34]. In fact, a similarthree-field imaging modality was evaluated by Murgatroyd etal. and they reported similar results [39]. We did comparethree-field photography in the eye with the poorer VA to thesame three-field protocol in both eyes, and there was substan-tial agreement for the presence of DR and STDR (kappa > 60).This finding offers a new argument for undertaking only three-field photography of the eye with the poorer VA for screeningpurposes as we showed before [14,34].

One potential limitation of this paper may be that it reportson data on patients with known diabetes who chose to partic-ipate in a screening programme for retinopathy. Volunteersare likely to be different from those who do not volunteer in anumber of ways that may bias the outcome. In general, volun-teers tend to have better health than the general populationand are more likely to adhere to prescribed medical regimens[40]. On the other hand, those who volunteer for a screeningprogramme may represent the “worried well,” that is, asymp-tomatic individuals who are at higher risk of developing thedisease because of medical or family history, or any num-ber of lifestyle characteristics. Such individuals might havean increased risk of having the disease. The final direction ofthe potential patient selection bias may be difficult to predictin this sample of patients [41]. Although some deviation fromthe true prevalence might be expected, our results suggest thatselection bias should be ruled out because the prevalence ofDR among type 2 diabetic patients in this study was similarto that in patients attending primary care services in Spain[20,21].

In conclusion, the current guidelines for screening for DRin patients with type 2 diabetes in Spain are not being imple-mented in practice. Although the probability of developingSTDR is low in type 2 patients with duration of diabetes under5 years, there needs to be increased awareness of the needfor screening programs in this subgroup of patients becausethe medical management of DR is most effective in the initialstages of the disease when the pathology is still reversible.Our results suggest that a three-field non-mydriatic retinalcamera with an internal fixation device seems to be helpfulin reducing the proportion of ungradable photographs. Ourfindings also offered an argument for undertaking only three-field photography of the eye with the poorer VA for screeningpurposes. Further studies will be required to assess the imple-mentation of screening programmes that are based on thisimaging modality to confirm its clinical effectiveness and cost-effectiveness.

Conflict of interest

None to declare.

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cknowledgements

e gratefully acknowledge the invaluable assistance of Dr.eborah M. Broadbent MRCOphth (St. Paul’s Eye Unit, Royaliverpool University Hospital, Liverpool, UK) for helpful com-ents made during the preparation of the manuscript.The preparation of this manuscript was sponsored by a

rant from Ipsen Pharma S.A. (Barcelona, Spain).

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