Identifying Eye Changes in Children and Adolescents with Congenital Heart Disease with the Aid of a Smartphone: An Observational Study
Main Article Content
Abstract
Background: Among congenital diseases, congenital heart disease is one of the most frequent defects, accounting for high morbidity and mortality rates. Coexistence of ocular sequelae, especially in retinal microvascularization, is frequent, and may be a marker of vascular damage and severity of underlying disease.
Aims: To identify ocular anatomical repercussions in children with congenital heart diseases; to describe the prevalence of potential markers associated with retinal vessels using a smartphone.
Methods: This was a cross-sectional observational study with children diagnosed with congenital heart disease treated at the Instituto de Cardiologia in Porto Alegre-RS from 4 up to (but not over) 18 years old.
Results: Of a total of 218 patients assessed, 206 were included in the study. Mean age was 10.19 years +- 3.88. Uncorrected visual acuity poorer than 0.6 in at least one eye was found in 11.65% (24) of all patients. Regarding retinal findings, estimated mean arterial tortuosity was 437.79 μm, and estimated mean venous tortuosity was 336.41 μm. Taking only the cyanotic group, the arterial mean reached 557.29 μm, and the venous mean reached 401.86 (p=.001 and p=.004, respectively). In the multivariate analysis, estimated mean arterial tortuosity of cyanotic patients undergoing clinical treatment was 699.13 μm versus 489.74 μm for those without clinical treatment (p<0.001).
Conclusion: Presence of retinal vascular tortuosity, especially in the arterial bed, is associated with cyanotic CHD. Identification of ocular changes, especially through an easily accessible and universal method such as the smartphone, may have diagnostic and prognostic significance.
Article Details
How to Cite
MENGUE, Carolina da Silva et al.
Identifying Eye Changes in Children and Adolescents with Congenital Heart Disease with the Aid of a Smartphone: An Observational Study.
Medical Research Archives, [S.l.], v. 11, n. 7.2, july 2023.
ISSN 2375-1924.
Available at: <https://esmed.org/MRA/mra/article/view/4003>. Date accessed: 23 nov. 2024.
doi: https://doi.org/10.18103/mra.v11i7.2.4003.
Section
Research Articles
The Medical Research Archives grants authors the right to publish and reproduce the unrevised contribution in whole or in part at any time and in any form for any scholarly non-commercial purpose with the condition that all publications of the contribution include a full citation to the journal as published by the Medical Research Archives.
References
1. Mansour AM, Bitar FF, Traboulsi EI, Kassak KM, Obeid MY, Megarbane A, et al. Ocular pathology in congenital heart disease. Eye. 2005;19(1):29–34.
2. Vilela MAP, Sbruzzi G, Pellanda LC. Prevalence of ophthalmological abnormalities in children and adolescents with CHD: Systematic review and meta-analysis of observational studies. Vol. 26, Cardiology in the Young. 2016.
3. Li C, Zhong P, Yuan H, Dong X, Peng Q, Huang M, et al. Retinal microvasculature impairment in patients with congenital heart disease investigated by optical coherence tomography angiography. Clin Exp Ophthalmol. 2020;48(9).
4. Vilela MAP, Amaral CEV, Ferreira MAT. Retinal vascular tortuosity: Mechanisms and measurements. Eur J Ophthalmol. 2021;31(3):1497–506.
5. Tai ELM, Kueh YC, Hitam WHW, Wong TY, Shatriah I. Comparison of retinal vascular geometry in obese and non-obese children. PLoS One. 2018;13(2).
6. Malek J, Azar AT, Tourki R. Impact of retinal vascular tortuosity on retinal circulation. Neural Comput Appl. 2015;26(1):25–40.
7. Le Gloan L, Chakor H, Mercier LA, Harasymowycz P, Dore A, Lachapelle P, et al. Aortic coarctation and the retinal microvasculature. Int J Cardiol [Internet]. 2014;174(1):25–30. Available from: http://dx.doi.org/10.1016/j.ijcard.2014.03.129
8. Vilela MAP, Colossi C, Freitas H, Valle G, Pellanda LC. Ocular alterations associated with primary congenital heart disease - A cross-sectional study. Middle East Afr J Ophthalmol. 2020;27(1).
9. Rajalakshmi R, Arulmalar S, Usha M, Prathiba V, Kareemuddin KS, Anjana RM, et al. Validation of smartphone based retinal photography for diabetic retinopathy screening. PLoS One. 2015 Sep 24;10(9).
10. Abràmoff MD, Magalhães PJ, Ram SJ. Image processing with imageJ. Biophotonics Int. 2004;11(7):36–41.
11. Gilboa SM, Salemi JL, Nembhard WN, Fixler DE, Correa A. Mortality Resulting From Congenital Heart Disease Among Children and Adults in the United States, 1999 to 2006. Circulation. 2010;122(22):22-54–2263.
12. Fettah N, Kabatas EU, Dogan V, Zenciroglu A, Dilli D, Ozyazici E, et al. Retinovascular findings in newborns with critical congenital heart disease: A case series. Arch Argent Pediatr. 2017;115(3):e175–8.
13. Kohner EM, Allen EM, Saunders KB, Emery VM, Pallis C. Electroencephalogram and Retinal Vessels in Congenital Cyanotic Heart Disease Before and After Surgery. Br Med J. 1967;4(5573):207–10.
14. Gardiner PA, Joseph M. Eye Defects in Children with Congenital Heart Lesions: A Preliminary Study. Dev Med Child Neurol. 1968;10(1):42–8.
15. Johns KJ, Johns JA, Feman SS. Retinal Vascular Abnormalities in Patients with Coarctation of the Aorta. Arch Ophthalmol. 1991;109(9):1266–8.
16. Eisalo A, Raitta C, Kala R, Halonen PI. Fluorescence angiography of the fundus vessels in aortic coarctation. Br Heart J. 1970;32(1):71–5.
17. Maccormick IJC, Somner J, Morris DS, Macgillivray TJ, Bourne RRA, Huang SS, et al. Retinal Vessel Tortuosity in Response to Hypobaric Hypoxia. Higt Alt Med Biol. 2012;13(4):263–8.
18. Wagener HP, Clay GE, Gipner JF. Classification of retinal lesions in the presence of vascular hypertension. Trans Am Ophthalmol Soc. 1947;45:57–73.
19. Taarnhøj NCBB, Munch IC, Sander B, Kessel L, Hougaard JL, Kyvik K, et al. Straight versus tortuous retinal arteries in relation to blood pressure and genetics. Br J Ophthalmol. 2008;92(8):1055–60.
20. Cordina R, Leaney J, Golzan M, Grieve S, Celermajer DS, Graham SL. Ophthalmological consequences of cyanotic congenital heart disease: Vascular parameters and nerve fibre layer. Clin Exp Ophthalmol. 2015;43(2):115–23.
21. De Aguiar Remigio MC, Brandt CT, Santos CCL, Arantes TE, De Aguiar MIR. Macular and peripapillary retinal nerve fibre layer thickness in patients with cyanotic congenital heart disease. Eye [Internet]. 2015;29(4):465–8. Available from: http://dx.doi.org/10.1038/eye.2014.330
22. Patrick S. McQuillena, Donna A. Goffb and DJL. Effects of congenital heart disease on brain development Patrick. Prog Pediatr Cardiol [Internet]. 2010;29(2):79–85. Available from: https://www.ncbi.nlm.nih.gov/pmc/articles/PMC3624763/pdf/nihms412728.pdf
23. Gariano RF, Gardner TW. Retinal angiogenesis in development and disease. Nature. 2005;438(7070):960–6.
24. Sun Y, Smith LEH. Retinal Vasculature in Development and Diseases. Annu Rev Vis Sci. 2018;4(1):101–22.
25. Selvam S, Kumar T, Fruttiger M. Retinal vasculature development in health and disease. Prog Retin Eye Res [Internet]. 2017;63:1–19. Available from: https://doi.org/10.1016/j.preteyeres.2017.11.001
26. Yasuda S, Kachi S, Kondo M, Ueno S, Kaneko H. Significant Correlation between Retinal Venous Tortuosity and Aqueous Vascular Endothelial Growth Factor Concentration in Eyes with Central Retinal Vein Occlusion. PLoS One. 2015;10(7):1–11.
27. Gerhardt H, Golding M, Fruttiger M, Ruhrberg C, Lundkvist A, Abramsson A, et al. Article VEGF guides angiogenic sprouting utilizing endothelial tip cell filopodia. J Cell Biol. 2003;161(6):1163–78.
28. Zeng G, Taylor SM, Mccolm JR, Kappas NC, Kearney JB, Williams LH, et al. Plenary paper Orientation of endothelial cell division is regulated by VEGF signaling during blood vessel formation. Blood. 2007;109(4):1345–53.
29. Wieder MS, Blace N, Szlechter MM, Shulman E, Thankenchen J, Mbekeani JN. Central retinal artery occlusion associated with patent foramen ovale: a case report and literature review. Arq Bras Oftalmol. 2021;84(5):494–8.
30. Tsui I, Shamsa K, Perloff JK, Lee E, Wirthlin RS, Schwartz SD. Retinal vascular patterns in adults with cyanotic congenital heart disease. Semin Ophthalmol. 2009;24(6):262–5.
31. Goel N, Kumar V, Seth A, Ghosh B. Proliferative retinopathy in a child with congenital cyanotic heart disease. J AAPOS [Internet]. 2010;14(5):455–6. Available from: http://dx.doi.org/10.1016/j.jaapos.2010.08.005
32. HO I-V, Spaide R. Central Retinal Artery Occlusion Associated With A Patent Foramen Ovale. Retina. 2005;27(2):259–60.
33. Cheung CYL, Zheng Y, Hsu W, Lee ML, Lau QP, Mitchell P, et al. Retinal vascular tortuosity, blood pressure, and cardiovascular risk factors. Ophthalmology [Internet]. 2011;118(5):812–8. Available from: http://dx.doi.org/10.1016/j.ophtha.2010.08.045
34. Dascalu J, Liu M, Lycett K, Grobler AC, He M, Burgner DP, et al. Retinal microvasculature: Population epidemiology and concordance in Australian children aged 11-12 years and their parents. Vol. 9, BMJ Open. 2019.
35. Boillot A, Zoungas S, Mitchell P, Klein R, Klein B, Ikram MK, et al. Obesity and the Microvasculature: A Systematic Review and Meta-Analysis. PLoS One. 2013;8(2).
36. Ding J, Wai KL, McGeechan K, Ikram MK, Kawasaki R, Xie J, et al. Review: Retinal vascular caliber and the development of hypertension: A meta-analysis of individual participant data. J Hypertens. 2014;32(2):207–15.
37. McGeechan K, Liew G, MacAskill P, Irwig L, Klein R, Klein BEK, et al. Prediction of incident stroke events based on retinal vessel caliber: A systematic review and individual-participant meta-analysis. Am J Epidemiol. 2009;170(11):1323–32.
38. MBoistat KM, Liew G, Macashill P, Irwig L, Klein R, K. KBE, et al. Retinal Vessel Caliber and Risk for Coronary Heart Disease: A Systematic Review and Meta-Analysis. Ann Intern Med. 2007;151(June 2009):404–13.
39. Gishti O, Jaddoe VWV, Duijts L, Steegers E, Reiss I, Hofman A, et al. Impact of birth parameters and early life growth patterns on retinalmicrovascular structure in children: The Generation RStudy. J Hypertens. 2015;33(7):1429–37.
40. Li LJ, Liao J, Fan Q, Cheung YCL, Kamran Ikram M, Cheng CY, et al. Familial correlation of retinal vascular caliber in Singapore Chinese. Investig Ophthalmol Vis Sci. 2013;54(8):5638–42.
41. David S. Friedman, Michael X. Repka, Joanne Katz, Lydia Giordano, Josephine Ibironke, Patricia Hawse and JMT. Prevalence of Amblyopia and Strabismus in White and African- American Children Aged 6 through 71 Months: The Baltimore Pediatric Eye Disease Study. Ophthalmology. 2009;116(11):1128-34.el – 2.
42. Repka MX, Lum F, Burugapalli B. Strabismus, Strabismus Surgery, and Reoperation Rate in the United States: Analysis from the IRIS Registry. Ophthalmology [Internet]. 2018;125(10):1646–53. Available from: https://doi.org/10.1016/j.ophtha.2018.04.024
43. Won Yeol Ryu SRL. Incidence of strabismus and amblyopia among children initially diagnosed with pseudostrabismus using the Optum® dataset. Physiol Behav. 2020;211:98–104.
44. Hart WE, Goldbaum M, Côté B, Kube P, Nelson MR. Measurement and classification of retinal vascular tortuosity. Int J Med Inform. 1999;53(2–3):239–52.
45. Soares JVB, Leandro JJG, Cesar RM, Jelinek HF, Cree MJ. Retinal vessel segmentation using the 2-D Gabor wavelet and supervised classification. IEEE Trans Med Imaging. 2006;25(9):1214–22.
46. Wenstedt EFE, Beugelink L, Schrooten EM, Rademaker E, Rorije NMG, Wouda RD, et al. High-salt intake affects retinal vascular tortuosity in healthy males: an exploratory randomized cross-over trial. Sci Rep [Internet]. 2021;11(1):1–9. Available from: https://doi.org/10.1038/s41598-020-79753-6
47. Lotmar W, Freiburghaus A, Bracher D. Measurement of vessel tortuosity on fundus photographs. Albr von Graefes Arch für Klin und Exp Ophthalmol. 1979;211(1):49–57.
48. Capowski JJ, Kylstra JA, Freedman SF. A numeric index based on spatial frequency for the tortuosity of retinal vessels and its application to plus disease in retinopathy of prematurity. Retina. 1995;15(6):490–500.
49. Roque WL, Costa RRA. A plugin for computing the pore/grain network tortuosity of a porous medium from 2D/3D MicroCT image. Appl Comput Geosci [Internet]. 2020;5(January):100019. Available from: https://doi.org/10.1016/j.acags.2020.100019
50. Imran A, Li J, Pei Y, Yang JJ, Wang Q. Comparative Analysis of Vessel Segmentation Techniques in Retinal Images. IEEE Access. 2019;7:114862–87.
51. Shahbaz R, Salducci M. Law and order of modern ophthalmology: Teleophthalmology, smartphones legal and ethics. Eur J Ophthalmol. 2021;31(1):13–21.
52. Sharafeldin N, Kawaguchi A, Sundaram A, Campbell S, Rudnisky C, Weis E, et al. Review of economic evaluations of teleophthalmology as a screening strategy for chronic eye disease in adults. Br J Ophthalmol. 2018;102(11):1485–91.
53. Hong SC. 3D printable retinal imaging adapter for smartphones could go global. Graefe’s Arch Clin Exp Ophthalmol. 2015;253(10):1831–3.
54. Kohler J, Tran TM, Sun S, Montezuma SR. Teaching smartphone funduscopy with 20 diopter lens in undergraduate medical education. Clin Ophthalmol. 2021;15:2013–23.
55. Wintergerst MWM, Jansen LG, Holz FG, Finger RP. Smartphone-based fundus imaging - Where are we now? Asia-Pacific J Ophthalmol. 2020;9(4):308–14.
56. Omari A, Samad M, Bakhsh SR, Tajran J, Williams GA. Accuracy of Remote Diagnosis of Acute Posterior Segment Pathology by Residents and Attendings Captured with a Smartphone and Standard 20/28D Lens. Clin Ophthalmol. 2022;16(June):2751–7.
57. Kim Y. Comparison of smartphone ophthalmoscopy vs conventional direct ophthalmoscopy as a teaching tool for medical students : the COSMOS study. 2019;13:391–401.
58. Vilela MAP, Valença FM, Barreto PKM, Amaral CEV, Pellanda LC. Agreement between retinal images obtained via smartphones and images obtained with retinal cameras or fundoscopic exams – Systematic review and meta-analysis. Clin Ophthalmol. 2018;12:2581–9.
59. Murtaza K. Adam, Christopher J. Brady, Alexis M. Flowers, Alexander T. Juhn, Jason Hsu, Sunir J. Garg et al. Quality and Diagnostic Utility of Mydriatic Smartphone Photography: The Smartphone Ophthalmoscopy Reliability Trial. Ophthalmic Surg Lasers Imaging Retin. 2015;46:631–7.
60. Jones S, Edwards RT. Diabetic retinopathy screening: A systematic review of the economic evidence. Diabet Med. 2010;27(3):249–56.
61. Law MX, Pimentel MF, Oldenburg CE, de Alba Campomanes AG. Positive predictive value and screening performance of GoCheck Kids in a primary care university clinic. J AAPOS [Internet]. 2020;24(1):17.e1-17.e5. Available from: https://doi.org/10.1016/j.jaapos.2019.11.006
62. Ting DSW, Pasquale LR, Peng L, Campbell JP, Lee AY, Raman R, et al. Artificial intelligence and deep learning in ophthalmology. Br J Ophthalmol. 2019;103(2):167–75.
63. Wintergerst MWM, Petrak M, Li JQ, Larsen PP, Berger M, Holz FG, et al. Non-contact smartphone-based fundus imaging compared to conventional fundus imaging: a low-cost alternative for retinopathy of prematurity screening and documentation. Sci Rep. 2019;9(1):1–8.
64. Chalam K V., Brar VS, Keshavamurthy R. Evaluation of modified portable digital camera for screening of diabetic retinopathy. Ophthalmic Res. 2009;42(1):60–2.
65. Fleming AD, Philip S, Goatman KA, Olson JA, Sharp PF. Automated assessment of diabetic retinal image quality based on clarity and field definition. Investig Ophthalmol Vis Sci. 2006;47(3):1120–5.
66. Tran K, Mendel TA, Holbrook KL, Yates PA. Construction of an inexpensive, hand-held fundus camera through modification of a consumer “point-and-shoot” camera. Investig Ophthalmol Vis Sci. 2012;53(12):7600–7.
67. Bifolck E, Fink A, Pedersen D, Gregory T. Smartphone imaging for the ophthalmic examination in primary care. J Am Acad Physician Assist. 2018;31(8):34–8.
68. Pujari A, Saluja G, Agarwal D, Sinha A, P R A, Kumar A, et al. Clinical Role of Smartphone Fundus Imaging in Diabetic Retinopathy and Other Neuro-retinal Diseases. Curr Eye Res [Internet]. 2021;46(11):1605–13. Available from: https://doi.org/10.1080/02713683.2021.1958347
2. Vilela MAP, Sbruzzi G, Pellanda LC. Prevalence of ophthalmological abnormalities in children and adolescents with CHD: Systematic review and meta-analysis of observational studies. Vol. 26, Cardiology in the Young. 2016.
3. Li C, Zhong P, Yuan H, Dong X, Peng Q, Huang M, et al. Retinal microvasculature impairment in patients with congenital heart disease investigated by optical coherence tomography angiography. Clin Exp Ophthalmol. 2020;48(9).
4. Vilela MAP, Amaral CEV, Ferreira MAT. Retinal vascular tortuosity: Mechanisms and measurements. Eur J Ophthalmol. 2021;31(3):1497–506.
5. Tai ELM, Kueh YC, Hitam WHW, Wong TY, Shatriah I. Comparison of retinal vascular geometry in obese and non-obese children. PLoS One. 2018;13(2).
6. Malek J, Azar AT, Tourki R. Impact of retinal vascular tortuosity on retinal circulation. Neural Comput Appl. 2015;26(1):25–40.
7. Le Gloan L, Chakor H, Mercier LA, Harasymowycz P, Dore A, Lachapelle P, et al. Aortic coarctation and the retinal microvasculature. Int J Cardiol [Internet]. 2014;174(1):25–30. Available from: http://dx.doi.org/10.1016/j.ijcard.2014.03.129
8. Vilela MAP, Colossi C, Freitas H, Valle G, Pellanda LC. Ocular alterations associated with primary congenital heart disease - A cross-sectional study. Middle East Afr J Ophthalmol. 2020;27(1).
9. Rajalakshmi R, Arulmalar S, Usha M, Prathiba V, Kareemuddin KS, Anjana RM, et al. Validation of smartphone based retinal photography for diabetic retinopathy screening. PLoS One. 2015 Sep 24;10(9).
10. Abràmoff MD, Magalhães PJ, Ram SJ. Image processing with imageJ. Biophotonics Int. 2004;11(7):36–41.
11. Gilboa SM, Salemi JL, Nembhard WN, Fixler DE, Correa A. Mortality Resulting From Congenital Heart Disease Among Children and Adults in the United States, 1999 to 2006. Circulation. 2010;122(22):22-54–2263.
12. Fettah N, Kabatas EU, Dogan V, Zenciroglu A, Dilli D, Ozyazici E, et al. Retinovascular findings in newborns with critical congenital heart disease: A case series. Arch Argent Pediatr. 2017;115(3):e175–8.
13. Kohner EM, Allen EM, Saunders KB, Emery VM, Pallis C. Electroencephalogram and Retinal Vessels in Congenital Cyanotic Heart Disease Before and After Surgery. Br Med J. 1967;4(5573):207–10.
14. Gardiner PA, Joseph M. Eye Defects in Children with Congenital Heart Lesions: A Preliminary Study. Dev Med Child Neurol. 1968;10(1):42–8.
15. Johns KJ, Johns JA, Feman SS. Retinal Vascular Abnormalities in Patients with Coarctation of the Aorta. Arch Ophthalmol. 1991;109(9):1266–8.
16. Eisalo A, Raitta C, Kala R, Halonen PI. Fluorescence angiography of the fundus vessels in aortic coarctation. Br Heart J. 1970;32(1):71–5.
17. Maccormick IJC, Somner J, Morris DS, Macgillivray TJ, Bourne RRA, Huang SS, et al. Retinal Vessel Tortuosity in Response to Hypobaric Hypoxia. Higt Alt Med Biol. 2012;13(4):263–8.
18. Wagener HP, Clay GE, Gipner JF. Classification of retinal lesions in the presence of vascular hypertension. Trans Am Ophthalmol Soc. 1947;45:57–73.
19. Taarnhøj NCBB, Munch IC, Sander B, Kessel L, Hougaard JL, Kyvik K, et al. Straight versus tortuous retinal arteries in relation to blood pressure and genetics. Br J Ophthalmol. 2008;92(8):1055–60.
20. Cordina R, Leaney J, Golzan M, Grieve S, Celermajer DS, Graham SL. Ophthalmological consequences of cyanotic congenital heart disease: Vascular parameters and nerve fibre layer. Clin Exp Ophthalmol. 2015;43(2):115–23.
21. De Aguiar Remigio MC, Brandt CT, Santos CCL, Arantes TE, De Aguiar MIR. Macular and peripapillary retinal nerve fibre layer thickness in patients with cyanotic congenital heart disease. Eye [Internet]. 2015;29(4):465–8. Available from: http://dx.doi.org/10.1038/eye.2014.330
22. Patrick S. McQuillena, Donna A. Goffb and DJL. Effects of congenital heart disease on brain development Patrick. Prog Pediatr Cardiol [Internet]. 2010;29(2):79–85. Available from: https://www.ncbi.nlm.nih.gov/pmc/articles/PMC3624763/pdf/nihms412728.pdf
23. Gariano RF, Gardner TW. Retinal angiogenesis in development and disease. Nature. 2005;438(7070):960–6.
24. Sun Y, Smith LEH. Retinal Vasculature in Development and Diseases. Annu Rev Vis Sci. 2018;4(1):101–22.
25. Selvam S, Kumar T, Fruttiger M. Retinal vasculature development in health and disease. Prog Retin Eye Res [Internet]. 2017;63:1–19. Available from: https://doi.org/10.1016/j.preteyeres.2017.11.001
26. Yasuda S, Kachi S, Kondo M, Ueno S, Kaneko H. Significant Correlation between Retinal Venous Tortuosity and Aqueous Vascular Endothelial Growth Factor Concentration in Eyes with Central Retinal Vein Occlusion. PLoS One. 2015;10(7):1–11.
27. Gerhardt H, Golding M, Fruttiger M, Ruhrberg C, Lundkvist A, Abramsson A, et al. Article VEGF guides angiogenic sprouting utilizing endothelial tip cell filopodia. J Cell Biol. 2003;161(6):1163–78.
28. Zeng G, Taylor SM, Mccolm JR, Kappas NC, Kearney JB, Williams LH, et al. Plenary paper Orientation of endothelial cell division is regulated by VEGF signaling during blood vessel formation. Blood. 2007;109(4):1345–53.
29. Wieder MS, Blace N, Szlechter MM, Shulman E, Thankenchen J, Mbekeani JN. Central retinal artery occlusion associated with patent foramen ovale: a case report and literature review. Arq Bras Oftalmol. 2021;84(5):494–8.
30. Tsui I, Shamsa K, Perloff JK, Lee E, Wirthlin RS, Schwartz SD. Retinal vascular patterns in adults with cyanotic congenital heart disease. Semin Ophthalmol. 2009;24(6):262–5.
31. Goel N, Kumar V, Seth A, Ghosh B. Proliferative retinopathy in a child with congenital cyanotic heart disease. J AAPOS [Internet]. 2010;14(5):455–6. Available from: http://dx.doi.org/10.1016/j.jaapos.2010.08.005
32. HO I-V, Spaide R. Central Retinal Artery Occlusion Associated With A Patent Foramen Ovale. Retina. 2005;27(2):259–60.
33. Cheung CYL, Zheng Y, Hsu W, Lee ML, Lau QP, Mitchell P, et al. Retinal vascular tortuosity, blood pressure, and cardiovascular risk factors. Ophthalmology [Internet]. 2011;118(5):812–8. Available from: http://dx.doi.org/10.1016/j.ophtha.2010.08.045
34. Dascalu J, Liu M, Lycett K, Grobler AC, He M, Burgner DP, et al. Retinal microvasculature: Population epidemiology and concordance in Australian children aged 11-12 years and their parents. Vol. 9, BMJ Open. 2019.
35. Boillot A, Zoungas S, Mitchell P, Klein R, Klein B, Ikram MK, et al. Obesity and the Microvasculature: A Systematic Review and Meta-Analysis. PLoS One. 2013;8(2).
36. Ding J, Wai KL, McGeechan K, Ikram MK, Kawasaki R, Xie J, et al. Review: Retinal vascular caliber and the development of hypertension: A meta-analysis of individual participant data. J Hypertens. 2014;32(2):207–15.
37. McGeechan K, Liew G, MacAskill P, Irwig L, Klein R, Klein BEK, et al. Prediction of incident stroke events based on retinal vessel caliber: A systematic review and individual-participant meta-analysis. Am J Epidemiol. 2009;170(11):1323–32.
38. MBoistat KM, Liew G, Macashill P, Irwig L, Klein R, K. KBE, et al. Retinal Vessel Caliber and Risk for Coronary Heart Disease: A Systematic Review and Meta-Analysis. Ann Intern Med. 2007;151(June 2009):404–13.
39. Gishti O, Jaddoe VWV, Duijts L, Steegers E, Reiss I, Hofman A, et al. Impact of birth parameters and early life growth patterns on retinalmicrovascular structure in children: The Generation RStudy. J Hypertens. 2015;33(7):1429–37.
40. Li LJ, Liao J, Fan Q, Cheung YCL, Kamran Ikram M, Cheng CY, et al. Familial correlation of retinal vascular caliber in Singapore Chinese. Investig Ophthalmol Vis Sci. 2013;54(8):5638–42.
41. David S. Friedman, Michael X. Repka, Joanne Katz, Lydia Giordano, Josephine Ibironke, Patricia Hawse and JMT. Prevalence of Amblyopia and Strabismus in White and African- American Children Aged 6 through 71 Months: The Baltimore Pediatric Eye Disease Study. Ophthalmology. 2009;116(11):1128-34.el – 2.
42. Repka MX, Lum F, Burugapalli B. Strabismus, Strabismus Surgery, and Reoperation Rate in the United States: Analysis from the IRIS Registry. Ophthalmology [Internet]. 2018;125(10):1646–53. Available from: https://doi.org/10.1016/j.ophtha.2018.04.024
43. Won Yeol Ryu SRL. Incidence of strabismus and amblyopia among children initially diagnosed with pseudostrabismus using the Optum® dataset. Physiol Behav. 2020;211:98–104.
44. Hart WE, Goldbaum M, Côté B, Kube P, Nelson MR. Measurement and classification of retinal vascular tortuosity. Int J Med Inform. 1999;53(2–3):239–52.
45. Soares JVB, Leandro JJG, Cesar RM, Jelinek HF, Cree MJ. Retinal vessel segmentation using the 2-D Gabor wavelet and supervised classification. IEEE Trans Med Imaging. 2006;25(9):1214–22.
46. Wenstedt EFE, Beugelink L, Schrooten EM, Rademaker E, Rorije NMG, Wouda RD, et al. High-salt intake affects retinal vascular tortuosity in healthy males: an exploratory randomized cross-over trial. Sci Rep [Internet]. 2021;11(1):1–9. Available from: https://doi.org/10.1038/s41598-020-79753-6
47. Lotmar W, Freiburghaus A, Bracher D. Measurement of vessel tortuosity on fundus photographs. Albr von Graefes Arch für Klin und Exp Ophthalmol. 1979;211(1):49–57.
48. Capowski JJ, Kylstra JA, Freedman SF. A numeric index based on spatial frequency for the tortuosity of retinal vessels and its application to plus disease in retinopathy of prematurity. Retina. 1995;15(6):490–500.
49. Roque WL, Costa RRA. A plugin for computing the pore/grain network tortuosity of a porous medium from 2D/3D MicroCT image. Appl Comput Geosci [Internet]. 2020;5(January):100019. Available from: https://doi.org/10.1016/j.acags.2020.100019
50. Imran A, Li J, Pei Y, Yang JJ, Wang Q. Comparative Analysis of Vessel Segmentation Techniques in Retinal Images. IEEE Access. 2019;7:114862–87.
51. Shahbaz R, Salducci M. Law and order of modern ophthalmology: Teleophthalmology, smartphones legal and ethics. Eur J Ophthalmol. 2021;31(1):13–21.
52. Sharafeldin N, Kawaguchi A, Sundaram A, Campbell S, Rudnisky C, Weis E, et al. Review of economic evaluations of teleophthalmology as a screening strategy for chronic eye disease in adults. Br J Ophthalmol. 2018;102(11):1485–91.
53. Hong SC. 3D printable retinal imaging adapter for smartphones could go global. Graefe’s Arch Clin Exp Ophthalmol. 2015;253(10):1831–3.
54. Kohler J, Tran TM, Sun S, Montezuma SR. Teaching smartphone funduscopy with 20 diopter lens in undergraduate medical education. Clin Ophthalmol. 2021;15:2013–23.
55. Wintergerst MWM, Jansen LG, Holz FG, Finger RP. Smartphone-based fundus imaging - Where are we now? Asia-Pacific J Ophthalmol. 2020;9(4):308–14.
56. Omari A, Samad M, Bakhsh SR, Tajran J, Williams GA. Accuracy of Remote Diagnosis of Acute Posterior Segment Pathology by Residents and Attendings Captured with a Smartphone and Standard 20/28D Lens. Clin Ophthalmol. 2022;16(June):2751–7.
57. Kim Y. Comparison of smartphone ophthalmoscopy vs conventional direct ophthalmoscopy as a teaching tool for medical students : the COSMOS study. 2019;13:391–401.
58. Vilela MAP, Valença FM, Barreto PKM, Amaral CEV, Pellanda LC. Agreement between retinal images obtained via smartphones and images obtained with retinal cameras or fundoscopic exams – Systematic review and meta-analysis. Clin Ophthalmol. 2018;12:2581–9.
59. Murtaza K. Adam, Christopher J. Brady, Alexis M. Flowers, Alexander T. Juhn, Jason Hsu, Sunir J. Garg et al. Quality and Diagnostic Utility of Mydriatic Smartphone Photography: The Smartphone Ophthalmoscopy Reliability Trial. Ophthalmic Surg Lasers Imaging Retin. 2015;46:631–7.
60. Jones S, Edwards RT. Diabetic retinopathy screening: A systematic review of the economic evidence. Diabet Med. 2010;27(3):249–56.
61. Law MX, Pimentel MF, Oldenburg CE, de Alba Campomanes AG. Positive predictive value and screening performance of GoCheck Kids in a primary care university clinic. J AAPOS [Internet]. 2020;24(1):17.e1-17.e5. Available from: https://doi.org/10.1016/j.jaapos.2019.11.006
62. Ting DSW, Pasquale LR, Peng L, Campbell JP, Lee AY, Raman R, et al. Artificial intelligence and deep learning in ophthalmology. Br J Ophthalmol. 2019;103(2):167–75.
63. Wintergerst MWM, Petrak M, Li JQ, Larsen PP, Berger M, Holz FG, et al. Non-contact smartphone-based fundus imaging compared to conventional fundus imaging: a low-cost alternative for retinopathy of prematurity screening and documentation. Sci Rep. 2019;9(1):1–8.
64. Chalam K V., Brar VS, Keshavamurthy R. Evaluation of modified portable digital camera for screening of diabetic retinopathy. Ophthalmic Res. 2009;42(1):60–2.
65. Fleming AD, Philip S, Goatman KA, Olson JA, Sharp PF. Automated assessment of diabetic retinal image quality based on clarity and field definition. Investig Ophthalmol Vis Sci. 2006;47(3):1120–5.
66. Tran K, Mendel TA, Holbrook KL, Yates PA. Construction of an inexpensive, hand-held fundus camera through modification of a consumer “point-and-shoot” camera. Investig Ophthalmol Vis Sci. 2012;53(12):7600–7.
67. Bifolck E, Fink A, Pedersen D, Gregory T. Smartphone imaging for the ophthalmic examination in primary care. J Am Acad Physician Assist. 2018;31(8):34–8.
68. Pujari A, Saluja G, Agarwal D, Sinha A, P R A, Kumar A, et al. Clinical Role of Smartphone Fundus Imaging in Diabetic Retinopathy and Other Neuro-retinal Diseases. Curr Eye Res [Internet]. 2021;46(11):1605–13. Available from: https://doi.org/10.1080/02713683.2021.1958347