Eccentric Infrared Photorefraction: A Review of Evolution, Optical Design, Features and Applications

Abstract

Photorefraction is seven-decade old technology that allows objective and non-invasive estimation of the eye’s refractive error using retro-illuminated photographs of the pupil. A special variant of this technique—eccentric infrared photorefraction—has now become the technology of choice for the screening of uncorrected refractive errors and other amblyogenic factors in the pediatric population. Eccentric infrared photorefraction is also the preferred measurement tool for scientific investigations on the physiology and pathobiology of the near-triadic reflex (accommodation, convergence and pupil miosis). Broadly, this technique uses an extended near-infrared light source that is mounted eccentric to the camera aperture to illuminate the retina. The optically double-pass reflected light generates a retro-illuminated luminance profile across the pupil, the gradient of which may be used to estimate the eye’s refractive power using standard calibration techniques. The present review summarizes the origins of photorefraction and then delves into the optical principles of eccentric infrared photorefraction, its properties, calibration techniques and associated pitfalls. The review also discusses the present and future use-cases of this technology. Overall, this review provides the basics of photorefraction for early readers of this topic and offers some practical guidelines for the moderate to advanced users of this technique.

Keywords

amblyopia / defocus / pediatric eye screening / keratoconus / retro-illumination / uncorrected refractive errors

References

[1] Howland H.C. Photorefraction of eyes: History and future prospects. Optom. Vis. Sci. 2009, 86, 603-606. https://doi.org/10.1097/OPX.0b013e3181a523c9.

[2] Howland H.C.; Braddick O.; Atkinson J.; et al. Optics of photorefraction: Orthogonal and isotropic methods. J. Opt. Soc. Am. 1983, 73, 1701-1708. https://doi.org/10.1364/josa.73.001701.

[3] Kaakinen K. A simple method for screening of children with strabismus, anisometropia or ametropia by simultaneous photography of the corneal and the fundus reflexes. Acta Ophthalmol. 1979, 57, 161-171. https://doi.org/10.1111/j.1755-3768.1979.tb00481.x.

[4] Kaakinen K.; Tommila V. A clinical study on the detection of strabismus, anisometropia or ametropia of children by simultaneous photography of the corneal and the fundus reflexes. Acta Ophthalmol. 1979, 57, 600-611. https://doi.org/10.1111/j.1755-3768.1979.tb00507.x.

[5] Bobier W.R.; Braddick O.J. Eccentric photorefraction: Optical analysis and empirical measures. Am. J. Optom. Physiol. Opt. 1985, 62, 614-620.

[6] Norcia A.M.; Zadnik K.; Day S.H. Photorefraction with a catadioptric lens. Improvement on the method of Kaakinen. Acta Ophthalmol. 1986, 64, 379-385. https://doi.org/10.1111/j.1755-3768.1986.tb06939.x.

[7] Schaeffel F.; Wilhelm H.; Zrenner E. Inter-individual variability in the dynamics of natural accommodation in humans: Relation to age and refractive errors. J. Physiol. 1993, 461, 301-320.

[8] Kaur K.; Gurnani B. Slit-Lamp Biomicroscope; StatPearls Publishing LLC: St. Petersburg, FL, USA, 2024.

[9] Schaeffel F.; Farkas L.; Howland H.C. Infrared photoretinoscope. Appl. Opt. 1987, 26, 1505-1509. https://doi.org/10.1364/AO.26.001505.

[10] Bharadwaj S.R.; Sravani N.G.; Little J.A.; et al. Empirical variability in the calibration of slope-based eccentric photorefraction. J. Opt. Soc. Am. A Opt. Image Sci. Vis. 2013, 30, 923-931. https://doi.org/10.1364/JOSAA.30.000923.

[11] Campbell M.C.; Bobier W.R.; Roorda A. Effect of monochromatic aberrations on photorefractive patterns. J. Opt. Soc. Am. A Opt. Image Sci. Vis. 1995, 12, 1637-1646. https://doi.org/10.1364/josaa.12.001637.

[12] Roorda A.; Campbell M.C.; Bobier W.R. Slope-based eccentric photorefraction: Theoretical analysis of different light source configurations and effects of ocular aberrations. J. Opt. Soc. Am. A Opt. Image Sci. Vis. 1997, 14, 2547-2556. https://doi.org/10.1364/josaa.14.002547.

[13] Wu Y.; Thibos L.N.; Candy T.R. Two-dimensional simulation of eccentric photorefraction images for ametropes: Factors influencing the measurement. Ophthalmic Physiol. Opt. 2018, 38, 432-446. https://doi.org/10.1111/opo.12563.

[14] Ferreira A.; Vieira R.; Maia S.; et al. Photoscreening for amblyopia risk factors assessment in young children: A systematic review with meta-analysis. Eur. J. Ophthalmol. 2023, 33, 92-103. https://doi.org/10.1177/11206721221099777.

[15] Horwood A.M.; Griffiths H.J.; Carlton J.; et al. Scope and costs of autorefraction and photoscreening for childhood amblyopia-a systematic narrative review in relation to the EUSCREEN project data. Eye 2021, 35, 739-752. https://doi.org/10.1038/s41433-020-01261-8.

[16] Silverstein E.; Donahue S.P. Preschool Vision Screening: Where We Have Been and Where We Are Going. Am. J. Ophthalmol. 2018, 194, xviii-xxiii. https://doi.org/10.1016/j.ajo.2018.07.022.

[17] Bharadwaj S.R.; Wang J.; Candy T.R. Pupil responses to near visual demand during human visual development. J. Vis. 2011, 11, 6. https://doi.org/10.1167/11.4.6.

[18] Horwood A.M.; Riddell P.M. Developmental changes in the balance of disparity, blur, and looming/proximity cues to drive ocular alignment and focus. Perception 2013, 42, 693-715. https://doi.org/10.1068/p7506.

[19] Kasthurirangan S.; Glasser A. Age related changes in accommodative dynamics in humans. Vision. Res. 2006, 46, 1507-1519. https://doi.org/10.1016/j.visres.2005.11.012.

[20] Toor S.; Horwood A.; Riddell P. The effect of asymmetrical accommodation on anisometropic amblyopia treatment outcomes. J. AAPOS 2019, 23, 203.e1-203.e5. https://doi.org/10.1016/j.jaapos.2019.05.010.

[21] Barathi V.A.; Beuerman R.W.; Schaeffel F. Effects of unilateral topical atropine on binocular pupil responses and eye growth in mice. Vision. Res. 2009, 49, 383-387. https://doi.org/10.1016/j.visres.2008.11.005.

[22] Bossong H.; Swann M.; Glasser A.; et al. Applicability of infrared photorefraction for measurement of accommodation in awake-behaving normal and strabismic monkeys. Investig. Ophthalmol. Vis. Sci. 2009, 50, 966-973. https://doi.org/10.1167/iovs.08-2686.

[23] Feldkaemper M.P.; Schaeffel F. Evidence for a potential role of glucagon during eye growth regulation in chicks. Vis. Neurosci. 2002, 19, 755-766. https://doi.org/10.1017/s0952523802196064.

[24] Katzir G.; Howland H.C. Corneal power and underwater accommodation in great cormorants (Phalacrocorax carbo sinensis). J. Exp. Biol. 2003, 206, 833-841. https://doi.org/10.1242/jeb.00142.

[25] Machovsky-Capuska G.E.; Howland H.C.; Raubenheimer D.; et al. Visual accommodation and active pursuit of prey underwater in a plunge-diving bird:The Australasian gannet. Proc. Biol. Sci. 2012, 279, 4118-4125. https://doi.org/10.1098/rspb.2012.1519.

[26] Troilo D.; Howland H.C.; Judge S.J. Visual optics and retinal cone topography in the common marmoset (Callithrix jacchus). Vision. Res. 1993, 33, 1301-1310. https://doi.org/10.1016/0042-6989(93)90038-x.

[27] Vilupuru A.S.; Kasthurirangan S.; Glasser A. Dynamics of accommodative fatigue in rhesus monkeys and humans. Vision. Res. 2005, 45, 181-191. https://doi.org/10.1016/j.visres.2004.07.036.

[28] Duret A.; Humphries R.; Ramanujam S.; et al. The infrared reflex: A potential new method for congenital cataract screening. Eye 2019, 33, 1865-1870. https://doi.org/10.1038/s41433-019-0509-9.

[29] Chen Y.L.; Tan B.; Baker K.; et al. Simulation of keratoconus observation in photorefraction. Opt. Express 2006, 14, 11477-11485. https://doi.org/10.1364/oe.14.011477.

[30] Patel A.M.; Kumar P.; Vaddavalli P.K.; et al. The Value of Eccentric Infrared Photorefraction in Evaluating Keratoconus. Optom. Vis. Sci. 2022, 99, 763-773. https://doi.org/10.1097/OPX.0000000000001940.

[31] Thibos L.N.; Hong X.; Bradley A.; et al. Statistical variation of aberration structure and image quality in a normal population of healthy eyes. J. Opt. Soc. Am. A Opt. Image Sci. Vis. 2002, 19, 2329-2348.

[32] Chen Y.C.; Jiang C.J.; Yang T.H.; et al. Development of a human eye model incorporated with intraocular scattering for visual performance assessment. J. Biomed. Opt. 2012, 17, 075009. https://doi.org/10.1117/1.JBO.17.7.075009.

[33] Howland H.C. Optics of photoretinoscopy: Results from ray tracing. Am. J. Optom. Physiol. Opt. 1985, 62, 621-625.

[34] Howland H.C.; Sayles N. Photokeratometric and photorefractive measurements of astigmatism in infants and young children. Vision. Res. 1985, 25, 73-81. https://doi.org/10.1016/0042-6989(85)90082-3.

[35] Sravani N.G.; Nilagiri V.K.; Bharadwaj S.R. Photorefraction estimates of refractive power varies with the ethnic origin of human eyes. Sci. Rep. 2015, 5, 7976. https://doi.org/10.1038/srep07976.

[36] Bharadwaj S.R.; Candy T.R. Cues for the control of ocular accommodation and vergence during postnatal human development. J. Vis. 2008, 8, 14. https://doi.org/10.1167/8.16.14.

[37] Ntodie M.; Bharadwaj S.R.; Balaji S.; et al. Comparison of Three Gaze-position Calibration Techniques in First Purkinje Image-based Eye Trackers. Optom. Vis. Sci. 2019, 96, 587-598. https://doi.org/10.1097/OPX.0000000000001405.

[38] Schaeffel F. Kappa and Hirschberg ratio measured with an automated video gaze tracker. Optom. Vis. Sci. 2002, 79, 329-334. https://doi.org/10.1097/00006324-200205000-00013.

[39] Choi M.; Weiss S.; Schaeffel F.; et al. Laboratory, clinical, and kindergarten test of a new eccentric infrared photorefractor (PowerRefractor). Optom. Vis. Sci. 2000, 77, 537-548. https://doi.org/10.1097/00006324-200010000-00008.

[40] Schaeffel F.; Mathis U.; Bruggemann G. Noncycloplegic photorefractive screening in pre-school children with the “PowerRefractor” in a pediatric practice. Optom. Vis. Sci. 2007, 84, 630-639. https://doi.org/10.1097/OPX.0b013e3180dc99ea.

[41] Gabriel G.M.; Mutti D.O. Evaluation of infant accommodation using retinoscopy and photoretinoscopy. Optom. Vis. Sci. 2009, 86, 208-215. https://doi.org/10.1097/OPX.0b013e3181960652.

[42] Gehring A.M.; Haensel J.X.; Curtiss M.K.; et al. Validation of the PowerRef 3 for Measuring Accommodation: Comparison With the Grand Seiko WAM-5500A Autorefractor. Transl. Vis. Sci. Technol. 2022, 11, 25. https://doi.org/10.1167/tvst.11.10.25.

[43] Seidemann A.; Schaeffel F. An evaluation of the lag of accommodation using photorefraction. Vision. Res. 2003, 43, 419-430. https://doi.org/10.1016/s0042-6989(02)00571-0.

[44] Bharadwaj S.R.; Candy T.R. Accommodative and vergence responses to conflicting blur and disparity stimuli during development. J. Vis. 2009, 9, 4. https://doi.org/10.1167/9.11.4.

[45] Blade P.J.; Candy T.R. Validation of the PowerRefractor for measuring human infant refraction. Optom. Vis. Sci. 2006, 83, 346-353. https://doi.org/10.1097/01.opx.0000221402.35099.fb.

[46] Ghahghaei S.; Reed O.; Candy T.R.; et al. Calibration of the PlusOptix PowerRef 3 with change in viewing distance, adult age and refractive error. Ophthalmic Physiol. Opt. 2019, 39, 253-259. https://doi.org/10.1111/opo.12631.

[47] Horwood A.M.; Riddell P.M. Can misalignments in typical infants be used as a model for infantile esotropia? Investig. Ophthalmol. Vis. Sci. 2004, 45, 714-720. https://doi.org/10.1167/iovs.03-0454.

[48] Gekeler F.; Schaeffel F.; Howland H.C.; et al. Measurement of astigmatism by automated infrared photoretinoscopy. Optom. Vis. Sci. 1997, 74, 472-482. https://doi.org/10.1097/00006324-199707000-00013.

[49] Bharadwaj S.R.; Schor C.M. Acceleration characteristics of human ocular accommodation. Vision. Res. 2005, 45, 17-28. https://doi.org/10.1016/j.visres.2004.07.040.

[50] Tondel G.M.; Candy T.R. Accommodation and vergence latencies in human infants. Vision. Res. 2008, 48, 564-576. https://doi.org/10.1016/j.visres.2007.11.016.

[51] Marran L.; Schor C.M. Lens induced aniso-accommodation. Vision. Res. 1998, 38, 3601-3619. https://doi.org/10.1016/s0042-6989(98)00064-9.

[52] Sravani N.G.; Bharadwaj S.R. Ocular Focusing Behavior of the One-Eyed Child. Optom. Vis. Sci. 2017, 94, 150-158. https://doi.org/10.1097/OPX.0000000000001009.

[53] Pophal C.J.; Trivedi R.H.; Bowsher J.D.; et al. Effectiveness of the Spot (tm) Vision Screener With Variations in Ocular Pigments. Am. J. Ophthalmol. 2024, 264, 99-103. https://doi.org/10.1016/j.ajo.2024.03.018.

[54] Tabernero J.; Ohlendorf A.; Fischer M.D.; et al. Peripheral refraction profiles in subjects with low foveal refractive errors. Optom. Vis. Sci. 2011, 88, E388-E394. https://doi.org/10.1097/OPX.0b013e31820bb0f5.

[55] Tabernero J.; Schaeffel F. Fast scanning photoretinoscope for measuring peripheral refraction as a function of accommodation. J. Opt. Soc. Am. A Opt. Image Sci. Vis. 2009, 26, 2206-2210. https://doi.org/10.1364/JOSAA.26.002206.

[56] Marshall J.; Gole G.A. Unilateral leukocoria in off axis flash photographs of normal eyes. Am. J. Ophthalmol. 2003, 135, 709-711. https://doi.org/10.1016/s0002-9394(02)02079-2.

[57] Asensio-Sanchez V.M.; Diaz-Cabanas L.; Martin-Prieto A. Photoleukocoria with smartphone photographs. Int. Med. Case Rep. J. 2018, 11, 117-119. https://doi.org/10.2147/IMCRJ.S163735.

[58] Nilagiri V.K.; Metlapally S.; Schor C.M.; et al. A computational analysis of retinal image quality in eyes with keratoconus. Sci. Rep. 2020, 10, 1321. https://doi.org/10.1038/s41598-020-57993-w.

[59] Pantanelli S.; MacRae S.; Jeong T.M.; et al. Characterizing the wave aberration in eyes with keratoconus or penetrating keratoplasty using a high-dynamic range wavefront sensor. Ophthalmology 2007, 114, 2013-2021. https://doi.org/10.1016/j.ophtha.2007.01.008.

[60] Sarkar S.; Devi P.; Vaddavalli P.K.; et al. Differences in Image Quality after Three Laser Keratorefractive Procedures for Myopia. Optom. Vis. Sci. 2022, 99, 137-149. https://doi.org/10.1097/OPX.0000000000001850.

[61] Sarkar S.; Vaddavalli P.K.; Bharadwaj S.R. Image Quality Analysis of Eyes Undergoing LASER Refractive Surgery. PLoS ONE 2016, 11, e0148085. https://doi.org/10.1371/journal.pone.0148085.

[62] Devkar K.; Arunkumar S.; Bhakta T.; et al. Explainable XceptionNet-Based Keratoconus Detection Using Infrared Images and Edge Computing. IEEE Sens. Lett. 2024, 9, 6000404, https://doi.org/10.1109/LSENS.2024.3509503.

[63] Rabbetts R.B. Subsidiary effects of correcting lenses; magnifying devices. In Bennett & Rabbetts’ Clinical Visual Optics, 4th ed.; Rabbetts, R.B., Ed.; Butterworth Heinemann: Edinburgh, UK, 2007; pp. 245-274.

[64] Bharadwaj S.R.; Bandela P.K.; Nilagiri V.K. Lens magnification affects the estimates of refractive error obtained using eccentric infrared photorefraction. J. Opt. Soc. Am. A Opt. Image Sci. Vis. 2018, 35, 908-915. https://doi.org/10.1364/JOSAA.35.000908.

[65] Anderson H.A.; Manny R.E.; Glasser A.; et al. Static and dynamic measurements of accommodation in individuals with down syndrome. Investig. Ophthalmol. Vis. Sci. 2011, 52, 310-317.

[66] Doyle L.; Saunders K.J.; Little J.A. Trying to see, failing to focus: Near visual impairment in Down syndrome. Sci. Rep. 2016, 6, 20444.

[67] Roorda A.; Bobier W.R.; Campbell M.C. An infrared eccentric photo-optometer. Vision. Res. 1998, 38, 1913-1924. https://doi.org/10.1016/s0042-6989(97)00424-0.

[68] Chun J.; Kim Y.; Shin K.Y.; et al. Deep Learning-Based Prediction of Refractive Error Using Photorefraction Images Captured by a Smartphone: Model Development and Validation Study. JMIR Med. Inform. 2020, 8, e16225. https://doi.org/10.2196/16225.

[69] Kwok T.C.K.; Shum N.C.M.; Ngai G.; et al. Democratizing Optometric Care: A Vision-Based, Data-Driven Approach to Automatic Refractive Error Measurement for Vision Screening. In Proceedings of the IEEE International Symposium on Multimedia (ISM), Miami, FL, USA, 14-16 December 2015; pp. 7-12. https://doi.org/10.1109/ISM.2015.55.

[70] Yang Z.; Fu E.Y.; Ngai G.; et al. Screening for refractive error with low-quality smartphone images. In Proceedings of the Proceedings of the 18th International Conference on Advances in Mobile Computing & Multimedia, Chiang Mai Thailand, 30 November-2 December 2020. https://doi.org/10.1145/3428690.3429175.

[71] Linde G.; Chalakkal R.; Zhou L.; et al. Automatic Refractive Error Estimation Using Deep Learning-Based Analysis of Red Reflex Images. Diagnostics 2023, 13, 2810. https://doi.org/10.3390/diagnostics13172810.

[72] Xu D.; Ding S.; Zheng T.; et al. Deep learning for predicting refractive error from multiple photorefraction images. Biomed. Eng. Online 2022, 21, 55. https://doi.org/10.1186/s12938-022-01025-3.

[73] Bharadwaj S.R.; Ravisankar C.; Roy S.; et al. Fluctuations of Steady-State Accommodation Is a Marker for Screening Spasm of Near Reflex. Transl. Vis. Sci. Technol. 2021, 10, 9. https://doi.org/10.1167/tvst.10.11.9.

[74] Bharadwaj S.R.; Roy S.; Satgunam P. Spasm of Near Reflex: Objective Assessment of the Near-Triad. Investig. Ophthalmol. Vis. Sci. 2020, 61, 18. https://doi.org/10.1167/iovs.61.8.18.

[75] Santodomingo-Rubido J.; Carracedo G.; Suzaki A.; et al. Keratoconus: An updated review. Cont. Lens Anterior Eye 2022, 45, 101559. https://doi.org/10.1016/j.clae.2021.101559.