Letter to the Editor Open Access
Copyright ©The Author(s) 2024. Published by Baishideng Publishing Group Inc. All rights reserved.
World J Diabetes. Aug 15, 2024; 15(8): 1820-1823
Published online Aug 15, 2024. doi: 10.4239/wjd.v15.i8.1820
Enhancing diabetic retinopathy screening: Non-mydriatic fundus photography-assisted telemedicine for improved clinical management
Kira J Szulborski, David J Ramsey, Department of Ophthalmology, Tufts University School of Medicine, Boston, MA 02111, United States
Kira J Szulborski, David J Ramsey, Lahey Department of Surgery, Division of Ophthalmology, UMass Chan Medical School, University of Massachusetts, Burlington, MA 01805, United States
David J Ramsey, Graduate Faculty, New England College of Optometry, Boston, MA 02115, United States
ORCID number: Kira J Szulborski (0009-0002-1618-7431); David J Ramsey (0000-0002-5504-812X).
Author contributions: Szulborski KJ and Ramsey DJ designed and performed the research, and wrote and revised the manuscript. All authors have read and approved the final manuscript.
Conflict-of-interest statement: All the authors report no relevant conflicts of interest for this article.
Open-Access: This article is an open-access article that was selected by an in-house editor and fully peer-reviewed by external reviewers. It is distributed in accordance with the Creative Commons Attribution NonCommercial (CC BY-NC 4.0) license, which permits others to distribute, remix, adapt, build upon this work non-commercially, and license their derivative works on different terms, provided the original work is properly cited and the use is non-commercial. See: https://creativecommons.org/Licenses/by-nc/4.0/
Corresponding author: David J Ramsey, MD, PhD, MPH Associate Professor, Lahey De-partment of Surgery, Division of Ophthalmology, UMass Chan Medical School, University of Massachusetts, 41 Mall Road, Burlington, MA 01805, United States. david.j.ramsey@lahey.org
Received: March 31, 2024
Revised: May 29, 2024
Accepted: June 21, 2024
Published online: August 15, 2024
Processing time: 116 Days and 10.2 Hours

Abstract

The utilization of non-mydriatic fundus photography-assisted telemedicine to screen patients with diabetes mellitus for diabetic retinopathy provides an accurate, efficient, and cost-effective method to improve early detection of disease. It has also been shown to correlate with increased participation of patients in other aspects of diabetes care. In particular, patients who undergo teleretinal imaging are more likely to meet Comprehensive Diabetes Care Healthcare Effectiveness Data and Information Set metrics, which are linked to preservation of quality-adjusted life years and additional downstream healthcare savings.

Key Words: Diabetes; Diabetic retinopathy; Telemedicine; Tele-ophthalmology; Non-mydriatic fundus photography-assisted telemedicine; Vision screening; Preventative health services; Health policy

Core Tip: Point-of-care screening for diabetic retinopathy by means of teleretinal imaging provides an effective and economical method to improve early detection of eye disease in at-risk populations. Non-mydriatic fundus photography (NMFP)-assisted telemedicine allows critical ophthalmic examinations to reach individuals when resources for eye care are limited or difficult to access. As technology continues to evolve, further research efforts should focus on refining NMFP-assisted telemedicine protocols and evaluating its long-term impact on patient outcomes across the spectrum of healthcare settings.



TO THE EDITOR

Telemedicine screening for eye disease is key to making eye care more available to the growing numbers of individuals with diabetes mellitus (DM) worldwide[1,2]. We read with great interest the paper by Zhou et al[3], which validated the effectiveness of screening patients with DM for diabetic retinopathy (DR) at a major university-based medical center located in Hefei, Anhui Province, China. The authors compared non-mydriatic fundus photography (NMFP)-assisted telemedicine screening with fundus fluorescein angiography as the gold standard for diagnosis and staging of DR. The authors present compelling evidence for the efficacy of NMFP-assisted telemedicine in detecting and staging DR, finding a high degree of consistency between the two modalities. This study has significant implications for improving the early detection of DR, thereby allowing for earlier referrals to ophthalmologists for interventions capable of improving patient outcomes.

We agree with the authors that point-of-care screening for DR incorporating teleretinal imaging (TRI) offers an accurate and cost-effective means for improving early detection of disease in at-risk populations[4-7]. It also has the advantage of increasing patient participation in the care of their DM[8-12] and allows optimal resource allocation within healthcare systems that are at risk of becoming overextended[13-16]. For a comprehensive review of the diagnostic accuracy of telemedicine screening protocols for the detection of DR in various settings see the meta-analysis by Mehraban Far et al[17]. However, there is an equal, if not a greater, value derived from the use of TRI to screen lower-risk populations. In this context, its introduction could also reduce the costs associated with diabetic eye examinations, especially for patients without prior evidence of DR or who have completed a comprehensive eye examination within the prior year[18,19]. We particularly want to commend the authors for including in their discussion due attention to how the use of a hand-held NMFP allows for increased accessibility for certain patients who would otherwise be unable to avail themselves of traditional fixed ocular imaging or fundus examining devices. This flexibility, combined with their generally lower acquisition costs and portability, is one of the most compelling reasons for advocating for the expanded use of hand-held fundus cameras.

Though the authors highlighted several significant advantages of NMFP-assisted telemedicine screening, we feel that further discussion is warranted encompassing a broader view of the full extent of their potential benefits for comprehensive diabetes care. Our own recent study examined the factors associated with the utilization of point-of-care TRI for DR screening in a primary care setting in the United States[20]. The patients screened in our study were well-insured, suburban patients. They included both sexes, spanned a broad range of ages, types of health insurance, and, to a lesser extent, races. In this population, we found that participation in TRI was closely associated with the completion of other Comprehensive Diabetes Care Healthcare Effectiveness Data and Information Set (HEDIS) metrics. In particular, those patients screened were more likely to have had their hemoglobin A1c and microalbumin levels measured[21]. This combination of earlier and more regular DR screening, as well as the completion of HEDIS metrics, has the potential to improve more than just the ocular health of these patients. Furthermore, the detection of DR and other diabetes-associated complications may allow for the timely initiation of treatments that may preserve or prevent loss of quality-adjusted life years[22]. Finally, a more complete analysis of the cost-effectiveness of these technologies ought to take into consideration additional indirect economic benefits brought about by the earlier detection and treatment of diabetes-associated complications, as well as the costs linked to downstream healthcare service utilization[23].

One of the features of the manuscript by Zhou et al[3] that may cause difficulties for some readers is the use of non-standard abbreviations and nomenclature for certain aspects of diabetic eye disease. For example, the use of the acronym “NDR” to describe patients with “no” DR is very similar to the clinical acronym in common use for nonproliferative diabetic retinopathy, NPDR, and may potentially cause confusion. There is also use of some less common terminology for features associated with DR. For example, in place of the term “microhemangioma” in the context of DR, we recommend using more established terminology to describe small vascular abnormalities such as “microaneurysms” or “intraretinal microvascular abnormalities”. The study also does not utilize the most current definition of DR staging. The authors mention relying on the International Federation of Ophthalmological Societies’ guidelines for DR screening and staging established in 2002. We urge consultation of more up-to-date standards on diagnosis, management, and treatment of diabetic eye disease such as those published by the American Academy of Ophthalmology and American Diabetes Association[1,2]. Finally, the discussion would have benefited from a more comprehensive examination of the potential limitations and challenges associated with NMFP-assisted telemedicine. These issues include acknowledgement of the barriers related to patient and provider acceptance of TRI technology, the need to put in place robust data security to protect patient privacy, and the requirement for an adequate referral system to ophthalmologists and retina specialists to assure timely monitoring and treatment of any patients identified to have DR. By addressing these needs, researchers can refine NMFP-assisted telemedicine protocols and increase their implementation in clinical practice.

These issues aside, we want to emphasize that the authors deserve to be recognized for their forward-thinking approach to the introduction of TRI in an underserved population in a major urban center in a Chinese province that has undergone rapid development. Teleophthalmology has been successfully employed in China for many years[24,25]. Elsewhere in Asia, Singapore’s Integrated Diabetic Retinopathy Program has also demonstrated significant cost savings, without sacrificing health outcomes in an urban population[4]. Importantly, countries that have established universal DR screening programs supported by registries, such as in the United Kingdom, have achieved considerably higher screening rates among eligible patients with DM and have successfully reduced the incidence of blindness associated with DR[22].

Our own research, as well as many others, focused on the use of TRI in primary medical care settings[21]. It is exciting to see this technology extended for use in an endocrinology department by Zhou et al[3]. Endocrinologists see a larger proportion of patients with DM that is often more challenging to control or of longer duration[26]. Many of the patients in this study by Zhou et al[3] would, therefore, not likely be considered low-risk for DR. Including additional demographic details such as age and sex distribution, duration of DM, and socioeconomic status would help readers better assess the generalizability of their findings to other populations. Nevertheless, this setting may explain the very high rate of DR encountered in their study population, which is well above the rate expected in the overall diabetic population, including in China[24,25]. In the United States, most of those patients would not generally be monitored by means of NMFP-assisted telemedicine to screen for vision-threatening eye disease.

In conclusion, the study by Zhou et al[3] contributes significantly to the literature on DR screening, and it underscores the potential of NMFP-assisted telemedicine in improving early detection and management of DR. As technology continues to evolve, further research efforts should focus on refining NMFP-assisted telemedicine protocols, integrating them into current healthcare practice standards, and evaluating their long-term impact on patient outcomes.

ACKNOWLEDGEMENTS

The authors thank Dr. Shiyoung Roh, Dr. Jeffrey L. Marx, and Dr. John T. Ramsey, as well as Carol Spencer, Lahey Hospital Librarian, for research support. This work was performed as part of regular employment duties at the Lahey Hospital & Medical Center, Beth Israel Lahey Health.

Footnotes

Provenance and peer review: Unsolicited article; Externally peer reviewed.

Peer-review model: Single blind

Specialty type: Endocrinology and metabolism

Country of origin: United States

Peer-review report’s classification

Scientific Quality: Grade D

Novelty: Grade C

Creativity or Innovation: Grade B

Scientific Significance: Grade C

P-Reviewer: Gaurav K S-Editor: Wang JJ L-Editor: A P-Editor: Chen YX

References
1.  Wong TY, Sun J, Kawasaki R, Ruamviboonsuk P, Gupta N, Lansingh VC, Maia M, Mathenge W, Moreker S, Muqit MMK, Resnikoff S, Verdaguer J, Zhao P, Ferris F, Aiello LP, Taylor HR. Guidelines on Diabetic Eye Care: The International Council of Ophthalmology Recommendations for Screening, Follow-up, Referral, and Treatment Based on Resource Settings. Ophthalmology. 2018;125:1608-1622.  [PubMed]  [DOI]  [Cited in This Article: ]  [Cited by in Crossref: 273]  [Cited by in F6Publishing: 407]  [Article Influence: 67.8]  [Reference Citation Analysis (0)]
2.  American Diabetes Association Professional Practice Committee. 12. Retinopathy, Neuropathy, and Foot Care: Standards of Care in Diabetes-2024. Diabetes Care. 2024;47:S231-S243.  [PubMed]  [DOI]  [Cited in This Article: ]  [Cited by in Crossref: 1]  [Cited by in F6Publishing: 22]  [Article Influence: 22.0]  [Reference Citation Analysis (0)]
3.  Zhou W, Yuan XJ, Li J, Wang W, Zhang HQ, Hu YY, Ye SD. Application of non-mydriatic fundus photography-assisted telemedicine in diabetic retinopathy screening. World J Diabetes. 2024;15:251-259.  [PubMed]  [DOI]  [Cited in This Article: ]  [Reference Citation Analysis (1)]
4.  Nguyen HV, Tan GS, Tapp RJ, Mital S, Ting DS, Wong HT, Tan CS, Laude A, Tai ES, Tan NC, Finkelstein EA, Wong TY, Lamoureux EL. Cost-effectiveness of a National Telemedicine Diabetic Retinopathy Screening Program in Singapore. Ophthalmology. 2016;123:2571-2580.  [PubMed]  [DOI]  [Cited in This Article: ]  [Cited by in Crossref: 102]  [Cited by in F6Publishing: 133]  [Article Influence: 16.6]  [Reference Citation Analysis (0)]
5.  Gomez-Ulla F, Alonso F, Aibar B, Gonzalez F. A comparative cost analysis of digital fundus imaging and direct fundus examination for assessment of diabetic retinopathy. Telemed J E Health. 2008;14:912-918.  [PubMed]  [DOI]  [Cited in This Article: ]  [Cited by in Crossref: 24]  [Cited by in F6Publishing: 27]  [Article Influence: 1.8]  [Reference Citation Analysis (0)]
6.  Ullah W, Pathan SK, Panchal A, Anandan S, Saleem K, Sattar Y, Ahmad E, Mukhtar M, Nawaz H. Cost-effectiveness and diagnostic accuracy of telemedicine in macular disease and diabetic retinopathy: A systematic review and meta-analysis. Medicine (Baltimore). 2020;99:e20306.  [PubMed]  [DOI]  [Cited in This Article: ]  [Cited by in Crossref: 21]  [Cited by in F6Publishing: 22]  [Article Influence: 5.5]  [Reference Citation Analysis (0)]
7.  Fuller SD, Hu J, Liu JC, Gibson E, Gregory M, Kuo J, Rajagopal R. Five-Year Cost-Effectiveness Modeling of Primary Care-Based, Nonmydriatic Automated Retinal Image Analysis Screening Among Low-Income Patients With Diabetes. J Diabetes Sci Technol. 2022;16:415-427.  [PubMed]  [DOI]  [Cited in This Article: ]  [Cited by in Crossref: 12]  [Cited by in F6Publishing: 19]  [Article Influence: 9.5]  [Reference Citation Analysis (0)]
8.  Chin EK, Ventura BV, See KY, Seibles J, Park SS. Nonmydriatic fundus photography for teleophthalmology diabetic retinopathy screening in rural and urban clinics. Telemed J E Health. 2014;20:102-108.  [PubMed]  [DOI]  [Cited in This Article: ]  [Cited by in Crossref: 37]  [Cited by in F6Publishing: 45]  [Article Influence: 4.1]  [Reference Citation Analysis (0)]
9.  Conlin PR, Fisch BM, Cavallerano AA, Cavallerano JD, Bursell SE, Aiello LM. Nonmydriatic teleretinal imaging improves adherence to annual eye examinations in patients with diabetes. J Rehabil Res Dev. 2006;43:733-740.  [PubMed]  [DOI]  [Cited in This Article: ]  [Cited by in Crossref: 47]  [Cited by in F6Publishing: 52]  [Article Influence: 2.9]  [Reference Citation Analysis (0)]
10.  Boucher MC, Nguyen QT, Angioi K. Mass community screening for diabetic retinopathy using a nonmydriatic camera with telemedicine. Can J Ophthalmol. 2005;40:734-742.  [PubMed]  [DOI]  [Cited in This Article: ]  [Cited by in Crossref: 47]  [Cited by in F6Publishing: 49]  [Article Influence: 2.6]  [Reference Citation Analysis (0)]
11.  Gibson AA, Humphries J, Gillies M, Nassar N, Colagiuri S. Adherence to eye examination guidelines among individuals with diabetes: An analysis of linked health data. Clin Exp Ophthalmol. 2020;48:1229-1238.  [PubMed]  [DOI]  [Cited in This Article: ]  [Cited by in Crossref: 7]  [Cited by in F6Publishing: 10]  [Article Influence: 2.5]  [Reference Citation Analysis (0)]
12.  Gange WS, Xu BY, Lung K, Toy BC, Seabury SA. Rates of Eye Care and Diabetic Eye Disease among Insured Patients with Newly Diagnosed Type 2 Diabetes. Ophthalmol Retina. 2021;5:160-168.  [PubMed]  [DOI]  [Cited in This Article: ]  [Cited by in Crossref: 17]  [Cited by in F6Publishing: 16]  [Article Influence: 5.3]  [Reference Citation Analysis (0)]
13.  Nathoo N, Ng M, Rudnisky CJ, Tennant MT. The prevalence of diabetic retinopathy as identified by teleophthalmology in rural Alberta. Can J Ophthalmol. 2010;45:28-32.  [PubMed]  [DOI]  [Cited in This Article: ]  [Cited by in Crossref: 30]  [Cited by in F6Publishing: 35]  [Article Influence: 2.5]  [Reference Citation Analysis (0)]
14.  Mansberger SL, Sheppler C, Barker G, Gardiner SK, Demirel S, Wooten K, Becker TM. Long-term Comparative Effectiveness of Telemedicine in Providing Diabetic Retinopathy Screening Examinations: A Randomized Clinical Trial. JAMA Ophthalmol. 2015;133:518-525.  [PubMed]  [DOI]  [Cited in This Article: ]  [Cited by in Crossref: 103]  [Cited by in F6Publishing: 124]  [Article Influence: 13.8]  [Reference Citation Analysis (0)]
15.  Joseph S, Kim R, Ravindran RD, Fletcher AE, Ravilla TD. Effectiveness of Teleretinal Imaging-Based Hospital Referral Compared With Universal Referral in Identifying Diabetic Retinopathy: A Cluster Randomized Clinical Trial. JAMA Ophthalmol. 2019;137:786-792.  [PubMed]  [DOI]  [Cited in This Article: ]  [Cited by in Crossref: 15]  [Cited by in F6Publishing: 18]  [Article Influence: 4.5]  [Reference Citation Analysis (0)]
16.  Sharif A, Jendle J, Hellgren KJ. Screening for Diabetic Retinopathy with Extended Intervals, Safe and Without Compromising Adherence: A Retrospective Cohort Study. Diabetes Ther. 2021;12:223-234.  [PubMed]  [DOI]  [Cited in This Article: ]  [Cited by in Crossref: 3]  [Cited by in F6Publishing: 2]  [Article Influence: 0.7]  [Reference Citation Analysis (0)]
17.  Mehraban Far P, Tai F, Ogunbameru A, Pechlivanoglou P, Sander B, Wong DT, Brent MH, Felfeli T. Diagnostic accuracy of teleretinal screening for detection of diabetic retinopathy and age-related macular degeneration: a systematic review and meta-analysis. BMJ Open Ophthalmol. 2022;7:e000915.  [PubMed]  [DOI]  [Cited in This Article: ]  [Cited by in F6Publishing: 9]  [Reference Citation Analysis (0)]
18.  Horton MB, Silva PS, Cavallerano JD, Aiello LP. Operational Components of Telemedicine Programs for Diabetic Retinopathy. Curr Diab Rep. 2016;16:128.  [PubMed]  [DOI]  [Cited in This Article: ]  [Cited by in Crossref: 15]  [Cited by in F6Publishing: 15]  [Article Influence: 1.9]  [Reference Citation Analysis (0)]
19.  Kuo KH, Anjum S, Nguyen B, Marx JL, Roh S, Ramsey DJ. Utilization of Remote Diabetic Retinal Screening in a Suburban Healthcare System. Clin Ophthalmol. 2021;15:3865-3875.  [PubMed]  [DOI]  [Cited in This Article: ]  [Cited by in Crossref: 1]  [Cited by in F6Publishing: 6]  [Article Influence: 2.0]  [Reference Citation Analysis (0)]
20.  National Committee for Quality Assurance  Comprehensive Diabetes Care (CDC). [cited 28 March 2024]. Available from: https://www.ncqa.org/hedis/measures/comprehensive-diabetes-care/.  [PubMed]  [DOI]  [Cited in This Article: ]
21.  Szulborski KJ, Gumustop S, Lasalle CC, Hughes K, Roh S, Ramsey DJ. Factors Associated with Utilization of Teleretinal Imaging in a Hospital-Based Primary Care Setting. Vision (Basel). 2023;7.  [PubMed]  [DOI]  [Cited in This Article: ]  [Reference Citation Analysis (0)]
22.  Pearce E, Sivaprasad S. A Review of Advancements and Evidence Gaps in Diabetic Retinopathy Screening Models. Clin Ophthalmol. 2020;14:3285-3296.  [PubMed]  [DOI]  [Cited in This Article: ]  [Cited by in Crossref: 9]  [Cited by in F6Publishing: 10]  [Article Influence: 2.5]  [Reference Citation Analysis (0)]
23.  Garoon RB, Lin WV, Young AK, Yeh AG, Chu YI, Weng CY. Cost Savings Analysis for a Diabetic Retinopathy Teleretinal Screening Program Using an Activity-Based Costing Approach. Ophthalmol Retina. 2018;2:906-913.  [PubMed]  [DOI]  [Cited in This Article: ]  [Cited by in Crossref: 10]  [Cited by in F6Publishing: 8]  [Article Influence: 1.3]  [Reference Citation Analysis (0)]
24.  Jin K, Lu H, Su Z, Cheng C, Ye J, Qian D. Telemedicine screening of retinal diseases with a handheld portable non-mydriatic fundus camera. BMC Ophthalmol. 2017;17:89.  [PubMed]  [DOI]  [Cited in This Article: ]  [Cited by in Crossref: 38]  [Cited by in F6Publishing: 28]  [Article Influence: 4.0]  [Reference Citation Analysis (0)]
25.  Hao Z, Xu R, Huang X, Ren X, Li H, Shao H. Application and observation of artificial intelligence in clinical practice of fundus screening for diabetic retinopathy with non-mydriatic fundus photography: a retrospective observational study of T2DM patients in Tianjin, China. Ther Adv Chronic Dis. 2022;13:20406223221097335.  [PubMed]  [DOI]  [Cited in This Article: ]  [Reference Citation Analysis (0)]
26.  Grunberger G, Sherr J, Allende M, Blevins T, Bode B, Handelsman Y, Hellman R, Lajara R, Roberts VL, Rodbard D, Stec C, Unger J. American Association of Clinical Endocrinology Clinical Practice Guideline: The Use of Advanced Technology in the Management of Persons With Diabetes Mellitus. Endocr Pract. 2021;27:505-537.  [PubMed]  [DOI]  [Cited in This Article: ]  [Cited by in Crossref: 109]  [Cited by in F6Publishing: 136]  [Article Influence: 45.3]  [Reference Citation Analysis (0)]