Abstract

This study investigates the influence of photopigment bleaching on autofluorescence lifetimes in the fundus in 21 young healthy volunteers. Three measurements of 30° retinal fields in two spectral channels (SSC: 498–560 nm, LSC: 560–720 nm) were obtained for each volunteer using fluorescence lifetime imaging ophthalmoscopy (FLIO). After dark-adaptation by wearing a custom-made lightproof mask for 30 minutes, the first FLIO-measurement was recorded (dark-adapted state). Subsequently, the eye was bleached for 1 minute (luminance: 3200 cd/m2), followed by a second FLIO-measurement (bleached state). Following an additional 10 minute dark adaptation using the mask, a final FLIO-measurement was recorded (recovered state). Average values of the fluorescence lifetimes were calculated from within different areas of a standardized early treatment diabetic retinopathy study (ETDRS) grid (central area, inner and outer rings). The acquisition time in the bleached state was significantly shortened by approximately 20%. The SSC did not show any significant changes in fluorescence lifetimes with photopigment bleaching, only the LSC showed small but significant bleaching-related changes in the fluorescence lifetimes τ1 and τ2 from all regions, as well as the mean fluorescence lifetime in the central area. The fluorescence lifetime differences caused by bleaching were by far less significant than pathological changes caused by eye diseases. The magnitudes of fluorescence lifetime changes are <10% and do not interfere with healthy or disease related FLIO patterns. Thus, we conclude that bleaching is not a relevant confounder in current clinical applications of FLIO.

© 2019 Optical Society of America under the terms of the OSA Open Access Publishing Agreement

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References

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2018 (8)

L. Sauer, K. M. Andersen, C. Dysli, M. S. Zinkernagel, P. S. Bernstein, and M. Hammer, “Review of clinical approaches in fluorescence lifetime imaging ophthalmoscopy,” J. Biomed. Opt. 23(9), 1–20 (2018).
[Crossref] [PubMed]

L. Sauer, R. H. Gensure, K. M. Andersen, L. Kreilkamp, G. S. Hageman, M. Hammer, and P. S. Bernstein, “Patterns of Fundus Autofluorescence Lifetimes In Eyes of Individuals With Nonexudative Age-Related Macular Degeneration,” Invest. Ophthalmol. Vis. Sci. 59(4), AMD65–AMD77 (2018).
[Crossref] [PubMed]

L. Sauer, R. H. Gensure, M. Hammer, and P. S. Bernstein, “Fluorescence Lifetime Imaging Ophthalmoscopy: A Novel Way to Assess Macular Telangiectasia Type 2,” Ophthalmol. Retina 2(6), 587–598 (2018).
[Crossref] [PubMed]

L. Sauer, K. M. Andersen, B. Li, R. H. Gensure, M. Hammer, and P. S. Bernstein, “Fluorescence Lifetime Imaging Ophthalmoscopy (FLIO) of Macular Pigment,” Invest. Ophthalmol. Vis. Sci. 59(7), 3094–3103 (2018).
[Crossref] [PubMed]

K. M. Andersen, L. Sauer, R. H. Gensure, M. Hammer, and P. S. Bernstein, “Characterization of Retinitis Pigmentosa Using Fluorescence Lifetime Imaging Ophthalmoscopy (FLIO),” Transl. Vis. Sci. Technol. 7(3), 20 (2018).
[Crossref] [PubMed]

C. Dysli, K. Schürch, E. Pascal, S. Wolf, and M. S. Zinkernagel, “Fundus Autofluorescence Lifetime Patterns in Retinitis Pigmentosa,” Invest. Ophthalmol. Vis. Sci. 59(5), 1769–1778 (2018).
[Crossref] [PubMed]

H. J. Kim and J. R. Sparrow, “Novel bisretinoids of human retina are lyso alkyl ether glycerophosphoethanolamine-bearing A2PE species,” J. Lipid Res. 59(9), 1620–1629 (2018).
[Crossref] [PubMed]

M. Hammer, L. Sauer, M. Klemm, S. Peters, R. Schultz, and J. Haueisen, “Fundus autofluorescence beyond lipofuscin: lesson learned from ex vivo fluorescence lifetime imaging in porcine eyes,” Biomed. Opt. Express 9(7), 3078–3091 (2018).
[Crossref] [PubMed]

2017 (3)

C. Dysli, R. Fink, S. Wolf, and M. S. Zinkernagel, “Fluorescence Lifetimes of Drusen in Age-Related Macular Degeneration,” Invest. Ophthalmol. Vis. Sci. 58(11), 4856–4862 (2017).
[Crossref] [PubMed]

J. Schmidt, S. Peters, L. Sauer, D. Schweitzer, M. Klemm, R. Augsten, N. Müller, and M. Hammer, “Fundus autofluorescence lifetimes are increased in non-proliferative diabetic retinopathy,” Acta Ophthalmol. 95(1), 33–40 (2017).
[Crossref] [PubMed]

C. Dysli, S. Wolf, M. Y. Berezin, L. Sauer, M. Hammer, and M. S. Zinkernagel, “Fluorescence lifetime imaging ophthalmoscopy,” Prog. Retin. Eye Res. 60, 120–143 (2017).
[Crossref] [PubMed]

2016 (3)

T. Ben Ami, Y. Tong, A. Bhuiyan, C. Huisingh, Z. Ablonczy, T. Ach, C. A. Curcio, and R. T. Smith, “Spatial and Spectral Characterization of Human Retinal Pigment Epithelium Fluorophore Families by Ex Vivo Hyperspectral Autofluorescence Imaging,” Transl. Vis. Sci. Technol. 5(3), 5 (2016).
[Crossref] [PubMed]

C. Dysli, S. Wolf, and M. S. Zinkernagel, “Autofluorescence Lifetimes in Geographic Atrophy in Patients With Age-Related Macular Degeneration,” Invest. Ophthalmol. Vis. Sci. 57(6), 2479–2487 (2016).
[Crossref] [PubMed]

C. Dysli, S. Wolf, K. Hatz, and M. S. Zinkernagel, “Fluorescence Lifetime Imaging in Stargardt Disease: Potential Marker for Disease Progression,” Invest. Ophthalmol. Vis. Sci. 57(3), 832–841 (2016).
[Crossref] [PubMed]

2015 (5)

C. Dysli, S. Wolf, and M. S. Zinkernagel, “Fluorescence lifetime imaging in retinal artery occlusion,” Invest. Ophthalmol. Vis. Sci. 56(5), 3329–3336 (2015).
[Crossref] [PubMed]

Z. Liu, K. Ueda, H. J. Kim, and J. R. Sparrow, “Photobleaching and Fluorescence Recovery of RPE Bisretinoids,” PLoS One 10(9), e0138081 (2015).
[Crossref] [PubMed]

D. Schweitzer, L. Deutsch, M. Klemm, S. Jentsch, M. Hammer, S. Peters, J. Haueisen, U. A. Müller, and J. Dawczynski, “Fluorescence lifetime imaging ophthalmoscopy in type 2 diabetic patients who have no signs of diabetic retinopathy,” J. Biomed. Opt. 20(6), 61106 (2015).
[Crossref] [PubMed]

L. Sauer, D. Schweitzer, L. Ramm, R. Augsten, M. Hammer, and S. Peters, “Impact of Macular Pigment on Fundus Autofluorescence Lifetimes,” Invest. Ophthalmol. Vis. Sci. 56(8), 4668–4679 (2015).
[Crossref] [PubMed]

M. Klemm, D. Schweitzer, S. Peters, L. Sauer, M. Hammer, and J. Haueisen, “FLIMX: A Software Package to Determine and Analyze the Fluorescence Lifetime in Time-Resolved Fluorescence Data from the Human Eye,” PLoS One 10(7), e0131640 (2015).
[Crossref] [PubMed]

2014 (1)

C. Dysli, G. Quellec, M. Abegg, M. N. Menke, U. Wolf-Schnurrbusch, J. Kowal, J. Blatz, O. La Schiazza, A. B. Leichtle, S. Wolf, and M. S. Zinkernagel, “Quantitative analysis of fluorescence lifetime measurements of the macula using the fluorescence lifetime imaging ophthalmoscope in healthy subjects,” Invest. Ophthalmol. Vis. Sci. 55(4), 2106–2113 (2014).
[Crossref] [PubMed]

2013 (2)

M. Klemm, A. Dietzel, J. Haueisen, E. Nagel, M. Hammer, and D. Schweitzer, “Repeatability of autofluorescence lifetime imaging at the human fundus in healthy volunteers,” Curr. Eye Res. 38(7), 793–801 (2013).
[Crossref] [PubMed]

Y. Miura, G. Huettmann, R. Orzekowsky-Schroeder, P. Steven, M. Szaszák, N. Koop, and R. Brinkmann, “Two-photon microscopy and fluorescence lifetime imaging of retinal pigment epithelial cells under oxidative stress,” Invest. Ophthalmol. Vis. Sci. 54(5), 3366–3377 (2013).
[Crossref] [PubMed]

2012 (4)

K. Yamamoto, J. Zhou, J. J. Hunter, D. R. Williams, and J. R. Sparrow, “Toward an understanding of bisretinoid autofluorescence bleaching and recovery,” Invest. Ophthalmol. Vis. Sci. 53(7), 3536–3544 (2012).
[Crossref] [PubMed]

D. Schweitzer, E. R. Gaillard, J. Dillon, R. F. Mullins, S. Russell, B. Hoffmann, S. Peters, M. Hammer, and C. Biskup, “Time-resolved autofluorescence imaging of human donor retina tissue from donors with significant extramacular drusen,” Invest. Ophthalmol. Vis. Sci. 53(7), 3376–3386 (2012).
[Crossref] [PubMed]

J. R. Sparrow, E. Gregory-Roberts, K. Yamamoto, A. Blonska, S. K. Ghosh, K. Ueda, and J. Zhou, “The bisretinoids of retinal pigment epithelium,” Prog. Retin. Eye Res. 31(2), 121–135 (2012).
[Crossref] [PubMed]

W. Becker, “Fluorescence lifetime imaging--techniques and applications,” J. Microsc. 247(2), 119–136 (2012).
[Crossref] [PubMed]

2011 (1)

F. Delori, J. P. Greenberg, R. L. Woods, J. Fischer, T. Duncker, J. Sparrow, and R. T. Smith, “Quantitative measurements of autofluorescence with the scanning laser ophthalmoscope,” Invest. Ophthalmol. Vis. Sci. 52(13), 9379–9390 (2011).
[Crossref] [PubMed]

2010 (4)

D. Moher, S. Hopewell, K. F. Schulz, V. Montori, P. C. Gøtzsche, P. J. Devereaux, D. Elbourne, M. Egger, and D. G. Altman, “CONSORT 2010 explanation and elaboration: updated guidelines for reporting parallel group randomised trials,” BMJ 340(mar23 1), c869 (2010).
[Crossref] [PubMed]

J. R. Sparrow, Y. Wu, T. Nagasaki, K. D. Yoon, K. Yamamoto, and J. Zhou, “Fundus autofluorescence and the bisretinoids of retina,” Photochem. Photobiol. Sci. 9(11), 1480–1489 (2010).
[Crossref] [PubMed]

J. R. Sparrow, Y. Wu, C. Y. Kim, and J. Zhou, “Phospholipid meets all-trans-retinal: the making of RPE bisretinoids,” J. Lipid Res. 51(2), 247–261 (2010).
[Crossref] [PubMed]

D. Schweitzer, S. Quick, M. Klemm, M. Hammer, S. Jentsch, and J. Dawczynski, “[Time-resolved autofluorescence in retinal vascular occlusions],” Ophthalmologe 107(12), 1145–1152 (2010).
[Crossref] [PubMed]

2009 (1)

M. Y. Loguinova, V. E. Zagidullin, T. B. Feldman, Y. V. Rostovtseva, V. Z. Paschenko, A. B. Rubin, and A. A. Ostrovsky, “Spectral Characteristics of Fluorophores Formed via Interaction between All-trans-Retinal with Rhodopsin and Lipids in Photoreceptor Membrane of Retina Rod Outer Segments,” Биол. мембраны 26, 83–93 (2009).

2008 (2)

S. Schmitz-Valckenberg, F. G. Holz, A. C. Bird, and R. F. Spaide, “Fundus autofluorescence imaging: review and perspectives,” Retina 28(3), 385–409 (2008).
[PubMed]

T. Theelen, T. T. J. M. Berendschot, C. J. F. Boon, C. B. Hoyng, and B. J. Klevering, “Analysis of visual pigment by fundus autofluorescence,” Exp. Eye Res. 86(2), 296–304 (2008).
[Crossref] [PubMed]

2007 (1)

D. Schweitzer, S. Schenke, M. Hammer, F. Schweitzer, S. Jentsch, E. Birckner, W. Becker, and A. Bergmann, “Towards metabolic mapping of the human retina,” Microsc. Res. Tech. 70(5), 410–419 (2007).
[Crossref] [PubMed]

2006 (3)

M. Hammer, S. Richter, K. H. Guehrs, and D. Schweitzer, “Retinal pigment epithelium cell damage by A2-E and its photo-derivatives,” Mol. Vis. 12, 1348–1354 (2006).
[PubMed]

S. R. Kim, K. Nakanishi, Y. Itagaki, and J. R. Sparrow, “Photooxidation of A2-PE, a photoreceptor outer segment fluorophore, and protection by lutein and zeaxanthin,” Exp. Eye Res. 82(5), 828–839 (2006).
[Crossref] [PubMed]

M. Sharifzadeh, P. S. Bernstein, and W. Gellermann, “Nonmydriatic fluorescence-based quantitative imaging of human macular pigment distributions,” J. Opt. Soc. Am. A 23(10), 2373–2387 (2006).
[Crossref] [PubMed]

2004 (2)

D. Schweitzer, M. Hammer, F. Schweitzer, R. Anders, T. Doebbecke, S. Schenke, E. R. Gaillard, and E. R. Gaillard, “In vivo measurement of time-resolved autofluorescence at the human fundus,” J. Biomed. Opt. 9(6), 1214–1222 (2004).
[Crossref] [PubMed]

O. A. R. Mahroo and T. D. Lamb, “Recovery of the human photopic electroretinogram after bleaching exposures: estimation of pigment regeneration kinetics,” J. Physiol. 554(Pt 2), 417–437 (2004).
[Crossref] [PubMed]

2003 (1)

A. J. Wenzel, K. Fuld, and J. M. Stringham, “Light exposure and macular pigment optical density,” Invest. Ophthalmol. Vis. Sci. 44(1), 306–309 (2003).
[Crossref] [PubMed]

2000 (2)

J. R. Sparrow, K. Nakanishi, and C. A. Parish, “The lipofuscin fluorophore A2E mediates blue light-induced damage to retinal pigmented epithelial cells,” Invest. Ophthalmol. Vis. Sci. 41(7), 1981–1989 (2000).
[PubMed]

A. A. V. Paupoo, O. A. R. Mahroo, C. Friedburg, and T. D. Lamb, “Human cone photoreceptor responses measured by the electoretinogram a-wave during and after exposure to intense illumination,” J. Physiol. 529(2), 469–482 (2000).
[Crossref] [PubMed]

1996 (1)

N. Sakai, J. Decatur, K. Nakanishi, and G. E. Eldred, “Ocular age pigment “A2-E”: An unprecedented pyridinium bisretinoid,” J. Am. Chem. Soc. 118(6), 1559–1560 (1996).
[Crossref]

1995 (2)

L. Song, E. J. Hennink, I. T. Young, and H. J. Tanke, “Photobleaching kinetics of fluorescein in quantitative fluorescence microscopy,” Biophys. J. 68(6), 2588–2600 (1995).
[Crossref] [PubMed]

F. C. Delori, C. K. Dorey, G. Staurenghi, O. Arend, D. G. Goger, and J. J. Weiter, “In vivo fluorescence of the ocular fundus exhibits retinal pigment epithelium lipofuscin characteristics,” Invest. Ophthalmol. Vis. Sci. 36(3), 718–729 (1995).
[PubMed]

1992 (1)

D. C. Coile and H. D. Baker, “Foveal dark adaptation, photopigment regeneration, and aging,” Vis. Neurosci. 8(1), 27–39 (1992).
[Crossref] [PubMed]

1991 (1)

Early Treatment Diabetic Retinopathy Study Research Group, “Grading diabetic retinopathy from stereoscopic color fundus photographs--an extension of the modified Airlie House classification. ETDRS report number 10,” Ophthalmology 98(5Suppl), 786–806 (1991).
[Crossref] [PubMed]

1981 (1)

R. Peters, A. Brünger, and K. Schulten, “Continuous fluorescence microphotolysis: A sensitive method for study of diffusion processes in single cells,” Proc. Natl. Acad. Sci. U.S.A. 78(2), 962–966 (1981).
[Crossref] [PubMed]

1973 (1)

M. Hollins and M. Alpern, “Dark adaptation and visual pigment regeneration in human cones,” J. Gen. Physiol. 62(4), 430–447 (1973).
[Crossref] [PubMed]

1968 (1)

W. A. H. Rushton and G. H. Henry, “Bleaching and regeneration of cone pigments in man,” Vision Res. 8(6), 617–631 (1968).
[Crossref] [PubMed]

1965 (2)

J. A. Nelder and R. Mead, “A Simplex-Method for Function Minimization,” Comput. J. 7(4), 308–313 (1965).
[Crossref]

S. S. Shapiro and M. B. Wilk, “An Analysis of Variance Test for Normality (Complete Samples),” Biometrika 52(3-4), 591–611 (1965).
[Crossref]

1933 (1)

W. S. Stiles and B. H. Crawford, “The Luminous Efficiency of Rays Entering the Eye Pupil at Different Points,” Proc. R. Soc. Lond., B 112(778), 428–450 (1933).
[Crossref]

1928 (1)

J. Neyman and E. S. Pearson, “On the Use and Interpretation of Certain Test Criteria for Purposes of Statistical Inference,” Biometrika 20A, 263–294 (1928).

Abegg, M.

C. Dysli, G. Quellec, M. Abegg, M. N. Menke, U. Wolf-Schnurrbusch, J. Kowal, J. Blatz, O. La Schiazza, A. B. Leichtle, S. Wolf, and M. S. Zinkernagel, “Quantitative analysis of fluorescence lifetime measurements of the macula using the fluorescence lifetime imaging ophthalmoscope in healthy subjects,” Invest. Ophthalmol. Vis. Sci. 55(4), 2106–2113 (2014).
[Crossref] [PubMed]

Ablonczy, Z.

T. Ben Ami, Y. Tong, A. Bhuiyan, C. Huisingh, Z. Ablonczy, T. Ach, C. A. Curcio, and R. T. Smith, “Spatial and Spectral Characterization of Human Retinal Pigment Epithelium Fluorophore Families by Ex Vivo Hyperspectral Autofluorescence Imaging,” Transl. Vis. Sci. Technol. 5(3), 5 (2016).
[Crossref] [PubMed]

Ach, T.

T. Ben Ami, Y. Tong, A. Bhuiyan, C. Huisingh, Z. Ablonczy, T. Ach, C. A. Curcio, and R. T. Smith, “Spatial and Spectral Characterization of Human Retinal Pigment Epithelium Fluorophore Families by Ex Vivo Hyperspectral Autofluorescence Imaging,” Transl. Vis. Sci. Technol. 5(3), 5 (2016).
[Crossref] [PubMed]

Alpern, M.

M. Hollins and M. Alpern, “Dark adaptation and visual pigment regeneration in human cones,” J. Gen. Physiol. 62(4), 430–447 (1973).
[Crossref] [PubMed]

Altman, D. G.

D. Moher, S. Hopewell, K. F. Schulz, V. Montori, P. C. Gøtzsche, P. J. Devereaux, D. Elbourne, M. Egger, and D. G. Altman, “CONSORT 2010 explanation and elaboration: updated guidelines for reporting parallel group randomised trials,” BMJ 340(mar23 1), c869 (2010).
[Crossref] [PubMed]

Anders, R.

D. Schweitzer, M. Hammer, F. Schweitzer, R. Anders, T. Doebbecke, S. Schenke, E. R. Gaillard, and E. R. Gaillard, “In vivo measurement of time-resolved autofluorescence at the human fundus,” J. Biomed. Opt. 9(6), 1214–1222 (2004).
[Crossref] [PubMed]

Andersen, K. M.

L. Sauer, K. M. Andersen, C. Dysli, M. S. Zinkernagel, P. S. Bernstein, and M. Hammer, “Review of clinical approaches in fluorescence lifetime imaging ophthalmoscopy,” J. Biomed. Opt. 23(9), 1–20 (2018).
[Crossref] [PubMed]

L. Sauer, K. M. Andersen, B. Li, R. H. Gensure, M. Hammer, and P. S. Bernstein, “Fluorescence Lifetime Imaging Ophthalmoscopy (FLIO) of Macular Pigment,” Invest. Ophthalmol. Vis. Sci. 59(7), 3094–3103 (2018).
[Crossref] [PubMed]

L. Sauer, R. H. Gensure, K. M. Andersen, L. Kreilkamp, G. S. Hageman, M. Hammer, and P. S. Bernstein, “Patterns of Fundus Autofluorescence Lifetimes In Eyes of Individuals With Nonexudative Age-Related Macular Degeneration,” Invest. Ophthalmol. Vis. Sci. 59(4), AMD65–AMD77 (2018).
[Crossref] [PubMed]

K. M. Andersen, L. Sauer, R. H. Gensure, M. Hammer, and P. S. Bernstein, “Characterization of Retinitis Pigmentosa Using Fluorescence Lifetime Imaging Ophthalmoscopy (FLIO),” Transl. Vis. Sci. Technol. 7(3), 20 (2018).
[Crossref] [PubMed]

Arend, O.

F. C. Delori, C. K. Dorey, G. Staurenghi, O. Arend, D. G. Goger, and J. J. Weiter, “In vivo fluorescence of the ocular fundus exhibits retinal pigment epithelium lipofuscin characteristics,” Invest. Ophthalmol. Vis. Sci. 36(3), 718–729 (1995).
[PubMed]

Augsten, R.

J. Schmidt, S. Peters, L. Sauer, D. Schweitzer, M. Klemm, R. Augsten, N. Müller, and M. Hammer, “Fundus autofluorescence lifetimes are increased in non-proliferative diabetic retinopathy,” Acta Ophthalmol. 95(1), 33–40 (2017).
[Crossref] [PubMed]

L. Sauer, D. Schweitzer, L. Ramm, R. Augsten, M. Hammer, and S. Peters, “Impact of Macular Pigment on Fundus Autofluorescence Lifetimes,” Invest. Ophthalmol. Vis. Sci. 56(8), 4668–4679 (2015).
[Crossref] [PubMed]

Baker, H. D.

D. C. Coile and H. D. Baker, “Foveal dark adaptation, photopigment regeneration, and aging,” Vis. Neurosci. 8(1), 27–39 (1992).
[Crossref] [PubMed]

Becker, W.

W. Becker, “Fluorescence lifetime imaging--techniques and applications,” J. Microsc. 247(2), 119–136 (2012).
[Crossref] [PubMed]

D. Schweitzer, S. Schenke, M. Hammer, F. Schweitzer, S. Jentsch, E. Birckner, W. Becker, and A. Bergmann, “Towards metabolic mapping of the human retina,” Microsc. Res. Tech. 70(5), 410–419 (2007).
[Crossref] [PubMed]

Ben Ami, T.

T. Ben Ami, Y. Tong, A. Bhuiyan, C. Huisingh, Z. Ablonczy, T. Ach, C. A. Curcio, and R. T. Smith, “Spatial and Spectral Characterization of Human Retinal Pigment Epithelium Fluorophore Families by Ex Vivo Hyperspectral Autofluorescence Imaging,” Transl. Vis. Sci. Technol. 5(3), 5 (2016).
[Crossref] [PubMed]

Berendschot, T. T. J. M.

T. Theelen, T. T. J. M. Berendschot, C. J. F. Boon, C. B. Hoyng, and B. J. Klevering, “Analysis of visual pigment by fundus autofluorescence,” Exp. Eye Res. 86(2), 296–304 (2008).
[Crossref] [PubMed]

Berezin, M. Y.

C. Dysli, S. Wolf, M. Y. Berezin, L. Sauer, M. Hammer, and M. S. Zinkernagel, “Fluorescence lifetime imaging ophthalmoscopy,” Prog. Retin. Eye Res. 60, 120–143 (2017).
[Crossref] [PubMed]

Bergmann, A.

D. Schweitzer, S. Schenke, M. Hammer, F. Schweitzer, S. Jentsch, E. Birckner, W. Becker, and A. Bergmann, “Towards metabolic mapping of the human retina,” Microsc. Res. Tech. 70(5), 410–419 (2007).
[Crossref] [PubMed]

Bernstein, P. S.

L. Sauer, K. M. Andersen, B. Li, R. H. Gensure, M. Hammer, and P. S. Bernstein, “Fluorescence Lifetime Imaging Ophthalmoscopy (FLIO) of Macular Pigment,” Invest. Ophthalmol. Vis. Sci. 59(7), 3094–3103 (2018).
[Crossref] [PubMed]

L. Sauer, K. M. Andersen, C. Dysli, M. S. Zinkernagel, P. S. Bernstein, and M. Hammer, “Review of clinical approaches in fluorescence lifetime imaging ophthalmoscopy,” J. Biomed. Opt. 23(9), 1–20 (2018).
[Crossref] [PubMed]

L. Sauer, R. H. Gensure, K. M. Andersen, L. Kreilkamp, G. S. Hageman, M. Hammer, and P. S. Bernstein, “Patterns of Fundus Autofluorescence Lifetimes In Eyes of Individuals With Nonexudative Age-Related Macular Degeneration,” Invest. Ophthalmol. Vis. Sci. 59(4), AMD65–AMD77 (2018).
[Crossref] [PubMed]

L. Sauer, R. H. Gensure, M. Hammer, and P. S. Bernstein, “Fluorescence Lifetime Imaging Ophthalmoscopy: A Novel Way to Assess Macular Telangiectasia Type 2,” Ophthalmol. Retina 2(6), 587–598 (2018).
[Crossref] [PubMed]

K. M. Andersen, L. Sauer, R. H. Gensure, M. Hammer, and P. S. Bernstein, “Characterization of Retinitis Pigmentosa Using Fluorescence Lifetime Imaging Ophthalmoscopy (FLIO),” Transl. Vis. Sci. Technol. 7(3), 20 (2018).
[Crossref] [PubMed]

M. Sharifzadeh, P. S. Bernstein, and W. Gellermann, “Nonmydriatic fluorescence-based quantitative imaging of human macular pigment distributions,” J. Opt. Soc. Am. A 23(10), 2373–2387 (2006).
[Crossref] [PubMed]

Bhuiyan, A.

T. Ben Ami, Y. Tong, A. Bhuiyan, C. Huisingh, Z. Ablonczy, T. Ach, C. A. Curcio, and R. T. Smith, “Spatial and Spectral Characterization of Human Retinal Pigment Epithelium Fluorophore Families by Ex Vivo Hyperspectral Autofluorescence Imaging,” Transl. Vis. Sci. Technol. 5(3), 5 (2016).
[Crossref] [PubMed]

Birckner, E.

D. Schweitzer, S. Schenke, M. Hammer, F. Schweitzer, S. Jentsch, E. Birckner, W. Becker, and A. Bergmann, “Towards metabolic mapping of the human retina,” Microsc. Res. Tech. 70(5), 410–419 (2007).
[Crossref] [PubMed]

Bird, A. C.

S. Schmitz-Valckenberg, F. G. Holz, A. C. Bird, and R. F. Spaide, “Fundus autofluorescence imaging: review and perspectives,” Retina 28(3), 385–409 (2008).
[PubMed]

Biskup, C.

D. Schweitzer, E. R. Gaillard, J. Dillon, R. F. Mullins, S. Russell, B. Hoffmann, S. Peters, M. Hammer, and C. Biskup, “Time-resolved autofluorescence imaging of human donor retina tissue from donors with significant extramacular drusen,” Invest. Ophthalmol. Vis. Sci. 53(7), 3376–3386 (2012).
[Crossref] [PubMed]

Blatz, J.

C. Dysli, G. Quellec, M. Abegg, M. N. Menke, U. Wolf-Schnurrbusch, J. Kowal, J. Blatz, O. La Schiazza, A. B. Leichtle, S. Wolf, and M. S. Zinkernagel, “Quantitative analysis of fluorescence lifetime measurements of the macula using the fluorescence lifetime imaging ophthalmoscope in healthy subjects,” Invest. Ophthalmol. Vis. Sci. 55(4), 2106–2113 (2014).
[Crossref] [PubMed]

Blonska, A.

J. R. Sparrow, E. Gregory-Roberts, K. Yamamoto, A. Blonska, S. K. Ghosh, K. Ueda, and J. Zhou, “The bisretinoids of retinal pigment epithelium,” Prog. Retin. Eye Res. 31(2), 121–135 (2012).
[Crossref] [PubMed]

Boon, C. J. F.

T. Theelen, T. T. J. M. Berendschot, C. J. F. Boon, C. B. Hoyng, and B. J. Klevering, “Analysis of visual pigment by fundus autofluorescence,” Exp. Eye Res. 86(2), 296–304 (2008).
[Crossref] [PubMed]

Brinkmann, R.

Y. Miura, G. Huettmann, R. Orzekowsky-Schroeder, P. Steven, M. Szaszák, N. Koop, and R. Brinkmann, “Two-photon microscopy and fluorescence lifetime imaging of retinal pigment epithelial cells under oxidative stress,” Invest. Ophthalmol. Vis. Sci. 54(5), 3366–3377 (2013).
[Crossref] [PubMed]

Brünger, A.

R. Peters, A. Brünger, and K. Schulten, “Continuous fluorescence microphotolysis: A sensitive method for study of diffusion processes in single cells,” Proc. Natl. Acad. Sci. U.S.A. 78(2), 962–966 (1981).
[Crossref] [PubMed]

Coile, D. C.

D. C. Coile and H. D. Baker, “Foveal dark adaptation, photopigment regeneration, and aging,” Vis. Neurosci. 8(1), 27–39 (1992).
[Crossref] [PubMed]

Crawford, B. H.

W. S. Stiles and B. H. Crawford, “The Luminous Efficiency of Rays Entering the Eye Pupil at Different Points,” Proc. R. Soc. Lond., B 112(778), 428–450 (1933).
[Crossref]

Curcio, C. A.

T. Ben Ami, Y. Tong, A. Bhuiyan, C. Huisingh, Z. Ablonczy, T. Ach, C. A. Curcio, and R. T. Smith, “Spatial and Spectral Characterization of Human Retinal Pigment Epithelium Fluorophore Families by Ex Vivo Hyperspectral Autofluorescence Imaging,” Transl. Vis. Sci. Technol. 5(3), 5 (2016).
[Crossref] [PubMed]

Dawczynski, J.

D. Schweitzer, L. Deutsch, M. Klemm, S. Jentsch, M. Hammer, S. Peters, J. Haueisen, U. A. Müller, and J. Dawczynski, “Fluorescence lifetime imaging ophthalmoscopy in type 2 diabetic patients who have no signs of diabetic retinopathy,” J. Biomed. Opt. 20(6), 61106 (2015).
[Crossref] [PubMed]

D. Schweitzer, S. Quick, M. Klemm, M. Hammer, S. Jentsch, and J. Dawczynski, “[Time-resolved autofluorescence in retinal vascular occlusions],” Ophthalmologe 107(12), 1145–1152 (2010).
[Crossref] [PubMed]

Decatur, J.

N. Sakai, J. Decatur, K. Nakanishi, and G. E. Eldred, “Ocular age pigment “A2-E”: An unprecedented pyridinium bisretinoid,” J. Am. Chem. Soc. 118(6), 1559–1560 (1996).
[Crossref]

Delori, F.

F. Delori, J. P. Greenberg, R. L. Woods, J. Fischer, T. Duncker, J. Sparrow, and R. T. Smith, “Quantitative measurements of autofluorescence with the scanning laser ophthalmoscope,” Invest. Ophthalmol. Vis. Sci. 52(13), 9379–9390 (2011).
[Crossref] [PubMed]

Delori, F. C.

F. C. Delori, C. K. Dorey, G. Staurenghi, O. Arend, D. G. Goger, and J. J. Weiter, “In vivo fluorescence of the ocular fundus exhibits retinal pigment epithelium lipofuscin characteristics,” Invest. Ophthalmol. Vis. Sci. 36(3), 718–729 (1995).
[PubMed]

Deutsch, L.

D. Schweitzer, L. Deutsch, M. Klemm, S. Jentsch, M. Hammer, S. Peters, J. Haueisen, U. A. Müller, and J. Dawczynski, “Fluorescence lifetime imaging ophthalmoscopy in type 2 diabetic patients who have no signs of diabetic retinopathy,” J. Biomed. Opt. 20(6), 61106 (2015).
[Crossref] [PubMed]

Devereaux, P. J.

D. Moher, S. Hopewell, K. F. Schulz, V. Montori, P. C. Gøtzsche, P. J. Devereaux, D. Elbourne, M. Egger, and D. G. Altman, “CONSORT 2010 explanation and elaboration: updated guidelines for reporting parallel group randomised trials,” BMJ 340(mar23 1), c869 (2010).
[Crossref] [PubMed]

Dietzel, A.

M. Klemm, A. Dietzel, J. Haueisen, E. Nagel, M. Hammer, and D. Schweitzer, “Repeatability of autofluorescence lifetime imaging at the human fundus in healthy volunteers,” Curr. Eye Res. 38(7), 793–801 (2013).
[Crossref] [PubMed]

Dillon, J.

D. Schweitzer, E. R. Gaillard, J. Dillon, R. F. Mullins, S. Russell, B. Hoffmann, S. Peters, M. Hammer, and C. Biskup, “Time-resolved autofluorescence imaging of human donor retina tissue from donors with significant extramacular drusen,” Invest. Ophthalmol. Vis. Sci. 53(7), 3376–3386 (2012).
[Crossref] [PubMed]

Doebbecke, T.

D. Schweitzer, M. Hammer, F. Schweitzer, R. Anders, T. Doebbecke, S. Schenke, E. R. Gaillard, and E. R. Gaillard, “In vivo measurement of time-resolved autofluorescence at the human fundus,” J. Biomed. Opt. 9(6), 1214–1222 (2004).
[Crossref] [PubMed]

Dorey, C. K.

F. C. Delori, C. K. Dorey, G. Staurenghi, O. Arend, D. G. Goger, and J. J. Weiter, “In vivo fluorescence of the ocular fundus exhibits retinal pigment epithelium lipofuscin characteristics,” Invest. Ophthalmol. Vis. Sci. 36(3), 718–729 (1995).
[PubMed]

Duncker, T.

F. Delori, J. P. Greenberg, R. L. Woods, J. Fischer, T. Duncker, J. Sparrow, and R. T. Smith, “Quantitative measurements of autofluorescence with the scanning laser ophthalmoscope,” Invest. Ophthalmol. Vis. Sci. 52(13), 9379–9390 (2011).
[Crossref] [PubMed]

Dysli, C.

C. Dysli, K. Schürch, E. Pascal, S. Wolf, and M. S. Zinkernagel, “Fundus Autofluorescence Lifetime Patterns in Retinitis Pigmentosa,” Invest. Ophthalmol. Vis. Sci. 59(5), 1769–1778 (2018).
[Crossref] [PubMed]

L. Sauer, K. M. Andersen, C. Dysli, M. S. Zinkernagel, P. S. Bernstein, and M. Hammer, “Review of clinical approaches in fluorescence lifetime imaging ophthalmoscopy,” J. Biomed. Opt. 23(9), 1–20 (2018).
[Crossref] [PubMed]

C. Dysli, R. Fink, S. Wolf, and M. S. Zinkernagel, “Fluorescence Lifetimes of Drusen in Age-Related Macular Degeneration,” Invest. Ophthalmol. Vis. Sci. 58(11), 4856–4862 (2017).
[Crossref] [PubMed]

C. Dysli, S. Wolf, M. Y. Berezin, L. Sauer, M. Hammer, and M. S. Zinkernagel, “Fluorescence lifetime imaging ophthalmoscopy,” Prog. Retin. Eye Res. 60, 120–143 (2017).
[Crossref] [PubMed]

C. Dysli, S. Wolf, and M. S. Zinkernagel, “Autofluorescence Lifetimes in Geographic Atrophy in Patients With Age-Related Macular Degeneration,” Invest. Ophthalmol. Vis. Sci. 57(6), 2479–2487 (2016).
[Crossref] [PubMed]

C. Dysli, S. Wolf, K. Hatz, and M. S. Zinkernagel, “Fluorescence Lifetime Imaging in Stargardt Disease: Potential Marker for Disease Progression,” Invest. Ophthalmol. Vis. Sci. 57(3), 832–841 (2016).
[Crossref] [PubMed]

C. Dysli, S. Wolf, and M. S. Zinkernagel, “Fluorescence lifetime imaging in retinal artery occlusion,” Invest. Ophthalmol. Vis. Sci. 56(5), 3329–3336 (2015).
[Crossref] [PubMed]

C. Dysli, G. Quellec, M. Abegg, M. N. Menke, U. Wolf-Schnurrbusch, J. Kowal, J. Blatz, O. La Schiazza, A. B. Leichtle, S. Wolf, and M. S. Zinkernagel, “Quantitative analysis of fluorescence lifetime measurements of the macula using the fluorescence lifetime imaging ophthalmoscope in healthy subjects,” Invest. Ophthalmol. Vis. Sci. 55(4), 2106–2113 (2014).
[Crossref] [PubMed]

Egger, M.

D. Moher, S. Hopewell, K. F. Schulz, V. Montori, P. C. Gøtzsche, P. J. Devereaux, D. Elbourne, M. Egger, and D. G. Altman, “CONSORT 2010 explanation and elaboration: updated guidelines for reporting parallel group randomised trials,” BMJ 340(mar23 1), c869 (2010).
[Crossref] [PubMed]

Elbourne, D.

D. Moher, S. Hopewell, K. F. Schulz, V. Montori, P. C. Gøtzsche, P. J. Devereaux, D. Elbourne, M. Egger, and D. G. Altman, “CONSORT 2010 explanation and elaboration: updated guidelines for reporting parallel group randomised trials,” BMJ 340(mar23 1), c869 (2010).
[Crossref] [PubMed]

Eldred, G. E.

N. Sakai, J. Decatur, K. Nakanishi, and G. E. Eldred, “Ocular age pigment “A2-E”: An unprecedented pyridinium bisretinoid,” J. Am. Chem. Soc. 118(6), 1559–1560 (1996).
[Crossref]

Feldman, T. B.

M. Y. Loguinova, V. E. Zagidullin, T. B. Feldman, Y. V. Rostovtseva, V. Z. Paschenko, A. B. Rubin, and A. A. Ostrovsky, “Spectral Characteristics of Fluorophores Formed via Interaction between All-trans-Retinal with Rhodopsin and Lipids in Photoreceptor Membrane of Retina Rod Outer Segments,” Биол. мембраны 26, 83–93 (2009).

Fink, R.

C. Dysli, R. Fink, S. Wolf, and M. S. Zinkernagel, “Fluorescence Lifetimes of Drusen in Age-Related Macular Degeneration,” Invest. Ophthalmol. Vis. Sci. 58(11), 4856–4862 (2017).
[Crossref] [PubMed]

Fischer, J.

F. Delori, J. P. Greenberg, R. L. Woods, J. Fischer, T. Duncker, J. Sparrow, and R. T. Smith, “Quantitative measurements of autofluorescence with the scanning laser ophthalmoscope,” Invest. Ophthalmol. Vis. Sci. 52(13), 9379–9390 (2011).
[Crossref] [PubMed]

Friedburg, C.

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D. Schweitzer, E. R. Gaillard, J. Dillon, R. F. Mullins, S. Russell, B. Hoffmann, S. Peters, M. Hammer, and C. Biskup, “Time-resolved autofluorescence imaging of human donor retina tissue from donors with significant extramacular drusen,” Invest. Ophthalmol. Vis. Sci. 53(7), 3376–3386 (2012).
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D. Schweitzer, M. Hammer, F. Schweitzer, R. Anders, T. Doebbecke, S. Schenke, E. R. Gaillard, and E. R. Gaillard, “In vivo measurement of time-resolved autofluorescence at the human fundus,” J. Biomed. Opt. 9(6), 1214–1222 (2004).
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D. Schweitzer, M. Hammer, F. Schweitzer, R. Anders, T. Doebbecke, S. Schenke, E. R. Gaillard, and E. R. Gaillard, “In vivo measurement of time-resolved autofluorescence at the human fundus,” J. Biomed. Opt. 9(6), 1214–1222 (2004).
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Gensure, R. H.

K. M. Andersen, L. Sauer, R. H. Gensure, M. Hammer, and P. S. Bernstein, “Characterization of Retinitis Pigmentosa Using Fluorescence Lifetime Imaging Ophthalmoscopy (FLIO),” Transl. Vis. Sci. Technol. 7(3), 20 (2018).
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L. Sauer, R. H. Gensure, M. Hammer, and P. S. Bernstein, “Fluorescence Lifetime Imaging Ophthalmoscopy: A Novel Way to Assess Macular Telangiectasia Type 2,” Ophthalmol. Retina 2(6), 587–598 (2018).
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L. Sauer, R. H. Gensure, K. M. Andersen, L. Kreilkamp, G. S. Hageman, M. Hammer, and P. S. Bernstein, “Patterns of Fundus Autofluorescence Lifetimes In Eyes of Individuals With Nonexudative Age-Related Macular Degeneration,” Invest. Ophthalmol. Vis. Sci. 59(4), AMD65–AMD77 (2018).
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L. Sauer, K. M. Andersen, B. Li, R. H. Gensure, M. Hammer, and P. S. Bernstein, “Fluorescence Lifetime Imaging Ophthalmoscopy (FLIO) of Macular Pigment,” Invest. Ophthalmol. Vis. Sci. 59(7), 3094–3103 (2018).
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L. Sauer, R. H. Gensure, K. M. Andersen, L. Kreilkamp, G. S. Hageman, M. Hammer, and P. S. Bernstein, “Patterns of Fundus Autofluorescence Lifetimes In Eyes of Individuals With Nonexudative Age-Related Macular Degeneration,” Invest. Ophthalmol. Vis. Sci. 59(4), AMD65–AMD77 (2018).
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L. Sauer, R. H. Gensure, K. M. Andersen, L. Kreilkamp, G. S. Hageman, M. Hammer, and P. S. Bernstein, “Patterns of Fundus Autofluorescence Lifetimes In Eyes of Individuals With Nonexudative Age-Related Macular Degeneration,” Invest. Ophthalmol. Vis. Sci. 59(4), AMD65–AMD77 (2018).
[Crossref] [PubMed]

L. Sauer, R. H. Gensure, M. Hammer, and P. S. Bernstein, “Fluorescence Lifetime Imaging Ophthalmoscopy: A Novel Way to Assess Macular Telangiectasia Type 2,” Ophthalmol. Retina 2(6), 587–598 (2018).
[Crossref] [PubMed]

K. M. Andersen, L. Sauer, R. H. Gensure, M. Hammer, and P. S. Bernstein, “Characterization of Retinitis Pigmentosa Using Fluorescence Lifetime Imaging Ophthalmoscopy (FLIO),” Transl. Vis. Sci. Technol. 7(3), 20 (2018).
[Crossref] [PubMed]

L. Sauer, K. M. Andersen, B. Li, R. H. Gensure, M. Hammer, and P. S. Bernstein, “Fluorescence Lifetime Imaging Ophthalmoscopy (FLIO) of Macular Pigment,” Invest. Ophthalmol. Vis. Sci. 59(7), 3094–3103 (2018).
[Crossref] [PubMed]

M. Hammer, L. Sauer, M. Klemm, S. Peters, R. Schultz, and J. Haueisen, “Fundus autofluorescence beyond lipofuscin: lesson learned from ex vivo fluorescence lifetime imaging in porcine eyes,” Biomed. Opt. Express 9(7), 3078–3091 (2018).
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L. Sauer, K. M. Andersen, C. Dysli, M. S. Zinkernagel, P. S. Bernstein, and M. Hammer, “Review of clinical approaches in fluorescence lifetime imaging ophthalmoscopy,” J. Biomed. Opt. 23(9), 1–20 (2018).
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J. Schmidt, S. Peters, L. Sauer, D. Schweitzer, M. Klemm, R. Augsten, N. Müller, and M. Hammer, “Fundus autofluorescence lifetimes are increased in non-proliferative diabetic retinopathy,” Acta Ophthalmol. 95(1), 33–40 (2017).
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C. Dysli, S. Wolf, M. Y. Berezin, L. Sauer, M. Hammer, and M. S. Zinkernagel, “Fluorescence lifetime imaging ophthalmoscopy,” Prog. Retin. Eye Res. 60, 120–143 (2017).
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D. Schweitzer, L. Deutsch, M. Klemm, S. Jentsch, M. Hammer, S. Peters, J. Haueisen, U. A. Müller, and J. Dawczynski, “Fluorescence lifetime imaging ophthalmoscopy in type 2 diabetic patients who have no signs of diabetic retinopathy,” J. Biomed. Opt. 20(6), 61106 (2015).
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M. Klemm, D. Schweitzer, S. Peters, L. Sauer, M. Hammer, and J. Haueisen, “FLIMX: A Software Package to Determine and Analyze the Fluorescence Lifetime in Time-Resolved Fluorescence Data from the Human Eye,” PLoS One 10(7), e0131640 (2015).
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M. Klemm, A. Dietzel, J. Haueisen, E. Nagel, M. Hammer, and D. Schweitzer, “Repeatability of autofluorescence lifetime imaging at the human fundus in healthy volunteers,” Curr. Eye Res. 38(7), 793–801 (2013).
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D. Schweitzer, E. R. Gaillard, J. Dillon, R. F. Mullins, S. Russell, B. Hoffmann, S. Peters, M. Hammer, and C. Biskup, “Time-resolved autofluorescence imaging of human donor retina tissue from donors with significant extramacular drusen,” Invest. Ophthalmol. Vis. Sci. 53(7), 3376–3386 (2012).
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D. Schweitzer, S. Quick, M. Klemm, M. Hammer, S. Jentsch, and J. Dawczynski, “[Time-resolved autofluorescence in retinal vascular occlusions],” Ophthalmologe 107(12), 1145–1152 (2010).
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D. Schweitzer, S. Schenke, M. Hammer, F. Schweitzer, S. Jentsch, E. Birckner, W. Becker, and A. Bergmann, “Towards metabolic mapping of the human retina,” Microsc. Res. Tech. 70(5), 410–419 (2007).
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M. Hammer, S. Richter, K. H. Guehrs, and D. Schweitzer, “Retinal pigment epithelium cell damage by A2-E and its photo-derivatives,” Mol. Vis. 12, 1348–1354 (2006).
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D. Schweitzer, M. Hammer, F. Schweitzer, R. Anders, T. Doebbecke, S. Schenke, E. R. Gaillard, and E. R. Gaillard, “In vivo measurement of time-resolved autofluorescence at the human fundus,” J. Biomed. Opt. 9(6), 1214–1222 (2004).
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M. Hammer, L. Sauer, M. Klemm, S. Peters, R. Schultz, and J. Haueisen, “Fundus autofluorescence beyond lipofuscin: lesson learned from ex vivo fluorescence lifetime imaging in porcine eyes,” Biomed. Opt. Express 9(7), 3078–3091 (2018).
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D. Schweitzer, L. Deutsch, M. Klemm, S. Jentsch, M. Hammer, S. Peters, J. Haueisen, U. A. Müller, and J. Dawczynski, “Fluorescence lifetime imaging ophthalmoscopy in type 2 diabetic patients who have no signs of diabetic retinopathy,” J. Biomed. Opt. 20(6), 61106 (2015).
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M. Klemm, D. Schweitzer, S. Peters, L. Sauer, M. Hammer, and J. Haueisen, “FLIMX: A Software Package to Determine and Analyze the Fluorescence Lifetime in Time-Resolved Fluorescence Data from the Human Eye,” PLoS One 10(7), e0131640 (2015).
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M. Klemm, A. Dietzel, J. Haueisen, E. Nagel, M. Hammer, and D. Schweitzer, “Repeatability of autofluorescence lifetime imaging at the human fundus in healthy volunteers,” Curr. Eye Res. 38(7), 793–801 (2013).
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D. Schweitzer, L. Deutsch, M. Klemm, S. Jentsch, M. Hammer, S. Peters, J. Haueisen, U. A. Müller, and J. Dawczynski, “Fluorescence lifetime imaging ophthalmoscopy in type 2 diabetic patients who have no signs of diabetic retinopathy,” J. Biomed. Opt. 20(6), 61106 (2015).
[Crossref] [PubMed]

D. Schweitzer, S. Quick, M. Klemm, M. Hammer, S. Jentsch, and J. Dawczynski, “[Time-resolved autofluorescence in retinal vascular occlusions],” Ophthalmologe 107(12), 1145–1152 (2010).
[Crossref] [PubMed]

D. Schweitzer, S. Schenke, M. Hammer, F. Schweitzer, S. Jentsch, E. Birckner, W. Becker, and A. Bergmann, “Towards metabolic mapping of the human retina,” Microsc. Res. Tech. 70(5), 410–419 (2007).
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H. J. Kim and J. R. Sparrow, “Novel bisretinoids of human retina are lyso alkyl ether glycerophosphoethanolamine-bearing A2PE species,” J. Lipid Res. 59(9), 1620–1629 (2018).
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S. R. Kim, K. Nakanishi, Y. Itagaki, and J. R. Sparrow, “Photooxidation of A2-PE, a photoreceptor outer segment fluorophore, and protection by lutein and zeaxanthin,” Exp. Eye Res. 82(5), 828–839 (2006).
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M. Hammer, L. Sauer, M. Klemm, S. Peters, R. Schultz, and J. Haueisen, “Fundus autofluorescence beyond lipofuscin: lesson learned from ex vivo fluorescence lifetime imaging in porcine eyes,” Biomed. Opt. Express 9(7), 3078–3091 (2018).
[Crossref] [PubMed]

J. Schmidt, S. Peters, L. Sauer, D. Schweitzer, M. Klemm, R. Augsten, N. Müller, and M. Hammer, “Fundus autofluorescence lifetimes are increased in non-proliferative diabetic retinopathy,” Acta Ophthalmol. 95(1), 33–40 (2017).
[Crossref] [PubMed]

D. Schweitzer, L. Deutsch, M. Klemm, S. Jentsch, M. Hammer, S. Peters, J. Haueisen, U. A. Müller, and J. Dawczynski, “Fluorescence lifetime imaging ophthalmoscopy in type 2 diabetic patients who have no signs of diabetic retinopathy,” J. Biomed. Opt. 20(6), 61106 (2015).
[Crossref] [PubMed]

M. Klemm, D. Schweitzer, S. Peters, L. Sauer, M. Hammer, and J. Haueisen, “FLIMX: A Software Package to Determine and Analyze the Fluorescence Lifetime in Time-Resolved Fluorescence Data from the Human Eye,” PLoS One 10(7), e0131640 (2015).
[Crossref] [PubMed]

M. Klemm, A. Dietzel, J. Haueisen, E. Nagel, M. Hammer, and D. Schweitzer, “Repeatability of autofluorescence lifetime imaging at the human fundus in healthy volunteers,” Curr. Eye Res. 38(7), 793–801 (2013).
[Crossref] [PubMed]

D. Schweitzer, S. Quick, M. Klemm, M. Hammer, S. Jentsch, and J. Dawczynski, “[Time-resolved autofluorescence in retinal vascular occlusions],” Ophthalmologe 107(12), 1145–1152 (2010).
[Crossref] [PubMed]

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T. Theelen, T. T. J. M. Berendschot, C. J. F. Boon, C. B. Hoyng, and B. J. Klevering, “Analysis of visual pigment by fundus autofluorescence,” Exp. Eye Res. 86(2), 296–304 (2008).
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Y. Miura, G. Huettmann, R. Orzekowsky-Schroeder, P. Steven, M. Szaszák, N. Koop, and R. Brinkmann, “Two-photon microscopy and fluorescence lifetime imaging of retinal pigment epithelial cells under oxidative stress,” Invest. Ophthalmol. Vis. Sci. 54(5), 3366–3377 (2013).
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L. Sauer, R. H. Gensure, K. M. Andersen, L. Kreilkamp, G. S. Hageman, M. Hammer, and P. S. Bernstein, “Patterns of Fundus Autofluorescence Lifetimes In Eyes of Individuals With Nonexudative Age-Related Macular Degeneration,” Invest. Ophthalmol. Vis. Sci. 59(4), AMD65–AMD77 (2018).
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C. Dysli, G. Quellec, M. Abegg, M. N. Menke, U. Wolf-Schnurrbusch, J. Kowal, J. Blatz, O. La Schiazza, A. B. Leichtle, S. Wolf, and M. S. Zinkernagel, “Quantitative analysis of fluorescence lifetime measurements of the macula using the fluorescence lifetime imaging ophthalmoscope in healthy subjects,” Invest. Ophthalmol. Vis. Sci. 55(4), 2106–2113 (2014).
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L. Sauer, K. M. Andersen, B. Li, R. H. Gensure, M. Hammer, and P. S. Bernstein, “Fluorescence Lifetime Imaging Ophthalmoscopy (FLIO) of Macular Pigment,” Invest. Ophthalmol. Vis. Sci. 59(7), 3094–3103 (2018).
[Crossref] [PubMed]

Liu, Z.

Z. Liu, K. Ueda, H. J. Kim, and J. R. Sparrow, “Photobleaching and Fluorescence Recovery of RPE Bisretinoids,” PLoS One 10(9), e0138081 (2015).
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O. A. R. Mahroo and T. D. Lamb, “Recovery of the human photopic electroretinogram after bleaching exposures: estimation of pigment regeneration kinetics,” J. Physiol. 554(Pt 2), 417–437 (2004).
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Y. Miura, G. Huettmann, R. Orzekowsky-Schroeder, P. Steven, M. Szaszák, N. Koop, and R. Brinkmann, “Two-photon microscopy and fluorescence lifetime imaging of retinal pigment epithelial cells under oxidative stress,” Invest. Ophthalmol. Vis. Sci. 54(5), 3366–3377 (2013).
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D. Moher, S. Hopewell, K. F. Schulz, V. Montori, P. C. Gøtzsche, P. J. Devereaux, D. Elbourne, M. Egger, and D. G. Altman, “CONSORT 2010 explanation and elaboration: updated guidelines for reporting parallel group randomised trials,” BMJ 340(mar23 1), c869 (2010).
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J. Schmidt, S. Peters, L. Sauer, D. Schweitzer, M. Klemm, R. Augsten, N. Müller, and M. Hammer, “Fundus autofluorescence lifetimes are increased in non-proliferative diabetic retinopathy,” Acta Ophthalmol. 95(1), 33–40 (2017).
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Müller, U. A.

D. Schweitzer, L. Deutsch, M. Klemm, S. Jentsch, M. Hammer, S. Peters, J. Haueisen, U. A. Müller, and J. Dawczynski, “Fluorescence lifetime imaging ophthalmoscopy in type 2 diabetic patients who have no signs of diabetic retinopathy,” J. Biomed. Opt. 20(6), 61106 (2015).
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D. Schweitzer, E. R. Gaillard, J. Dillon, R. F. Mullins, S. Russell, B. Hoffmann, S. Peters, M. Hammer, and C. Biskup, “Time-resolved autofluorescence imaging of human donor retina tissue from donors with significant extramacular drusen,” Invest. Ophthalmol. Vis. Sci. 53(7), 3376–3386 (2012).
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M. Klemm, A. Dietzel, J. Haueisen, E. Nagel, M. Hammer, and D. Schweitzer, “Repeatability of autofluorescence lifetime imaging at the human fundus in healthy volunteers,” Curr. Eye Res. 38(7), 793–801 (2013).
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J. Schmidt, S. Peters, L. Sauer, D. Schweitzer, M. Klemm, R. Augsten, N. Müller, and M. Hammer, “Fundus autofluorescence lifetimes are increased in non-proliferative diabetic retinopathy,” Acta Ophthalmol. 95(1), 33–40 (2017).
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M. Klemm, D. Schweitzer, S. Peters, L. Sauer, M. Hammer, and J. Haueisen, “FLIMX: A Software Package to Determine and Analyze the Fluorescence Lifetime in Time-Resolved Fluorescence Data from the Human Eye,” PLoS One 10(7), e0131640 (2015).
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L. Sauer, D. Schweitzer, L. Ramm, R. Augsten, M. Hammer, and S. Peters, “Impact of Macular Pigment on Fundus Autofluorescence Lifetimes,” Invest. Ophthalmol. Vis. Sci. 56(8), 4668–4679 (2015).
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D. Schweitzer, E. R. Gaillard, J. Dillon, R. F. Mullins, S. Russell, B. Hoffmann, S. Peters, M. Hammer, and C. Biskup, “Time-resolved autofluorescence imaging of human donor retina tissue from donors with significant extramacular drusen,” Invest. Ophthalmol. Vis. Sci. 53(7), 3376–3386 (2012).
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L. Sauer, D. Schweitzer, L. Ramm, R. Augsten, M. Hammer, and S. Peters, “Impact of Macular Pigment on Fundus Autofluorescence Lifetimes,” Invest. Ophthalmol. Vis. Sci. 56(8), 4668–4679 (2015).
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M. Hammer, L. Sauer, M. Klemm, S. Peters, R. Schultz, and J. Haueisen, “Fundus autofluorescence beyond lipofuscin: lesson learned from ex vivo fluorescence lifetime imaging in porcine eyes,” Biomed. Opt. Express 9(7), 3078–3091 (2018).
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L. Sauer, K. M. Andersen, C. Dysli, M. S. Zinkernagel, P. S. Bernstein, and M. Hammer, “Review of clinical approaches in fluorescence lifetime imaging ophthalmoscopy,” J. Biomed. Opt. 23(9), 1–20 (2018).
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L. Sauer, K. M. Andersen, B. Li, R. H. Gensure, M. Hammer, and P. S. Bernstein, “Fluorescence Lifetime Imaging Ophthalmoscopy (FLIO) of Macular Pigment,” Invest. Ophthalmol. Vis. Sci. 59(7), 3094–3103 (2018).
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K. M. Andersen, L. Sauer, R. H. Gensure, M. Hammer, and P. S. Bernstein, “Characterization of Retinitis Pigmentosa Using Fluorescence Lifetime Imaging Ophthalmoscopy (FLIO),” Transl. Vis. Sci. Technol. 7(3), 20 (2018).
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L. Sauer, R. H. Gensure, M. Hammer, and P. S. Bernstein, “Fluorescence Lifetime Imaging Ophthalmoscopy: A Novel Way to Assess Macular Telangiectasia Type 2,” Ophthalmol. Retina 2(6), 587–598 (2018).
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J. Schmidt, S. Peters, L. Sauer, D. Schweitzer, M. Klemm, R. Augsten, N. Müller, and M. Hammer, “Fundus autofluorescence lifetimes are increased in non-proliferative diabetic retinopathy,” Acta Ophthalmol. 95(1), 33–40 (2017).
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M. Klemm, D. Schweitzer, S. Peters, L. Sauer, M. Hammer, and J. Haueisen, “FLIMX: A Software Package to Determine and Analyze the Fluorescence Lifetime in Time-Resolved Fluorescence Data from the Human Eye,” PLoS One 10(7), e0131640 (2015).
[Crossref] [PubMed]

L. Sauer, D. Schweitzer, L. Ramm, R. Augsten, M. Hammer, and S. Peters, “Impact of Macular Pigment on Fundus Autofluorescence Lifetimes,” Invest. Ophthalmol. Vis. Sci. 56(8), 4668–4679 (2015).
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D. Schweitzer, S. Schenke, M. Hammer, F. Schweitzer, S. Jentsch, E. Birckner, W. Becker, and A. Bergmann, “Towards metabolic mapping of the human retina,” Microsc. Res. Tech. 70(5), 410–419 (2007).
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D. Schweitzer, M. Hammer, F. Schweitzer, R. Anders, T. Doebbecke, S. Schenke, E. R. Gaillard, and E. R. Gaillard, “In vivo measurement of time-resolved autofluorescence at the human fundus,” J. Biomed. Opt. 9(6), 1214–1222 (2004).
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J. Schmidt, S. Peters, L. Sauer, D. Schweitzer, M. Klemm, R. Augsten, N. Müller, and M. Hammer, “Fundus autofluorescence lifetimes are increased in non-proliferative diabetic retinopathy,” Acta Ophthalmol. 95(1), 33–40 (2017).
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R. Peters, A. Brünger, and K. Schulten, “Continuous fluorescence microphotolysis: A sensitive method for study of diffusion processes in single cells,” Proc. Natl. Acad. Sci. U.S.A. 78(2), 962–966 (1981).
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J. Schmidt, S. Peters, L. Sauer, D. Schweitzer, M. Klemm, R. Augsten, N. Müller, and M. Hammer, “Fundus autofluorescence lifetimes are increased in non-proliferative diabetic retinopathy,” Acta Ophthalmol. 95(1), 33–40 (2017).
[Crossref] [PubMed]

D. Schweitzer, L. Deutsch, M. Klemm, S. Jentsch, M. Hammer, S. Peters, J. Haueisen, U. A. Müller, and J. Dawczynski, “Fluorescence lifetime imaging ophthalmoscopy in type 2 diabetic patients who have no signs of diabetic retinopathy,” J. Biomed. Opt. 20(6), 61106 (2015).
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M. Klemm, D. Schweitzer, S. Peters, L. Sauer, M. Hammer, and J. Haueisen, “FLIMX: A Software Package to Determine and Analyze the Fluorescence Lifetime in Time-Resolved Fluorescence Data from the Human Eye,” PLoS One 10(7), e0131640 (2015).
[Crossref] [PubMed]

L. Sauer, D. Schweitzer, L. Ramm, R. Augsten, M. Hammer, and S. Peters, “Impact of Macular Pigment on Fundus Autofluorescence Lifetimes,” Invest. Ophthalmol. Vis. Sci. 56(8), 4668–4679 (2015).
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D. Schweitzer, E. R. Gaillard, J. Dillon, R. F. Mullins, S. Russell, B. Hoffmann, S. Peters, M. Hammer, and C. Biskup, “Time-resolved autofluorescence imaging of human donor retina tissue from donors with significant extramacular drusen,” Invest. Ophthalmol. Vis. Sci. 53(7), 3376–3386 (2012).
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D. Schweitzer, S. Quick, M. Klemm, M. Hammer, S. Jentsch, and J. Dawczynski, “[Time-resolved autofluorescence in retinal vascular occlusions],” Ophthalmologe 107(12), 1145–1152 (2010).
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D. Schweitzer, S. Schenke, M. Hammer, F. Schweitzer, S. Jentsch, E. Birckner, W. Becker, and A. Bergmann, “Towards metabolic mapping of the human retina,” Microsc. Res. Tech. 70(5), 410–419 (2007).
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M. Hammer, S. Richter, K. H. Guehrs, and D. Schweitzer, “Retinal pigment epithelium cell damage by A2-E and its photo-derivatives,” Mol. Vis. 12, 1348–1354 (2006).
[PubMed]

D. Schweitzer, M. Hammer, F. Schweitzer, R. Anders, T. Doebbecke, S. Schenke, E. R. Gaillard, and E. R. Gaillard, “In vivo measurement of time-resolved autofluorescence at the human fundus,” J. Biomed. Opt. 9(6), 1214–1222 (2004).
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Schweitzer, F.

D. Schweitzer, S. Schenke, M. Hammer, F. Schweitzer, S. Jentsch, E. Birckner, W. Becker, and A. Bergmann, “Towards metabolic mapping of the human retina,” Microsc. Res. Tech. 70(5), 410–419 (2007).
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D. Schweitzer, M. Hammer, F. Schweitzer, R. Anders, T. Doebbecke, S. Schenke, E. R. Gaillard, and E. R. Gaillard, “In vivo measurement of time-resolved autofluorescence at the human fundus,” J. Biomed. Opt. 9(6), 1214–1222 (2004).
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Smith, R. T.

T. Ben Ami, Y. Tong, A. Bhuiyan, C. Huisingh, Z. Ablonczy, T. Ach, C. A. Curcio, and R. T. Smith, “Spatial and Spectral Characterization of Human Retinal Pigment Epithelium Fluorophore Families by Ex Vivo Hyperspectral Autofluorescence Imaging,” Transl. Vis. Sci. Technol. 5(3), 5 (2016).
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F. Delori, J. P. Greenberg, R. L. Woods, J. Fischer, T. Duncker, J. Sparrow, and R. T. Smith, “Quantitative measurements of autofluorescence with the scanning laser ophthalmoscope,” Invest. Ophthalmol. Vis. Sci. 52(13), 9379–9390 (2011).
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L. Song, E. J. Hennink, I. T. Young, and H. J. Tanke, “Photobleaching kinetics of fluorescein in quantitative fluorescence microscopy,” Biophys. J. 68(6), 2588–2600 (1995).
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S. Schmitz-Valckenberg, F. G. Holz, A. C. Bird, and R. F. Spaide, “Fundus autofluorescence imaging: review and perspectives,” Retina 28(3), 385–409 (2008).
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F. Delori, J. P. Greenberg, R. L. Woods, J. Fischer, T. Duncker, J. Sparrow, and R. T. Smith, “Quantitative measurements of autofluorescence with the scanning laser ophthalmoscope,” Invest. Ophthalmol. Vis. Sci. 52(13), 9379–9390 (2011).
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H. J. Kim and J. R. Sparrow, “Novel bisretinoids of human retina are lyso alkyl ether glycerophosphoethanolamine-bearing A2PE species,” J. Lipid Res. 59(9), 1620–1629 (2018).
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Z. Liu, K. Ueda, H. J. Kim, and J. R. Sparrow, “Photobleaching and Fluorescence Recovery of RPE Bisretinoids,” PLoS One 10(9), e0138081 (2015).
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K. Yamamoto, J. Zhou, J. J. Hunter, D. R. Williams, and J. R. Sparrow, “Toward an understanding of bisretinoid autofluorescence bleaching and recovery,” Invest. Ophthalmol. Vis. Sci. 53(7), 3536–3544 (2012).
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J. R. Sparrow, E. Gregory-Roberts, K. Yamamoto, A. Blonska, S. K. Ghosh, K. Ueda, and J. Zhou, “The bisretinoids of retinal pigment epithelium,” Prog. Retin. Eye Res. 31(2), 121–135 (2012).
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J. R. Sparrow, Y. Wu, C. Y. Kim, and J. Zhou, “Phospholipid meets all-trans-retinal: the making of RPE bisretinoids,” J. Lipid Res. 51(2), 247–261 (2010).
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J. R. Sparrow, Y. Wu, T. Nagasaki, K. D. Yoon, K. Yamamoto, and J. Zhou, “Fundus autofluorescence and the bisretinoids of retina,” Photochem. Photobiol. Sci. 9(11), 1480–1489 (2010).
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S. R. Kim, K. Nakanishi, Y. Itagaki, and J. R. Sparrow, “Photooxidation of A2-PE, a photoreceptor outer segment fluorophore, and protection by lutein and zeaxanthin,” Exp. Eye Res. 82(5), 828–839 (2006).
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J. R. Sparrow, K. Nakanishi, and C. A. Parish, “The lipofuscin fluorophore A2E mediates blue light-induced damage to retinal pigmented epithelial cells,” Invest. Ophthalmol. Vis. Sci. 41(7), 1981–1989 (2000).
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F. C. Delori, C. K. Dorey, G. Staurenghi, O. Arend, D. G. Goger, and J. J. Weiter, “In vivo fluorescence of the ocular fundus exhibits retinal pigment epithelium lipofuscin characteristics,” Invest. Ophthalmol. Vis. Sci. 36(3), 718–729 (1995).
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Y. Miura, G. Huettmann, R. Orzekowsky-Schroeder, P. Steven, M. Szaszák, N. Koop, and R. Brinkmann, “Two-photon microscopy and fluorescence lifetime imaging of retinal pigment epithelial cells under oxidative stress,” Invest. Ophthalmol. Vis. Sci. 54(5), 3366–3377 (2013).
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Y. Miura, G. Huettmann, R. Orzekowsky-Schroeder, P. Steven, M. Szaszák, N. Koop, and R. Brinkmann, “Two-photon microscopy and fluorescence lifetime imaging of retinal pigment epithelial cells under oxidative stress,” Invest. Ophthalmol. Vis. Sci. 54(5), 3366–3377 (2013).
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L. Song, E. J. Hennink, I. T. Young, and H. J. Tanke, “Photobleaching kinetics of fluorescein in quantitative fluorescence microscopy,” Biophys. J. 68(6), 2588–2600 (1995).
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T. Ben Ami, Y. Tong, A. Bhuiyan, C. Huisingh, Z. Ablonczy, T. Ach, C. A. Curcio, and R. T. Smith, “Spatial and Spectral Characterization of Human Retinal Pigment Epithelium Fluorophore Families by Ex Vivo Hyperspectral Autofluorescence Imaging,” Transl. Vis. Sci. Technol. 5(3), 5 (2016).
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Z. Liu, K. Ueda, H. J. Kim, and J. R. Sparrow, “Photobleaching and Fluorescence Recovery of RPE Bisretinoids,” PLoS One 10(9), e0138081 (2015).
[Crossref] [PubMed]

J. R. Sparrow, E. Gregory-Roberts, K. Yamamoto, A. Blonska, S. K. Ghosh, K. Ueda, and J. Zhou, “The bisretinoids of retinal pigment epithelium,” Prog. Retin. Eye Res. 31(2), 121–135 (2012).
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F. C. Delori, C. K. Dorey, G. Staurenghi, O. Arend, D. G. Goger, and J. J. Weiter, “In vivo fluorescence of the ocular fundus exhibits retinal pigment epithelium lipofuscin characteristics,” Invest. Ophthalmol. Vis. Sci. 36(3), 718–729 (1995).
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A. J. Wenzel, K. Fuld, and J. M. Stringham, “Light exposure and macular pigment optical density,” Invest. Ophthalmol. Vis. Sci. 44(1), 306–309 (2003).
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Wilk, M. B.

S. S. Shapiro and M. B. Wilk, “An Analysis of Variance Test for Normality (Complete Samples),” Biometrika 52(3-4), 591–611 (1965).
[Crossref]

Williams, D. R.

K. Yamamoto, J. Zhou, J. J. Hunter, D. R. Williams, and J. R. Sparrow, “Toward an understanding of bisretinoid autofluorescence bleaching and recovery,” Invest. Ophthalmol. Vis. Sci. 53(7), 3536–3544 (2012).
[Crossref] [PubMed]

Wolf, S.

C. Dysli, K. Schürch, E. Pascal, S. Wolf, and M. S. Zinkernagel, “Fundus Autofluorescence Lifetime Patterns in Retinitis Pigmentosa,” Invest. Ophthalmol. Vis. Sci. 59(5), 1769–1778 (2018).
[Crossref] [PubMed]

C. Dysli, S. Wolf, M. Y. Berezin, L. Sauer, M. Hammer, and M. S. Zinkernagel, “Fluorescence lifetime imaging ophthalmoscopy,” Prog. Retin. Eye Res. 60, 120–143 (2017).
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C. Dysli, R. Fink, S. Wolf, and M. S. Zinkernagel, “Fluorescence Lifetimes of Drusen in Age-Related Macular Degeneration,” Invest. Ophthalmol. Vis. Sci. 58(11), 4856–4862 (2017).
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C. Dysli, S. Wolf, K. Hatz, and M. S. Zinkernagel, “Fluorescence Lifetime Imaging in Stargardt Disease: Potential Marker for Disease Progression,” Invest. Ophthalmol. Vis. Sci. 57(3), 832–841 (2016).
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C. Dysli, S. Wolf, and M. S. Zinkernagel, “Autofluorescence Lifetimes in Geographic Atrophy in Patients With Age-Related Macular Degeneration,” Invest. Ophthalmol. Vis. Sci. 57(6), 2479–2487 (2016).
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C. Dysli, S. Wolf, and M. S. Zinkernagel, “Fluorescence lifetime imaging in retinal artery occlusion,” Invest. Ophthalmol. Vis. Sci. 56(5), 3329–3336 (2015).
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C. Dysli, G. Quellec, M. Abegg, M. N. Menke, U. Wolf-Schnurrbusch, J. Kowal, J. Blatz, O. La Schiazza, A. B. Leichtle, S. Wolf, and M. S. Zinkernagel, “Quantitative analysis of fluorescence lifetime measurements of the macula using the fluorescence lifetime imaging ophthalmoscope in healthy subjects,” Invest. Ophthalmol. Vis. Sci. 55(4), 2106–2113 (2014).
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C. Dysli, G. Quellec, M. Abegg, M. N. Menke, U. Wolf-Schnurrbusch, J. Kowal, J. Blatz, O. La Schiazza, A. B. Leichtle, S. Wolf, and M. S. Zinkernagel, “Quantitative analysis of fluorescence lifetime measurements of the macula using the fluorescence lifetime imaging ophthalmoscope in healthy subjects,” Invest. Ophthalmol. Vis. Sci. 55(4), 2106–2113 (2014).
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Woods, R. L.

F. Delori, J. P. Greenberg, R. L. Woods, J. Fischer, T. Duncker, J. Sparrow, and R. T. Smith, “Quantitative measurements of autofluorescence with the scanning laser ophthalmoscope,” Invest. Ophthalmol. Vis. Sci. 52(13), 9379–9390 (2011).
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Wu, Y.

J. R. Sparrow, Y. Wu, T. Nagasaki, K. D. Yoon, K. Yamamoto, and J. Zhou, “Fundus autofluorescence and the bisretinoids of retina,” Photochem. Photobiol. Sci. 9(11), 1480–1489 (2010).
[Crossref] [PubMed]

J. R. Sparrow, Y. Wu, C. Y. Kim, and J. Zhou, “Phospholipid meets all-trans-retinal: the making of RPE bisretinoids,” J. Lipid Res. 51(2), 247–261 (2010).
[Crossref] [PubMed]

Yamamoto, K.

J. R. Sparrow, E. Gregory-Roberts, K. Yamamoto, A. Blonska, S. K. Ghosh, K. Ueda, and J. Zhou, “The bisretinoids of retinal pigment epithelium,” Prog. Retin. Eye Res. 31(2), 121–135 (2012).
[Crossref] [PubMed]

K. Yamamoto, J. Zhou, J. J. Hunter, D. R. Williams, and J. R. Sparrow, “Toward an understanding of bisretinoid autofluorescence bleaching and recovery,” Invest. Ophthalmol. Vis. Sci. 53(7), 3536–3544 (2012).
[Crossref] [PubMed]

J. R. Sparrow, Y. Wu, T. Nagasaki, K. D. Yoon, K. Yamamoto, and J. Zhou, “Fundus autofluorescence and the bisretinoids of retina,” Photochem. Photobiol. Sci. 9(11), 1480–1489 (2010).
[Crossref] [PubMed]

Yoon, K. D.

J. R. Sparrow, Y. Wu, T. Nagasaki, K. D. Yoon, K. Yamamoto, and J. Zhou, “Fundus autofluorescence and the bisretinoids of retina,” Photochem. Photobiol. Sci. 9(11), 1480–1489 (2010).
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Young, I. T.

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Zhou, J.

J. R. Sparrow, E. Gregory-Roberts, K. Yamamoto, A. Blonska, S. K. Ghosh, K. Ueda, and J. Zhou, “The bisretinoids of retinal pigment epithelium,” Prog. Retin. Eye Res. 31(2), 121–135 (2012).
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K. Yamamoto, J. Zhou, J. J. Hunter, D. R. Williams, and J. R. Sparrow, “Toward an understanding of bisretinoid autofluorescence bleaching and recovery,” Invest. Ophthalmol. Vis. Sci. 53(7), 3536–3544 (2012).
[Crossref] [PubMed]

J. R. Sparrow, Y. Wu, T. Nagasaki, K. D. Yoon, K. Yamamoto, and J. Zhou, “Fundus autofluorescence and the bisretinoids of retina,” Photochem. Photobiol. Sci. 9(11), 1480–1489 (2010).
[Crossref] [PubMed]

J. R. Sparrow, Y. Wu, C. Y. Kim, and J. Zhou, “Phospholipid meets all-trans-retinal: the making of RPE bisretinoids,” J. Lipid Res. 51(2), 247–261 (2010).
[Crossref] [PubMed]

Zinkernagel, M. S.

L. Sauer, K. M. Andersen, C. Dysli, M. S. Zinkernagel, P. S. Bernstein, and M. Hammer, “Review of clinical approaches in fluorescence lifetime imaging ophthalmoscopy,” J. Biomed. Opt. 23(9), 1–20 (2018).
[Crossref] [PubMed]

C. Dysli, K. Schürch, E. Pascal, S. Wolf, and M. S. Zinkernagel, “Fundus Autofluorescence Lifetime Patterns in Retinitis Pigmentosa,” Invest. Ophthalmol. Vis. Sci. 59(5), 1769–1778 (2018).
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C. Dysli, S. Wolf, M. Y. Berezin, L. Sauer, M. Hammer, and M. S. Zinkernagel, “Fluorescence lifetime imaging ophthalmoscopy,” Prog. Retin. Eye Res. 60, 120–143 (2017).
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C. Dysli, R. Fink, S. Wolf, and M. S. Zinkernagel, “Fluorescence Lifetimes of Drusen in Age-Related Macular Degeneration,” Invest. Ophthalmol. Vis. Sci. 58(11), 4856–4862 (2017).
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C. Dysli, S. Wolf, K. Hatz, and M. S. Zinkernagel, “Fluorescence Lifetime Imaging in Stargardt Disease: Potential Marker for Disease Progression,” Invest. Ophthalmol. Vis. Sci. 57(3), 832–841 (2016).
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C. Dysli, S. Wolf, and M. S. Zinkernagel, “Autofluorescence Lifetimes in Geographic Atrophy in Patients With Age-Related Macular Degeneration,” Invest. Ophthalmol. Vis. Sci. 57(6), 2479–2487 (2016).
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[Crossref] [PubMed]

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[Crossref] [PubMed]

C. Dysli, S. Wolf, and M. S. Zinkernagel, “Fluorescence lifetime imaging in retinal artery occlusion,” Invest. Ophthalmol. Vis. Sci. 56(5), 3329–3336 (2015).
[Crossref] [PubMed]

C. Dysli, S. Wolf, K. Hatz, and M. S. Zinkernagel, “Fluorescence Lifetime Imaging in Stargardt Disease: Potential Marker for Disease Progression,” Invest. Ophthalmol. Vis. Sci. 57(3), 832–841 (2016).
[Crossref] [PubMed]

C. Dysli, K. Schürch, E. Pascal, S. Wolf, and M. S. Zinkernagel, “Fundus Autofluorescence Lifetime Patterns in Retinitis Pigmentosa,” Invest. Ophthalmol. Vis. Sci. 59(5), 1769–1778 (2018).
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C. Dysli, G. Quellec, M. Abegg, M. N. Menke, U. Wolf-Schnurrbusch, J. Kowal, J. Blatz, O. La Schiazza, A. B. Leichtle, S. Wolf, and M. S. Zinkernagel, “Quantitative analysis of fluorescence lifetime measurements of the macula using the fluorescence lifetime imaging ophthalmoscope in healthy subjects,” Invest. Ophthalmol. Vis. Sci. 55(4), 2106–2113 (2014).
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L. Sauer, K. M. Andersen, B. Li, R. H. Gensure, M. Hammer, and P. S. Bernstein, “Fluorescence Lifetime Imaging Ophthalmoscopy (FLIO) of Macular Pigment,” Invest. Ophthalmol. Vis. Sci. 59(7), 3094–3103 (2018).
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L. Sauer, D. Schweitzer, L. Ramm, R. Augsten, M. Hammer, and S. Peters, “Impact of Macular Pigment on Fundus Autofluorescence Lifetimes,” Invest. Ophthalmol. Vis. Sci. 56(8), 4668–4679 (2015).
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D. Schweitzer, L. Deutsch, M. Klemm, S. Jentsch, M. Hammer, S. Peters, J. Haueisen, U. A. Müller, and J. Dawczynski, “Fluorescence lifetime imaging ophthalmoscopy in type 2 diabetic patients who have no signs of diabetic retinopathy,” J. Biomed. Opt. 20(6), 61106 (2015).
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L. Sauer, K. M. Andersen, C. Dysli, M. S. Zinkernagel, P. S. Bernstein, and M. Hammer, “Review of clinical approaches in fluorescence lifetime imaging ophthalmoscopy,” J. Biomed. Opt. 23(9), 1–20 (2018).
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D. Schweitzer, M. Hammer, F. Schweitzer, R. Anders, T. Doebbecke, S. Schenke, E. R. Gaillard, and E. R. Gaillard, “In vivo measurement of time-resolved autofluorescence at the human fundus,” J. Biomed. Opt. 9(6), 1214–1222 (2004).
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J. R. Sparrow, Y. Wu, C. Y. Kim, and J. Zhou, “Phospholipid meets all-trans-retinal: the making of RPE bisretinoids,” J. Lipid Res. 51(2), 247–261 (2010).
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Figures (6)

Fig. 1
Fig. 1 Schematic of the FLIO instrument. A 473 nm pulsed laser is fed into a scanning laser ophthalmoscope by a monomode fiber to excite retinal autofluorescence. Fluorescence emission is transmitted by a multimode fiber to a dichroic mirror (DM), which divides the fluorescence signal into a short (498–560 nm) and a long spectral channel (560–720 nm). Hybrid photomultiplier tube detectors convert the fluorescence photons into electrical pulses, which are then processed using time-correlated single photon-counting (TCSPC). A continuous wave (CW) infrared (IR) laser illuminates the fundus for online image registration. Blocking filters (BF) protect the detectors from excitation and infrared light.
Fig. 2
Fig. 2 Custom-made lightproof mask, its optical density, miniaturized bleaching device, and the bleaching spectrum. The custom-made lightproof mask used for dark adaptation is shown in (A). Its optical density is shown in (B). The miniaturized tube-shaped bleaching device (C) consists a high-power white light emitting diode, connected to a standard power supply, a Lambertian-scattering plastic hemisphere (concave against the eye, diameter 40 mm) and a passive aluminum heat sink. The bleaching device was connected to the side of the FLIO device. The bleaching procedure is demonstrated for a right eye using a Styrofoam head model. The effective bleaching spectrum (D) was measured with a scanning spectrometer and a fiber-connected detector. For a bleaching distance of 20 mm (tube edge - cornea), a normalized power of 0.46 mW/cm2 (corresponds to 1379 lx) was measured. The luminance was 3200 ± 200 cd/m2.
Fig. 3
Fig. 3 FAF intensity and lifetime images from SSC of a healthy volunteer. FAF intensity (A), and corresponding mean FAF lifetime images (B) for dark-adapted (1), bleached (2), and recovered (3) states in one healthy volunteer. Although the fluorescence intensity and lifetime images were very similar, the acquisition times differed significantly. The central area (C), inner ring (IR), and outer ring (OR) from the ETDRS grid were used for the data analysis (diameter 1, 3, and 6 mm, respectively). For better comparison, the color scaling is identical for the three fluorescence intensities, and the fluorescence lifetime plots.
Fig. 4
Fig. 4 Fluorescence lifetimes of the different bleaching states at different fundus locations. The fluorescence lifetimes are presented as mean ± standard deviation for both spectral channels in the central area, the inner ring, and the outer ring of the ETDRS grid. Significant differences are marked by * (p < 0.05). The differences between dark-adapted and bleached states of fluorescence lifetime τ1 in the long spectral channel occurred at trend level for the outer ring (p = 0.092). The plots are on a logarithmic scale, and values are rounded to the nearest decimal.
Fig. 5
Fig. 5 Bonferroni-corrected confidence intervals (confidence level 95%) of the pairwise fluorescence lifetime differences between the different bleaching states at different fundus locations. The scale for confidence intervals of the fluorescence lifetime τ3 is adjusted for better visibility (red). The confidence interval not including zero indicates a significant difference.
Fig. 6
Fig. 6 Average acquisition speeds for the different bleaching states at the different fundus locations. The acquisition speeds are plotted as mean ± standard deviation for both spectral channels in the central area, the inner ring, and the outer ring of the ETDRS grid. Significant differences are marked by * (p < 0.05).

Tables (1)

Tables Icon

Table 1 Fluorescence lifetime changes in patients with different diseases compared to the present worka

Equations (7)

Equations on this page are rendered with MathJax. Learn more.

E IRCL = 770 2500 E λ Δλ
E VIRR = 380 1400 E λ R(λ)Δλ
B= E v E v + E vp ( 1 e ( 1+ E v E vp ) t τ p )
r(t) r max =1B e t τ p
I(t)=IRF i α i e t τ i +b
χ r 2 = 1 mp j=1 m ( I M ( t j ) I C ( t j ) ) 2 I M ( t j )
τ m = i α i τ i i α i

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