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Tele-ophthalmology for diabetic retinopathy screening: 8 years of experience
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ARCHIVOS DE LA SOCIEDAD ESPAÑOLA DE OFTALMOLOGÍA www.elsevier.es/oftalmologia
Original article
Tele-ophthalmology for diabetic retinopathy screening: 8 years of experience夽 A. Pareja-Ríos a , S. Bonaque-González b,c , M. Serrano-García a,∗ , F. Cabrera-López d , P. Abreu-Reyes e , M.D. Marrero-Saavedra f a
Hospital Universitario de Canarias, La Laguna, Tenerife, Spain Departamento de Física, Universidad de La Laguna, La Laguna, Santa Cruz de Tenerife, Spain c Grupo de Ciencias de la Visión, Universidad de Murcia, Murcia, Spain d Complejo Hospitalario Universitario Insular Materno-Infantil, Las Palmas de Gran Canaria, Spain e Hospital Universitario Nuestra Senora ˜ de Candelaria, Santa Cruz de Tenerife, Spain f Hospital Universitario de Gran Canaria Dr. Negrín, Las Palmas de Gran Canaria, Spain b
a r t i c l e
i n f o
a b s t r a c t
Article history:
Purpose: To describe the results of a diabetic retinopathy screening program implemented
Received 29 March 2016
in a primary care area.
Accepted 16 August 2016
Methods: A retrospective study was conducted using data automatically collected since the
Available online xxx
program began on 1 January 2007 until 31 December 2015.
Keywords:
patients in 2007 to 42,339 diabetic patients in 2015. Furthermore, the ability of family doctors
Results: The number of screened diabetic patients has progressively increased from 7173 Diabetic retinopathy
to correctly interpret retinographies has improved, with the proportion of retinal images
Diabetes mellitus
classified as normal having increased from 55% in 2007 to 68% at the end of the study period.
Telemedicine
The proportion of non-evaluable retinographies decreased to 7% in 2015, having peaked at
Optical coherence tomography
15% during the program. This was partly due to a change in the screening program policy
Primary health care
that allowed the use of tropicamide. The number of severe cases detected has declined from 14% with severe non-proliferative and proliferative diabetic retinopathy in the initial phase of the program to 3% in 2015. Conclusions: Diabetic eye disease screening by tele-ophthalmology has shown to be a valuable method in a growing population of diabetics. It leads to a regular medical examination
夽 Please cite this article as: Pareja-Ríos A, Bonaque-González S, Serrano-García M, Cabrera-López F, Abreu-Reyes P, Marrero˜ Saavedra MD. Teleoftalmología para el cribado de la retinopatía diabética: experiencia de 8 anos. Arch Soc Esp Oftalmol. 2016. http://dx.doi.org/10.1016/j.oftal.2016.08.006 ∗ Corresponding author. E-mail address: [email protected] (M. Serrano-García). ˜ ˜ S.L.U. All rights reserved. 2173-5794/© 2016 Sociedad Espanola de Oftalmolog´ıa. Published by Elsevier Espana,
OFTALE-1078; No. of Pages 8
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of patients, helps ease the workload of specialized care services and favors the early detection of treatable cases. However, the results of implementing a program of this type are not immediate, achieving only modest results in the early years of the project that have improved over subsequent years. ˜ ˜ S.L.U. All rights © 2016 Sociedad Espanola de Oftalmolog´ıa. Published by Elsevier Espana, reserved.
Teleoftalmología para el cribado de la retinopatía diabética: experiencia ˜ de 8 anos r e s u m e n Palabras clave:
Objetivo: Mostrar los resultados de un programa de cribado de la retinopatía diabética desde
Retinopatía diabética
el ámbito de la atención primaria.
Diabetes mellitus
Métodos: Se realizó un estudio retrospectivo de los datos recogidos mediante registro infor-
Telemedicina
mático automatizado desde el 1 de enero de 2007, hasta el 31 de diciembre de 2015.
Tomografía de coherencia óptica
Resultados: El número de pacientes cribados aumentó progresivamente desde 7.173 en 2007
Atención primaria
hasta 42.339 en 2015. Asimismo, la habilidad de los médicos de familia en la interpretación de retinografías mejoró progresivamente, clasificando como normales un 55% de las retinografías en 2007, llegando a un 68% en 2015. El número de retinografías consideradas no valorables disminuyó a lo largo del programa, registrándose picos de hasta el 15% y situándose en un 7% en 2015, en parte gracias a un cambio en la normativa, que permitió dilatar la pupila. Se detectaron cada vez menos casos graves, pasándose de un 14% de retinopatías diabéticas no proliferativas severas y proliferativas al inicio del programa a un 3% en 2015. Conclusiones:
El cribado de la oftalmopatía diabética mediante teleoftalmología se
reveló como un método muy valioso en una población en crecimiento como es la diabética, facilitando las revisiones al usuario, ayudando a descongestionar los servicios de atención especializada y detectando los casos tratables con mayor precocidad. Sin embargo, los efectos de la implantación no fueron inmediatos, obteniéndose unos resultados modestos en ˜ ˜ los primeros anos del proyecto, que mejoraron en los anos subsiguientes. ˜ ˜ S.L.U. Todos © 2016 Sociedad Espanola de Oftalmolog´ıa. Publicado por Elsevier Espana, los derechos reservados.
Introduction The worldwide growth of the number of patients with diabetes type I is a fact,1 while type II diabetes is growing exponentially.2 It is estimated that in Europe about 53,000,000 adults have diabetes, nearly 8.1% of the adult population and that, by 2030, 9.5% of the adult population will have diabetes.3 In Spain, diabetes affects 13.8% of which 7.8% has recognized diabetes whereas the remaining 6% is not aware of having diabetes.4 In this scenario, health systems are facing the challenge of rapidly assessing a very large and growing population. Significant efforts have been made in the past few years to identify diabetes at an early stage. This identification is important for ophthalmology specialists because an undiagnosed diabetes patient cannot be included in the screening program for diabetic retinopathy. Such programs have gained importance as the advanced stages of diabetic retinopathy and diabetic macular edema constitute two of the main irreversible vision impairment causes in developed countries5,6 in addition to being one of the main causes of blindness.7
According to the American Diabetes Association and the American Ophthalmology Academy, an ocular fundus examination at least once a year is necessary for diabetes patients in order to identify possible lesions.8,9 This recommendation is based on the fact that, according to the World Health Organization, early treatment of diabetic retinopathy could reduce severe visual impairment risk in over 90%.10 Accordingly, the objective is early detection of patients in order to administer treatment before visual impairment becomes substantial and irreversible. However, not all patients undergo examinations once a year and it is estimated that up to 30% of all diabetes patients have never undergone an ophthalmological examination and that many of these could have undiagnosed ocular diseases.11–14 One of the proposed solutions for improving care of these patients is tele-ophthalmology. Digital photography and telemedicine are arising as strategies to facilitate access to healthcare all over the world. In similar studies, tele-ophthalmology has shown to be effective
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and cost-efficient15–24 and it seems particularly indicated as a method for extending medical care to remote populations.25–28 Considering the geographic characteristics of the Autonomous Community of the Canary Islands, a territory comprising 7 islands (some of which do not have a resident ophthalmologist), in 2002 a tele-ophthalmology program was launched for screening diabetic retinopathy with the objective of improving access to health services for diabetic patients.29 To this end, general practitioners were trained in a structured accreditation program to interpret ocular fundus photographs of their diabetes patients and referring pathological or doubtful cases to the ophthalmologist for a telematic assessment and to decide whether the patient should be examined at the ophthalmology practice. The present study describes the experience of said program (Retisalud) from January 1, 2007 up to December 31, 2015 in the Autonomous Community of the Canary Islands.
Material and methods The objective of this program is to screen for diabetic retinopathy analyzing ocular fundus images for the highest possible number of patients who meet the inclusion criteria of being affected by diabetes mellitus type I or 2 and do not meet any of the following exclusion criteria: (1) age under 15 (or before adolescence); (2) having a diagnostic of moderate or higher retinopathy, or macular edema; (3) having an ocular disease diagnostic (CIE-9) incompatible with screening (such as amaurosis or severe vision impairment, or awaiting ocular surgery such as cataracts or the like); (4) being a patient registered at another autonomous community; (5) being at home and unable to move; (6) having a registered ophthalmic control in a private or private-public regimen, and (7) being excluded from the program for any other reason. To fulfill said objectives, non-mydriatic Topcon TRC-NW6S cameras and subsequent models with similar features (Topcon Corporation, Tokyo, Japan) were progressively installed in 43 health centers uniformly distributed throughout the autonomous community in accordance with the population to be screened in each center. Said devices comprise a nonmydriatic retinal digital camera taking color photographs of the posterior pole and the peripheral retina. Images are taken in true color (24 bits) at a resolution of 1490 × 960 pixels. The procedure for focusing and centering the retinal image is simple and software-assisted. The photographer can see each image immediately after being captured and can repeat the process is the image is not adequate. The staff in charge of capturing images, mostly clinic personnel and nurses, were trained to ensure adequate image quality. In addition, training courses were held for family physicians, who had this service included in the list of objectives as an incentive. After said training, the physicians underwent an examination which established that the number of errors in 200 retinography readings should be under 30%. In December 2015, 1177 family physicians in the Autonomous Community of the Canary Islands were accredited for this activity. In addition, their work was followed up and additional seminars and accredited
Table 1 – Demographic data of diabetes patients and patients screened in the program from 2007 to 2015. Year
Estimated number of diabetes patients in the program
Number of screened patients (percentage of total number)
2007 2008 2009 2010 2011 2012 2013 2014 2015
73,326 85,598 98,891 109,323 146,702 144,177 145,313 132,674 128,975
7173 (9.78) 11,449 (13.38) 14,345 (14.51) 19,320 (17.67) 24,006 (16.36) 31,460 (21.82) 40,786 (28.07) 45,726 (34.46) 42,339 (32.83)
courses were provided to all health centers who required or requested it. Said seminars and courses explained the most frequent errors detected in the interpretation of retinographies and requested collaboration. At present, said training is continuing in health centers where the follow-up of diabetes patients is below average or those who request it as a part of their ongoing training program. The program is based on opportunistic screening as this region, similarly to other autonomous communities of Spain, does not carry a census of diabetes patients, which excludes systematic screening. Accordingly, only the diabetic patients that concerned with their general practitioner for different medical reasons can be included in the screening. The screening protocol consists in capturing an ocular fundus image centered on the macula, mostly without pupil dilatation up to the end of 2014 and utilizing pupil dilatation ® with a single tropicamide drop (Colircusí Tropicamida Alcon Cusí, SA, El Masnou, Barcelona, Spain) as from January 2015 when the quality of the retinography was considered inadequate. Said images are classified as invalid if they do not enable the observer to determine the presence or absence of disease. Valid images are classified as normal, pathological or doubtful. The procedure to be followed is shown in the flowchart of Fig. 1. It must be noted that if the image is classified as pathological, doubtful or invalid by the primary health care physician, the image is remotely screened in a second stage by a specialized care ophthalmologist. As the clinical data obtained during said process could be crucial for future nationwide programs, all the program outputs have been saved on automated computer records from the first years of the program. The same computer application used by general practitioners and ophthalmologists to check the retinographs also stores data on waiting time for image assessment and results.
Results The results detailed below are global and not segmented for each of the 7 islands because the distribution of cameras took into account the population of each district, with results being relatively homogeneous and all islands. Table 1 shows the number and percentage of diabetic patients against the total for the year that were assessed by the screening program. A growing trend can be appreciated,
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New image in 2 years
Image analysis by family physician
New image in one year
Yes
No
Classified as normal?
Any risk factors or diabetes with over 10 years evolution?
Yes
No
Remote assessment of image by ophthalmologist
Severe pathology or invalid image
Moderate pathology
Referral to reference hospital
Referral to district ophthalmologist
No pathology or risk factors
Slight pathology and risk factors
Fig. 1 – Screening process flowchart.
in which nearly 33% of the diabetic population was examined after 8 years. As the number of patients with diagnosed diabetes also increased, the program examined 6 times more patients in 2015 than in 2007. Fig. 2 illustrates the percentage of tests against the total considered by the general practitioner as normal, invalid or pathological/doubtful. The percentage of normal tests varied throughout the program between 54 and 68%. In the last 3 years, the primary health care physicians diagnosed a higher percentage of images as normal.
Images assessed by primary care physicians
80% 70%
68% 64%
60%
55%
57%
56%
55%
62%
59% 54%
%
50% 40%
35%
35%
35%
34% 29%
30%
29% 25%
25%
20% 10%
31%
10%
12%
10%
9%
15% 11%
9%
9%
7%
0% 2007
2008
2009
2010
2011
2012
2013
2014
2015
Year Invalid
Pathological/doubtful
Normal
Fig. 2 – Classification of retinographies by primary care physicians.
A number of factors took part in images being classified as invalid by the primary health care physicians, including opacity, typical old-age myosis or inadequate capturing technique. Fig. 2 shows the range between 9 and 50% with relative stability, excepting 2015 where the best values were achieved (7%) due to the use of tropicamide applied to all patients when adequate images could not be obtained. Similarly, the percentage of photographs classified as pathological or doubtful and referred to the specialist for remote assessment remained between 25 and 35%, although Fig. 2 shows that in the latest years the rights diminished. This is a good sign, considering that the highest number of patients was examined. Fig. 3 shows the amount of images classified as normal, invalid or pathological that were referred to the ophthalmology experts for remote assessment. It can be seen that the percentage of images classified as normal remained relatively stable despite the increase in the number of screened patients, which peaked in the last year. The proportion between referred images and those considered as invalid reached the lowest number in the last year. Due to the increase of the examined population year after year, in 2012, 2013, 2014 and 2015 ophthalmologists received 1900, 2135, 2279 and 1133 images that were finally classified as invalid. This number is significant because all the rejected retinographies are removed from the network and the patients must be examined by an ophthalmologist under pharmacological midriasis. Even
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250
Images assessed by specialized physicians 70%
200
63%
196
60%
42%
50%
52%
50%
47%
47% 42% 42%
41%
38%
37%
37%
36%
%
40%
16%
17%
100 47 34
50 28
0 2006
14%
13%
12%
9%
9%
16%
126
49 27%
20%
150
34%
30%
10%
Days
50%
49%
50%
2007
29
2008
28
2009
20
19 20
2010
12
2011
9
2012
19
2013
23 20
2014
22 19
2015
Year
9%
Family physician
Ophthalmologist
0% 2007
2008
2009
2010
2011
2012
2013
2014
2015
Fig. 5 – Waiting days for each retinograph to be assessed by the family physician and the ophthalmologist, respectively.
Year Invalid
Pathological
Normal
Fig. 3 – Classification by ophthalmology specialists of retinographies sent for remote assessment.
Discussion
though in this group of patients ocular fundus exploration was normal in a high percentage of cases, 30% exhibited diabetic retinopathy. Fig. 4 shows the classification of images classified as pathological as “slight or moderate” and “severe or higher” according to the ophthalmologists. The percentage of images that revealed severe or higher disease diminished year after year even though the number of patients progressively increased as mentioned above. Finally, Fig. 5 shows the mean waiting time for each retinograph before being assessed by the general practitioner or the ophthalmologist. In the case of the former, the waiting time showed a clearly descending trend with larger waiting times in the first 2 years of the project and progressively descending each year as the physicians included the assessment of said images in their daily practice. This was supported by the inclusion of this task as an objective to be assessed in incentives.
Classification of diabetic retinopathy by specialized physicians 120% 100% 86%
91% 83%
80%
80%
93%
93%
97%
80%
%
66%
60% 40% 20%
34%
14%
17%
20%
20% 9%
7%
7%
3%
0% 2007
2008
2009
2010
2011
2012
2013
2014
2015
Year Slight or moderate
Severe or superior
Fig. 4 – Grade of diabetic retinopathies identified remotely and classified by ophthalmology physicians.
In 2015, the Autonomous Community of Canary Islands had a population of approximately 2,100,306 inhabitants distributed in 7 main islands, of which approximately 221,000 were diabetics. As the number of ophthalmologists is approximately 160, each one should examine 7 diabetic patients every working day in order to screen each patient once a year. For this reason, in 2006 it was decided to implement a teleophthalmology system involving the primary health care of the region. The program is based on the family physicians who perform the metabolic control of the patients and are familiar with the comorbidities caused by the disease to generally monitor the condition of the retina. Family physicians already follow-up the microvascular complications of diabetes such as nephropathy or neuropathy and refer patients to nephrologists or neurologists only when specific thresholds have been exceeded. This makes family physicians adequate for assessing an additional microvascular complication such as the ocular fundus of patients. However, numerous obstacles appeared during the deployment of the program, particularly in the beginning. On the one hand, ophthalmologists had the feeling that the family physician could take over their functions, and in turn the latter felt that this new function would worsen their workload and raised fear of legal liabilities that could be derived from erroneously classifying a retinography as normal. A further obstacle was the high initial cost of the program for the health system, comprising equipment, training for technicians and physicians as well as follow-up programs, despite the fact that diminished prevalence of blindness and visual impairment as well as the improvement of specialized care obviously diminished the overall cost for the health system. However, previous financial studies involving similar programs evidenced that when adding up all the costs (direct costs for health services, for patients and productivity losses) these programs are cost effective.30 Throughout the 8 years of the program, the overall number of screened patients progressively increased to reach 42,339 in 2015, representing 32.83% of the estimated population of diabetics that year. Even though apparently the percentage of patients screened in 2015 could seem small considering the
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duration of the project, it must be taken into account that in the past the entire diabetic population was examined only by ophthalmology specialists in hospitals or in specialized care centers. Considering that the program supplemented existing services, a larger number of patients are still examined by their specialist in Social Security services, who receive ophthalmic attention through private insurances or who do not meet the characteristics to enter the program. On the other hand, in the past 2 years it was decided to screen patients who did not show signs of diabetic retinopathy (approximately 70%) at two-year intervals, which produced a significant reduction in the percentage of screened patients. A survey was carried out to obtain an estimate of the actual percentage of diabetic patients with ophthalmic examinations among 20 pharmacies of the region, both in rural and urban areas (results not published). The survey consisted in asking all diabetes patients to visit one of said pharmacy for any reason if their ocular fundus was regularly examined. In the survey, 82.6% of respondents indicated they underwent a regular ocular fundus examination through the Retisalud program, with their district ophthalmologist or in public or private hospitals. Even though a formal survey designed to ensure a representative sample of the diabetes population would be necessary to determine this information with greater precision, the results evidenced that the volume of diabetes patients with ophthalmological follow-up in the islands is much higher than those registered in the screening program. In addition, the figures and tables demonstrate that in 2015 ophthalmologists remotely assessed 7742 images that were considered as pathological, doubtful or invalid by the general practitioners and eventually were normal or invalid. However, it must be taken into account that these assessments take up significantly less time than examining each patient in the practice. In said year, 32,946 images were assessed as normal by family physicians, representing a high number of patients who did not visit the ophthalmology practice for the annual ocular fundus examination. Adding up all factors, the program enables a considerable reduction of the workload of the ophthalmology practices, allowing the specialists to dedicate more time to treatments instead of screening. In addition, it must be taken into account that the Retisalud program enables assessments of over 3000 pathological patients in 2015 who otherwise would have not been examined. In addition, family physicians felt increasingly confident to classify an image as normal (Fig. 2). During the first years of the program they referred the retinographs for expert assessment upon the slightest doubt, whereas after several years of experience they classified an increasing percentage as normal, to the point that in the last 3 years family physicians classified more retinographies as normal and less as invalid, pathological or doubtful. More importantly, the percentage of patients with severe retinopathy has diminished every year (Fig. 4), evidencing an increasingly effect to control the target population and enabling the identification of disease at early stages. An added advantage of the program is that frequent network communication has created communications channels between family physicians and ophthalmologists, which
has enabled the detection and consultation of ocular diseases other than those caused by diabetes. One of the challenges to overcome is to improve the number of invalid images. In this study, the percentage thereof increased regularly and peaked in 2012 (Fig. 2), matching the inclusion of numerous technicians and nurses in the program. It is likely that the learning curve negatively influenced the statistics of that year. The high number of invalid images increases the workload as all patients with invalid retinographies are personally examined at the ophthalmology practices. However, until December 2014 the images were captured without dilatation in the majority of cases. In order to diminish the number of invalid retinographies, since January 2015 and on the basis of similar studies that achieved good results with this strategy20,31 it was agreed that, whenever an adequate image was not obtained despite midriasis in the mesopic conditions in which the images were captured, the patient would be administered a single tropicamide drop. This diminished the number of invalid images when compared to previous years, reaching the lowest numbers since the beginning of the program. On the other hand, the waiting time for examining retinographies exhibited a downward curve both at the ophthalmological and the primary health care level (Fig. 5), being approximately 3 weeks in the past 2 years. As regards potential improvements for the program, studies should be made to verify if the percentage of blindness derived from diabetic retinopathy has diminished (and to what extent) since the deployment of the program. It would also be useful to carry out control studies with protocols, randomly examining retinographies classified as normal by family physicians to assess the degree of sensitivity, although other studies have already evidenced that the level of agreement in diagnostic between primary health care physicians and ophthalmologists means that the examination of diabetes patients by primary health care physicians is reliable.19 The proposed improvements include the possibility of a diabetics census in order to automatically issue an appointment for capturing a retinography as soon as the patient is diagnosed with diabetes as well as establishing the periodicity thereof. Even though this measure would not prevent the absenteeism of patients who do not attend their appointments, it would enable the inclusion of all diabetics in the program and not only those who visit their family physician. On the other hand, it would be interesting to have an improved software protocol enabling easy access to previous patient retinographies. In addition, the possibility of capturing a second image focused on the optic nerve, including the proximal nasal area, is being considered to improve screening sensitivity. A further possibility is the use of automated software for identifying pathological images as well as the possibility of using combined OCT/retinograph systems, particularly in densely populated areas, that could also enable early detection of diabetes macular edema. Other studies have recommended the presence of the optician-optometrist in primary health centers on the basis that the optometrist optician is recognized as a health professional.19 This would easily increase patient examinations with visual acuity tests, tonometry or additional images focused
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on the optic nerve and the peripheral retina, thus increasing the scope of the screening to cover other diseases. In conclusion, said program is providing positive results, demonstrating that diabetic ophthalmopathy screening with tele-ophthalmology presents great potential, particularly considering the growth of the diabetic population and the small number of specialists. In addition, it exhibits the advantage of enhancing the relationship between family physicians and specialized health professionals.
Conflict of interest No conflict of interest has been declared by the authors.
Acknowledgments The authors wish to express their gratitude to the staff of the regional government for providing necessary data: Carmen Gloria Rodríguez Valerón, Santiago de la Huerga Moreno and María Rocío Ávarez Sánchez, as well to all staff (technicians, clinical assistance, University nurse graduates, primary health care physicians and ophthalmologists) who have supported Retisalud and make it a live program.
references
1. Harjutsalo V, Sjoberg L, Tuomilehto J. Time trends in the incidence of type 1 diabetes in Finnish children: a cohort study. Lancet. 2008;371:1777–82. 2. Shaw JE, Sicree RA, Zimmet PZ. Global estimates of the prevalence of diabetes for 2010 and 2030. Diabetes Res Clin Pract. 2010;87:4–14. 3. The International Diabetes Federation. Diabetes Atlas. 6th ed. IDF; 2013. 4. Soriguer F, Goday A, Bosch-Comas A, Bordiú E, Calle-Pascual A, Carmena R, et al. Prevalence of diabetes mellitus and impaired glucose regulation in Spain: the [email protected] Study. Diabetologia. 2012;55:88–93. ˜ 5. Congdon N, O’Colmain B, Klaver CC, Klein R, Munoz B, Friedman DS, et al. Causes and prevalence of visual impairment among adults in the United States. Arch Ophthalmol. 2004;122:477–85. 6. Friedman DS, Congdon NG, Kempen J, Tielsch JM. Vision problems in the U.S.: prevalence of adult vision impairment and age-related eye disease in America. Schaumburg, IL: The Silver Book; 2002. 7. Centers for Disease Control and Prevention. National diabetes fact sheet: general information and national estimates on diabetes and prediabetes in the United States. Atlanta: U.S. Department of Health and Human Services; 2011. 8. American Diabetes Association. Standards of medical care in diabetes – 2010. Diabetes Care. 2010;33 Suppl. 1:S11–61. 9. American Academy of Ophthalmology Retina Panel. Preferred Practice Pattern Guidelines: diabetic retinopathy. San Francisco, CA: American Academy of Ophthalmology; 2008.
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10. Cheung N, Mitchell P, Wong TY. Diabetic retinopathy. Lancet. 2010;376:124–36. 11. Sprafka JM, Fritsche TL, Baker R, Kurth D, Whipple D. Prevalence of undiagnosed eye disease in high-risk diabetic individuals. Arch Intern Med. 1990;150:857–61. 12. González-Clemente JM. Diabetes mellitus no dependiente de insulina: asistencia en un área de Barcelona. Med Clin (Barc). 1997;108:91–7. ˜ 13. Espinás J, Salla RM, Bellvehí M, Reig E, Iruela T, Munoz E, et al. Reevaluación del programa de diabetes mellitus tipo II. Propuesta de indicadores de calidad. Aten Prim. 1993;11:123–6. 14. Palacios MS, Vernet MV, Sáez PL, Figueras ET, Sala MF. Características sociodemográficas y clínicas de una población de pacientes con diabetes mellitus. Aten Prim. 2002;29:474–80. 15. Hautala N, Aikkila R, Korpelainen J, Keskitalo A, Kurikka A, Falck A, et al. Marked reductions in visual impairment due to diabetic retinopathy achieved by efficient screening and timely treatment. Acta Ophthalmol. 2014;92:582–7. 16. Hautala N, Hyytinen P, Saarela V, Hägg P, Kurikka A, Runtti M, et al. A mobile eye unit for screening of diabetic retinopathy and follow-up of glaucoma in remote locations in northern Finland. Acta Ophthalmol. 2009;87:912–3. 17. Jivraj I, Ng M, Rudnisky CJ, Dimla B, Tambe E, Nathoo N, et al. Prevalence and severity of diabetic retinopathy in Northwest Cameroon as identified by teleophthalmology. Telemed J E Health. 2011;17:294–8. 18. Peng J, Zou H, Wang W, Fu J, Shen B, Bai X, et al. Implementation and first-year screening results of an ocular telehealth system for diabetic retinopathy in China. BMC Health Serv Res. 2011;11:250. 19. Sender Palacios MJ, Vernet Vernet M, Maseras Bové M, Salvador Playà A, Pascual Batlle L, Ondategui Parra JC, et al. Oftalmopatía en la diabetes mellitus: detección desde la Atención Primaria de salud. Aten Prim. 2011;43:41–8. 20. Deb-Joardar N, Germain N, Thuret G, Manoli P, Garcin AF, Millot L, et al. Screening for diabetic retinopathy by ophthalmologists and endocrinologists with pupillary dilation and a nonmydriatic digital camera. Am J Ophthalmol. 2005;140:814–21. 21. Beynat J, Charles A, Astruc K, Metral P, Chirpaz L, Bron AM, et al. Screening for diabetic retinopathy in a rural French population with a mobile non-mydriatic camera. Diabetes Metab. 2009;35:49–56. 22. Surendran TS, Raman R. Teleophthalmology in diabetic retinopathy. J Diabetes Sci Technol. 2014;8:262–6. 23. Lopez-Bastida J, Cabrera-Lopez F, Serrano-Aguilar P. Sensitivity and specificity of digital retinal imaging for screening diabetic retinopathy. Diabet Med. 2007;24:403–7. 24. Cabrera-López F, Cardona-Guerra P, López-Bastida J, Díaz-Arriaga J. Evaluación de la efectividad y coste-efectividad de la imagen digital en el diagnóstico de la retinopatía diabética. Arch Soc Canar Oftal. 2004;15:21–31. 25. Chasan JE, Delaune B, Maa AY, Lynch MG. Effect of a teleretinal screening program on eye care use and resources. JAMA Ophthalmol. 2014;132:1045–51. 26. Jones S, Edwards RT. Diabetic retinopathy screening: a systematic review of the economic evidence. Diabet Med. 2010;27:249–56. 27. Whited JD, Datta SK, Aiello LM, Aiello LP, Cavallerano JD, Conlin PR, et al. A modelled economic analysis of a digital tele-ophthalmology system as used by three federal health care agencies for detecting proliferative diabetic retinopathy. Telemed J E Health. 2005;11:641–51. 28. Javitt JC, Aiello LP, Chiang Y, Ferris FL III, Canner JK, Greenfield S. Preventive eye care in people with diabetes is cost-saving to the federal government: implications for health-care reform. Diabetes Care. 1994;17:909–17.
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29. Abreu Reyes P, Gil Hernández MA, Abreu González R. Telemedicina en el screening de la retinopatía diabética: nuestra experiencia. Arch Soc Canar Oftal. 2003;14: 21–4. 30. López Bastida J, Soto Pedre E, Cabrera López FA. Revisión sistemática y análisis coste-efectividad del cribado de retinopatía diabética con retinógrafo no midriático de 45◦
mediante imágenes interpretadas por oftalmólogos frente a médicos de familia. Santa Cruz de Tenerife: Servicio Canario de Salud; 2008. 31. Murgatroyd H, Ellingford A, Cox A, Binnie M, Ellis JD, MacEwen CJ. Effect of mydriasis and different field strategies on digital image screening of diabetic eye disease. Br J Ophthalmol. 2004;88:920–4.
ARCHIVOS DE LA SOCIEDAD ESPAÑOLA DE OFTALMOLOGÍA www.elsevier.es/oftalmologia
Original article
Tele-ophthalmology for diabetic retinopathy screening: 8 years of experience夽 A. Pareja-Ríos a , S. Bonaque-González b,c , M. Serrano-García a,∗ , F. Cabrera-López d , P. Abreu-Reyes e , M.D. Marrero-Saavedra f a
Hospital Universitario de Canarias, La Laguna, Tenerife, Spain Departamento de Física, Universidad de La Laguna, La Laguna, Santa Cruz de Tenerife, Spain c Grupo de Ciencias de la Visión, Universidad de Murcia, Murcia, Spain d Complejo Hospitalario Universitario Insular Materno-Infantil, Las Palmas de Gran Canaria, Spain e Hospital Universitario Nuestra Senora ˜ de Candelaria, Santa Cruz de Tenerife, Spain f Hospital Universitario de Gran Canaria Dr. Negrín, Las Palmas de Gran Canaria, Spain b
a r t i c l e
i n f o
a b s t r a c t
Article history:
Purpose: To describe the results of a diabetic retinopathy screening program implemented
Received 29 March 2016
in a primary care area.
Accepted 16 August 2016
Methods: A retrospective study was conducted using data automatically collected since the
Available online xxx
program began on 1 January 2007 until 31 December 2015.
Keywords:
patients in 2007 to 42,339 diabetic patients in 2015. Furthermore, the ability of family doctors
Results: The number of screened diabetic patients has progressively increased from 7173 Diabetic retinopathy
to correctly interpret retinographies has improved, with the proportion of retinal images
Diabetes mellitus
classified as normal having increased from 55% in 2007 to 68% at the end of the study period.
Telemedicine
The proportion of non-evaluable retinographies decreased to 7% in 2015, having peaked at
Optical coherence tomography
15% during the program. This was partly due to a change in the screening program policy
Primary health care
that allowed the use of tropicamide. The number of severe cases detected has declined from 14% with severe non-proliferative and proliferative diabetic retinopathy in the initial phase of the program to 3% in 2015. Conclusions: Diabetic eye disease screening by tele-ophthalmology has shown to be a valuable method in a growing population of diabetics. It leads to a regular medical examination
夽 Please cite this article as: Pareja-Ríos A, Bonaque-González S, Serrano-García M, Cabrera-López F, Abreu-Reyes P, Marrero˜ Saavedra MD. Teleoftalmología para el cribado de la retinopatía diabética: experiencia de 8 anos. Arch Soc Esp Oftalmol. 2016. http://dx.doi.org/10.1016/j.oftal.2016.08.006 ∗ Corresponding author. E-mail address: [email protected] (M. Serrano-García). ˜ ˜ S.L.U. All rights reserved. 2173-5794/© 2016 Sociedad Espanola de Oftalmolog´ıa. Published by Elsevier Espana,
OFTALE-1078; No. of Pages 8
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of patients, helps ease the workload of specialized care services and favors the early detection of treatable cases. However, the results of implementing a program of this type are not immediate, achieving only modest results in the early years of the project that have improved over subsequent years. ˜ ˜ S.L.U. All rights © 2016 Sociedad Espanola de Oftalmolog´ıa. Published by Elsevier Espana, reserved.
Teleoftalmología para el cribado de la retinopatía diabética: experiencia ˜ de 8 anos r e s u m e n Palabras clave:
Objetivo: Mostrar los resultados de un programa de cribado de la retinopatía diabética desde
Retinopatía diabética
el ámbito de la atención primaria.
Diabetes mellitus
Métodos: Se realizó un estudio retrospectivo de los datos recogidos mediante registro infor-
Telemedicina
mático automatizado desde el 1 de enero de 2007, hasta el 31 de diciembre de 2015.
Tomografía de coherencia óptica
Resultados: El número de pacientes cribados aumentó progresivamente desde 7.173 en 2007
Atención primaria
hasta 42.339 en 2015. Asimismo, la habilidad de los médicos de familia en la interpretación de retinografías mejoró progresivamente, clasificando como normales un 55% de las retinografías en 2007, llegando a un 68% en 2015. El número de retinografías consideradas no valorables disminuyó a lo largo del programa, registrándose picos de hasta el 15% y situándose en un 7% en 2015, en parte gracias a un cambio en la normativa, que permitió dilatar la pupila. Se detectaron cada vez menos casos graves, pasándose de un 14% de retinopatías diabéticas no proliferativas severas y proliferativas al inicio del programa a un 3% en 2015. Conclusiones:
El cribado de la oftalmopatía diabética mediante teleoftalmología se
reveló como un método muy valioso en una población en crecimiento como es la diabética, facilitando las revisiones al usuario, ayudando a descongestionar los servicios de atención especializada y detectando los casos tratables con mayor precocidad. Sin embargo, los efectos de la implantación no fueron inmediatos, obteniéndose unos resultados modestos en ˜ ˜ los primeros anos del proyecto, que mejoraron en los anos subsiguientes. ˜ ˜ S.L.U. Todos © 2016 Sociedad Espanola de Oftalmolog´ıa. Publicado por Elsevier Espana, los derechos reservados.
Introduction The worldwide growth of the number of patients with diabetes type I is a fact,1 while type II diabetes is growing exponentially.2 It is estimated that in Europe about 53,000,000 adults have diabetes, nearly 8.1% of the adult population and that, by 2030, 9.5% of the adult population will have diabetes.3 In Spain, diabetes affects 13.8% of which 7.8% has recognized diabetes whereas the remaining 6% is not aware of having diabetes.4 In this scenario, health systems are facing the challenge of rapidly assessing a very large and growing population. Significant efforts have been made in the past few years to identify diabetes at an early stage. This identification is important for ophthalmology specialists because an undiagnosed diabetes patient cannot be included in the screening program for diabetic retinopathy. Such programs have gained importance as the advanced stages of diabetic retinopathy and diabetic macular edema constitute two of the main irreversible vision impairment causes in developed countries5,6 in addition to being one of the main causes of blindness.7
According to the American Diabetes Association and the American Ophthalmology Academy, an ocular fundus examination at least once a year is necessary for diabetes patients in order to identify possible lesions.8,9 This recommendation is based on the fact that, according to the World Health Organization, early treatment of diabetic retinopathy could reduce severe visual impairment risk in over 90%.10 Accordingly, the objective is early detection of patients in order to administer treatment before visual impairment becomes substantial and irreversible. However, not all patients undergo examinations once a year and it is estimated that up to 30% of all diabetes patients have never undergone an ophthalmological examination and that many of these could have undiagnosed ocular diseases.11–14 One of the proposed solutions for improving care of these patients is tele-ophthalmology. Digital photography and telemedicine are arising as strategies to facilitate access to healthcare all over the world. In similar studies, tele-ophthalmology has shown to be effective
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and cost-efficient15–24 and it seems particularly indicated as a method for extending medical care to remote populations.25–28 Considering the geographic characteristics of the Autonomous Community of the Canary Islands, a territory comprising 7 islands (some of which do not have a resident ophthalmologist), in 2002 a tele-ophthalmology program was launched for screening diabetic retinopathy with the objective of improving access to health services for diabetic patients.29 To this end, general practitioners were trained in a structured accreditation program to interpret ocular fundus photographs of their diabetes patients and referring pathological or doubtful cases to the ophthalmologist for a telematic assessment and to decide whether the patient should be examined at the ophthalmology practice. The present study describes the experience of said program (Retisalud) from January 1, 2007 up to December 31, 2015 in the Autonomous Community of the Canary Islands.
Material and methods The objective of this program is to screen for diabetic retinopathy analyzing ocular fundus images for the highest possible number of patients who meet the inclusion criteria of being affected by diabetes mellitus type I or 2 and do not meet any of the following exclusion criteria: (1) age under 15 (or before adolescence); (2) having a diagnostic of moderate or higher retinopathy, or macular edema; (3) having an ocular disease diagnostic (CIE-9) incompatible with screening (such as amaurosis or severe vision impairment, or awaiting ocular surgery such as cataracts or the like); (4) being a patient registered at another autonomous community; (5) being at home and unable to move; (6) having a registered ophthalmic control in a private or private-public regimen, and (7) being excluded from the program for any other reason. To fulfill said objectives, non-mydriatic Topcon TRC-NW6S cameras and subsequent models with similar features (Topcon Corporation, Tokyo, Japan) were progressively installed in 43 health centers uniformly distributed throughout the autonomous community in accordance with the population to be screened in each center. Said devices comprise a nonmydriatic retinal digital camera taking color photographs of the posterior pole and the peripheral retina. Images are taken in true color (24 bits) at a resolution of 1490 × 960 pixels. The procedure for focusing and centering the retinal image is simple and software-assisted. The photographer can see each image immediately after being captured and can repeat the process is the image is not adequate. The staff in charge of capturing images, mostly clinic personnel and nurses, were trained to ensure adequate image quality. In addition, training courses were held for family physicians, who had this service included in the list of objectives as an incentive. After said training, the physicians underwent an examination which established that the number of errors in 200 retinography readings should be under 30%. In December 2015, 1177 family physicians in the Autonomous Community of the Canary Islands were accredited for this activity. In addition, their work was followed up and additional seminars and accredited
Table 1 – Demographic data of diabetes patients and patients screened in the program from 2007 to 2015. Year
Estimated number of diabetes patients in the program
Number of screened patients (percentage of total number)
2007 2008 2009 2010 2011 2012 2013 2014 2015
73,326 85,598 98,891 109,323 146,702 144,177 145,313 132,674 128,975
7173 (9.78) 11,449 (13.38) 14,345 (14.51) 19,320 (17.67) 24,006 (16.36) 31,460 (21.82) 40,786 (28.07) 45,726 (34.46) 42,339 (32.83)
courses were provided to all health centers who required or requested it. Said seminars and courses explained the most frequent errors detected in the interpretation of retinographies and requested collaboration. At present, said training is continuing in health centers where the follow-up of diabetes patients is below average or those who request it as a part of their ongoing training program. The program is based on opportunistic screening as this region, similarly to other autonomous communities of Spain, does not carry a census of diabetes patients, which excludes systematic screening. Accordingly, only the diabetic patients that concerned with their general practitioner for different medical reasons can be included in the screening. The screening protocol consists in capturing an ocular fundus image centered on the macula, mostly without pupil dilatation up to the end of 2014 and utilizing pupil dilatation ® with a single tropicamide drop (Colircusí Tropicamida Alcon Cusí, SA, El Masnou, Barcelona, Spain) as from January 2015 when the quality of the retinography was considered inadequate. Said images are classified as invalid if they do not enable the observer to determine the presence or absence of disease. Valid images are classified as normal, pathological or doubtful. The procedure to be followed is shown in the flowchart of Fig. 1. It must be noted that if the image is classified as pathological, doubtful or invalid by the primary health care physician, the image is remotely screened in a second stage by a specialized care ophthalmologist. As the clinical data obtained during said process could be crucial for future nationwide programs, all the program outputs have been saved on automated computer records from the first years of the program. The same computer application used by general practitioners and ophthalmologists to check the retinographs also stores data on waiting time for image assessment and results.
Results The results detailed below are global and not segmented for each of the 7 islands because the distribution of cameras took into account the population of each district, with results being relatively homogeneous and all islands. Table 1 shows the number and percentage of diabetic patients against the total for the year that were assessed by the screening program. A growing trend can be appreciated,
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New image in 2 years
Image analysis by family physician
New image in one year
Yes
No
Classified as normal?
Any risk factors or diabetes with over 10 years evolution?
Yes
No
Remote assessment of image by ophthalmologist
Severe pathology or invalid image
Moderate pathology
Referral to reference hospital
Referral to district ophthalmologist
No pathology or risk factors
Slight pathology and risk factors
Fig. 1 – Screening process flowchart.
in which nearly 33% of the diabetic population was examined after 8 years. As the number of patients with diagnosed diabetes also increased, the program examined 6 times more patients in 2015 than in 2007. Fig. 2 illustrates the percentage of tests against the total considered by the general practitioner as normal, invalid or pathological/doubtful. The percentage of normal tests varied throughout the program between 54 and 68%. In the last 3 years, the primary health care physicians diagnosed a higher percentage of images as normal.
Images assessed by primary care physicians
80% 70%
68% 64%
60%
55%
57%
56%
55%
62%
59% 54%
%
50% 40%
35%
35%
35%
34% 29%
30%
29% 25%
25%
20% 10%
31%
10%
12%
10%
9%
15% 11%
9%
9%
7%
0% 2007
2008
2009
2010
2011
2012
2013
2014
2015
Year Invalid
Pathological/doubtful
Normal
Fig. 2 – Classification of retinographies by primary care physicians.
A number of factors took part in images being classified as invalid by the primary health care physicians, including opacity, typical old-age myosis or inadequate capturing technique. Fig. 2 shows the range between 9 and 50% with relative stability, excepting 2015 where the best values were achieved (7%) due to the use of tropicamide applied to all patients when adequate images could not be obtained. Similarly, the percentage of photographs classified as pathological or doubtful and referred to the specialist for remote assessment remained between 25 and 35%, although Fig. 2 shows that in the latest years the rights diminished. This is a good sign, considering that the highest number of patients was examined. Fig. 3 shows the amount of images classified as normal, invalid or pathological that were referred to the ophthalmology experts for remote assessment. It can be seen that the percentage of images classified as normal remained relatively stable despite the increase in the number of screened patients, which peaked in the last year. The proportion between referred images and those considered as invalid reached the lowest number in the last year. Due to the increase of the examined population year after year, in 2012, 2013, 2014 and 2015 ophthalmologists received 1900, 2135, 2279 and 1133 images that were finally classified as invalid. This number is significant because all the rejected retinographies are removed from the network and the patients must be examined by an ophthalmologist under pharmacological midriasis. Even
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250
Images assessed by specialized physicians 70%
200
63%
196
60%
42%
50%
52%
50%
47%
47% 42% 42%
41%
38%
37%
37%
36%
%
40%
16%
17%
100 47 34
50 28
0 2006
14%
13%
12%
9%
9%
16%
126
49 27%
20%
150
34%
30%
10%
Days
50%
49%
50%
2007
29
2008
28
2009
20
19 20
2010
12
2011
9
2012
19
2013
23 20
2014
22 19
2015
Year
9%
Family physician
Ophthalmologist
0% 2007
2008
2009
2010
2011
2012
2013
2014
2015
Fig. 5 – Waiting days for each retinograph to be assessed by the family physician and the ophthalmologist, respectively.
Year Invalid
Pathological
Normal
Fig. 3 – Classification by ophthalmology specialists of retinographies sent for remote assessment.
Discussion
though in this group of patients ocular fundus exploration was normal in a high percentage of cases, 30% exhibited diabetic retinopathy. Fig. 4 shows the classification of images classified as pathological as “slight or moderate” and “severe or higher” according to the ophthalmologists. The percentage of images that revealed severe or higher disease diminished year after year even though the number of patients progressively increased as mentioned above. Finally, Fig. 5 shows the mean waiting time for each retinograph before being assessed by the general practitioner or the ophthalmologist. In the case of the former, the waiting time showed a clearly descending trend with larger waiting times in the first 2 years of the project and progressively descending each year as the physicians included the assessment of said images in their daily practice. This was supported by the inclusion of this task as an objective to be assessed in incentives.
Classification of diabetic retinopathy by specialized physicians 120% 100% 86%
91% 83%
80%
80%
93%
93%
97%
80%
%
66%
60% 40% 20%
34%
14%
17%
20%
20% 9%
7%
7%
3%
0% 2007
2008
2009
2010
2011
2012
2013
2014
2015
Year Slight or moderate
Severe or superior
Fig. 4 – Grade of diabetic retinopathies identified remotely and classified by ophthalmology physicians.
In 2015, the Autonomous Community of Canary Islands had a population of approximately 2,100,306 inhabitants distributed in 7 main islands, of which approximately 221,000 were diabetics. As the number of ophthalmologists is approximately 160, each one should examine 7 diabetic patients every working day in order to screen each patient once a year. For this reason, in 2006 it was decided to implement a teleophthalmology system involving the primary health care of the region. The program is based on the family physicians who perform the metabolic control of the patients and are familiar with the comorbidities caused by the disease to generally monitor the condition of the retina. Family physicians already follow-up the microvascular complications of diabetes such as nephropathy or neuropathy and refer patients to nephrologists or neurologists only when specific thresholds have been exceeded. This makes family physicians adequate for assessing an additional microvascular complication such as the ocular fundus of patients. However, numerous obstacles appeared during the deployment of the program, particularly in the beginning. On the one hand, ophthalmologists had the feeling that the family physician could take over their functions, and in turn the latter felt that this new function would worsen their workload and raised fear of legal liabilities that could be derived from erroneously classifying a retinography as normal. A further obstacle was the high initial cost of the program for the health system, comprising equipment, training for technicians and physicians as well as follow-up programs, despite the fact that diminished prevalence of blindness and visual impairment as well as the improvement of specialized care obviously diminished the overall cost for the health system. However, previous financial studies involving similar programs evidenced that when adding up all the costs (direct costs for health services, for patients and productivity losses) these programs are cost effective.30 Throughout the 8 years of the program, the overall number of screened patients progressively increased to reach 42,339 in 2015, representing 32.83% of the estimated population of diabetics that year. Even though apparently the percentage of patients screened in 2015 could seem small considering the
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duration of the project, it must be taken into account that in the past the entire diabetic population was examined only by ophthalmology specialists in hospitals or in specialized care centers. Considering that the program supplemented existing services, a larger number of patients are still examined by their specialist in Social Security services, who receive ophthalmic attention through private insurances or who do not meet the characteristics to enter the program. On the other hand, in the past 2 years it was decided to screen patients who did not show signs of diabetic retinopathy (approximately 70%) at two-year intervals, which produced a significant reduction in the percentage of screened patients. A survey was carried out to obtain an estimate of the actual percentage of diabetic patients with ophthalmic examinations among 20 pharmacies of the region, both in rural and urban areas (results not published). The survey consisted in asking all diabetes patients to visit one of said pharmacy for any reason if their ocular fundus was regularly examined. In the survey, 82.6% of respondents indicated they underwent a regular ocular fundus examination through the Retisalud program, with their district ophthalmologist or in public or private hospitals. Even though a formal survey designed to ensure a representative sample of the diabetes population would be necessary to determine this information with greater precision, the results evidenced that the volume of diabetes patients with ophthalmological follow-up in the islands is much higher than those registered in the screening program. In addition, the figures and tables demonstrate that in 2015 ophthalmologists remotely assessed 7742 images that were considered as pathological, doubtful or invalid by the general practitioners and eventually were normal or invalid. However, it must be taken into account that these assessments take up significantly less time than examining each patient in the practice. In said year, 32,946 images were assessed as normal by family physicians, representing a high number of patients who did not visit the ophthalmology practice for the annual ocular fundus examination. Adding up all factors, the program enables a considerable reduction of the workload of the ophthalmology practices, allowing the specialists to dedicate more time to treatments instead of screening. In addition, it must be taken into account that the Retisalud program enables assessments of over 3000 pathological patients in 2015 who otherwise would have not been examined. In addition, family physicians felt increasingly confident to classify an image as normal (Fig. 2). During the first years of the program they referred the retinographs for expert assessment upon the slightest doubt, whereas after several years of experience they classified an increasing percentage as normal, to the point that in the last 3 years family physicians classified more retinographies as normal and less as invalid, pathological or doubtful. More importantly, the percentage of patients with severe retinopathy has diminished every year (Fig. 4), evidencing an increasingly effect to control the target population and enabling the identification of disease at early stages. An added advantage of the program is that frequent network communication has created communications channels between family physicians and ophthalmologists, which
has enabled the detection and consultation of ocular diseases other than those caused by diabetes. One of the challenges to overcome is to improve the number of invalid images. In this study, the percentage thereof increased regularly and peaked in 2012 (Fig. 2), matching the inclusion of numerous technicians and nurses in the program. It is likely that the learning curve negatively influenced the statistics of that year. The high number of invalid images increases the workload as all patients with invalid retinographies are personally examined at the ophthalmology practices. However, until December 2014 the images were captured without dilatation in the majority of cases. In order to diminish the number of invalid retinographies, since January 2015 and on the basis of similar studies that achieved good results with this strategy20,31 it was agreed that, whenever an adequate image was not obtained despite midriasis in the mesopic conditions in which the images were captured, the patient would be administered a single tropicamide drop. This diminished the number of invalid images when compared to previous years, reaching the lowest numbers since the beginning of the program. On the other hand, the waiting time for examining retinographies exhibited a downward curve both at the ophthalmological and the primary health care level (Fig. 5), being approximately 3 weeks in the past 2 years. As regards potential improvements for the program, studies should be made to verify if the percentage of blindness derived from diabetic retinopathy has diminished (and to what extent) since the deployment of the program. It would also be useful to carry out control studies with protocols, randomly examining retinographies classified as normal by family physicians to assess the degree of sensitivity, although other studies have already evidenced that the level of agreement in diagnostic between primary health care physicians and ophthalmologists means that the examination of diabetes patients by primary health care physicians is reliable.19 The proposed improvements include the possibility of a diabetics census in order to automatically issue an appointment for capturing a retinography as soon as the patient is diagnosed with diabetes as well as establishing the periodicity thereof. Even though this measure would not prevent the absenteeism of patients who do not attend their appointments, it would enable the inclusion of all diabetics in the program and not only those who visit their family physician. On the other hand, it would be interesting to have an improved software protocol enabling easy access to previous patient retinographies. In addition, the possibility of capturing a second image focused on the optic nerve, including the proximal nasal area, is being considered to improve screening sensitivity. A further possibility is the use of automated software for identifying pathological images as well as the possibility of using combined OCT/retinograph systems, particularly in densely populated areas, that could also enable early detection of diabetes macular edema. Other studies have recommended the presence of the optician-optometrist in primary health centers on the basis that the optometrist optician is recognized as a health professional.19 This would easily increase patient examinations with visual acuity tests, tonometry or additional images focused
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on the optic nerve and the peripheral retina, thus increasing the scope of the screening to cover other diseases. In conclusion, said program is providing positive results, demonstrating that diabetic ophthalmopathy screening with tele-ophthalmology presents great potential, particularly considering the growth of the diabetic population and the small number of specialists. In addition, it exhibits the advantage of enhancing the relationship between family physicians and specialized health professionals.
Conflict of interest No conflict of interest has been declared by the authors.
Acknowledgments The authors wish to express their gratitude to the staff of the regional government for providing necessary data: Carmen Gloria Rodríguez Valerón, Santiago de la Huerga Moreno and María Rocío Ávarez Sánchez, as well to all staff (technicians, clinical assistance, University nurse graduates, primary health care physicians and ophthalmologists) who have supported Retisalud and make it a live program.
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