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Published in: Graefe's Archive for Clinical and Experimental Ophthalmology 3/2019

01-03-2019 | Retinal Disorders

Development of a novel noninvasive system for measurement and imaging of the arterial phase oxygen density ratio in the retinal microcirculation

Authors: Shinichiro Ishikawa, Yukiyasu Yoshinaga, Daichi Kantake, Daisuke Nakamura, Noriko Yoshida, Toshio Hisatomi, Yasuhiro Ikeda, Tatsuro Ishibashi, Hiroshi Enaida

Published in: Graefe's Archive for Clinical and Experimental Ophthalmology | Issue 3/2019

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Abstract

Purpose

This study was conducted in order to develop a novel noninvasive system for measurement and imaging of the arterial oxygen density ratio (ODR) in the retinal microcirculation.

Methods

We developed a system composed of two digital cameras with two different filters, which were attached to a fundus camera capable of simultaneously obtaining two images. Actual measurements were performed on healthy volunteer eyes (n = 61). A new algorithm for ODR measurement and pixel-level imaging of erythrocytes was constructed from these data. The algorithm was based on the morphological closing operation and the line convergence index filter. For system calibration, we compared and verified the ODR values in arterioles and venules that were specified in advance for 56 eyes with reproducibility. In 10 additional volunteers, ODR measurements and imaging of the arterial phase in the retinal microcirculation corresponding to changes in oxygen saturation of the peripheral arteries at normal breathing and breath holding were performed.

Results

Estimation of incident light to erythrocytes and pixel-level ODR calculation were achieved using the algorithm. The mean ODR values of arterioles and venules were 0.77 ± 0.060 and 1.02 ± 0.067, respectively. It was possible to separate these regions, calibrate at the pixel level, and estimate the arterial phase. In each of the 10 volunteers, changes in the arterial phase ODR corresponding to changes in oxygen saturation of the peripheral arteries were observed before and after breath holding on ODR images. The mean ODR in 10 volunteers was increased by breath holding (p < 0.05).

Conclusions

We developed a basic system for arterial phase ODR measurement and imaging of the retinal microcirculation. With further validation and development, this may provide a useful tool for evaluating retinal oxygen metabolism in the retinal microcirculation.
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Literature
1.
go back to reference Hickam JB, Frayser R, Ross JC (1963) A study of retinal venous blood oxygen saturation in human subjects by photographic means. Circulation 27:375–385CrossRefPubMed Hickam JB, Frayser R, Ross JC (1963) A study of retinal venous blood oxygen saturation in human subjects by photographic means. Circulation 27:375–385CrossRefPubMed
2.
go back to reference Beach JM, Schwenzer KJ, Srinivas S, Kim D, Tiedeman JS (1999) Oximetry of retinal vessels by dual-wavelength imaging: calibration and influence of pigmentation. J Appl Physiol 86:748–758CrossRefPubMed Beach JM, Schwenzer KJ, Srinivas S, Kim D, Tiedeman JS (1999) Oximetry of retinal vessels by dual-wavelength imaging: calibration and influence of pigmentation. J Appl Physiol 86:748–758CrossRefPubMed
3.
go back to reference Hardarson SH, Harris A, Karlsson RA, Halldorsson GH, Kagemann L, Rechtman E, Zoega GM, Eysteinsson T, Benediktsson JA, Thorsteinsson A, Jensen PK, Beach J, Stefánsson E (2006) Automatic retinal oximetry. Invest Ophthalmol Vis Sci 47:5011–5016CrossRefPubMed Hardarson SH, Harris A, Karlsson RA, Halldorsson GH, Kagemann L, Rechtman E, Zoega GM, Eysteinsson T, Benediktsson JA, Thorsteinsson A, Jensen PK, Beach J, Stefánsson E (2006) Automatic retinal oximetry. Invest Ophthalmol Vis Sci 47:5011–5016CrossRefPubMed
4.
go back to reference Hardarson SH, Stefánsson E (2010) Oxygen saturation in central retinal vein occlusion. Am J Ophthalmol 150:871–875CrossRefPubMed Hardarson SH, Stefánsson E (2010) Oxygen saturation in central retinal vein occlusion. Am J Ophthalmol 150:871–875CrossRefPubMed
5.
go back to reference Blondal R, Sturludottir MK, Hardarson SH, Halldorsson GH, Stefánsson E (2011) Reliability of vessel diameter measurements with a retinal oximeter. Graefes Arch Clin Exp Ophthalmol 249:1311–1317CrossRefPubMed Blondal R, Sturludottir MK, Hardarson SH, Halldorsson GH, Stefánsson E (2011) Reliability of vessel diameter measurements with a retinal oximeter. Graefes Arch Clin Exp Ophthalmol 249:1311–1317CrossRefPubMed
6.
go back to reference Hardarson SH, Stefánsson E (2012) Retinal oxygen saturation is altered in diabetic retinopathy. Br J Ophthalmol 96:560–563CrossRefPubMed Hardarson SH, Stefánsson E (2012) Retinal oxygen saturation is altered in diabetic retinopathy. Br J Ophthalmol 96:560–563CrossRefPubMed
7.
go back to reference Geirsdottir A, Hardarson SH, Olafsdottir OB, Stefánsson E (2014) Retinal oxygen metabolism in exudative age-related macular degeneration. Acta Ophthalmol 92:27–33CrossRefPubMed Geirsdottir A, Hardarson SH, Olafsdottir OB, Stefánsson E (2014) Retinal oxygen metabolism in exudative age-related macular degeneration. Acta Ophthalmol 92:27–33CrossRefPubMed
8.
go back to reference Tayyari F, Khuu LA, Flanagan JG, Singer S, Brent MH, Hudson C (2015) Retinal blood flow and retinal blood oxygen saturation in mild to moderate diabetic retinopathy. Invest Ophthalmol Vis Sci 56:6796–6800CrossRefPubMed Tayyari F, Khuu LA, Flanagan JG, Singer S, Brent MH, Hudson C (2015) Retinal blood flow and retinal blood oxygen saturation in mild to moderate diabetic retinopathy. Invest Ophthalmol Vis Sci 56:6796–6800CrossRefPubMed
9.
go back to reference Eysteinsson T, Hardarson SH, Bragason D, Stefánsson E (2014) Retinal vessel oxygen saturation and vessel diameter in retinitis pigmentosa. Acta Ophthalmol 92:449–453CrossRefPubMed Eysteinsson T, Hardarson SH, Bragason D, Stefánsson E (2014) Retinal vessel oxygen saturation and vessel diameter in retinitis pigmentosa. Acta Ophthalmol 92:449–453CrossRefPubMed
10.
go back to reference Türksever C, Valmaggia C, Orgül S, Schorderet DF, Flammer J, Todorova MG (2014) Retinal vessel oxygen saturation and its correlation with structural changes in retinitis pigmentosa. Acta Ophthalmol 92:454–460CrossRefPubMed Türksever C, Valmaggia C, Orgül S, Schorderet DF, Flammer J, Todorova MG (2014) Retinal vessel oxygen saturation and its correlation with structural changes in retinitis pigmentosa. Acta Ophthalmol 92:454–460CrossRefPubMed
11.
go back to reference Van Keer K, Abegão Pinto L, Willekens K, Stalmans I, Vandewalle E (2015) Correlation between peripapillary choroidal thickness and retinal vessel oxygen saturation in young healthy individuals and glaucoma patients. Invest Ophthalmol Vis Sci 56:3758–3762CrossRefPubMed Van Keer K, Abegão Pinto L, Willekens K, Stalmans I, Vandewalle E (2015) Correlation between peripapillary choroidal thickness and retinal vessel oxygen saturation in young healthy individuals and glaucoma patients. Invest Ophthalmol Vis Sci 56:3758–3762CrossRefPubMed
12.
go back to reference Olafsdottir OB, Eliasdottir TS, Kristjansdottir JV, Hardarson SH, Stefánsson E (2015) Retinal vessel oxygen saturation during 100% oxygen breathing in healthy individuals. PLoS One 10:e0128780CrossRefPubMedPubMedCentral Olafsdottir OB, Eliasdottir TS, Kristjansdottir JV, Hardarson SH, Stefánsson E (2015) Retinal vessel oxygen saturation during 100% oxygen breathing in healthy individuals. PLoS One 10:e0128780CrossRefPubMedPubMedCentral
13.
go back to reference Yang W, Fu Y, Dong Y, Lin L, Huang X, Li Y, Lin X, Gao Q (2016) Retinal vessel oxygen saturation in a healthy young Chinese population. Acta Ophthalmol 94:373–379CrossRefPubMed Yang W, Fu Y, Dong Y, Lin L, Huang X, Li Y, Lin X, Gao Q (2016) Retinal vessel oxygen saturation in a healthy young Chinese population. Acta Ophthalmol 94:373–379CrossRefPubMed
14.
go back to reference Willerslev A, Hansen MM, Klefter ON, Bjerrum OW, Hasselbalch HC, Clemmensen SN, Larsen M, Munch IC (2017) Non-invasive imaging of retinal blood flow in myeloproliferative neoplasms. Acta Ophthalmol 95:146–152CrossRefPubMed Willerslev A, Hansen MM, Klefter ON, Bjerrum OW, Hasselbalch HC, Clemmensen SN, Larsen M, Munch IC (2017) Non-invasive imaging of retinal blood flow in myeloproliferative neoplasms. Acta Ophthalmol 95:146–152CrossRefPubMed
15.
go back to reference Nitta E, Hirooka K, Shimazaki T, Sato S, Ukegawa K, Nakano Y, Tsujikawa A (2017) Retinal oxygen saturation before and after glaucoma surgery. Acta Ophthalmol 95:e350–e353CrossRefPubMed Nitta E, Hirooka K, Shimazaki T, Sato S, Ukegawa K, Nakano Y, Tsujikawa A (2017) Retinal oxygen saturation before and after glaucoma surgery. Acta Ophthalmol 95:e350–e353CrossRefPubMed
16.
go back to reference Stefánsson E, Olafsdottir OB, Einarsdottir AB, Eliasdottir TS, Eysteinsson T, Vehmeijer W, Vandewalle E, Bek T, Hardarson SH (2017) Retinal oximetry discovers novel biomarkers in retinal and brain diseases. Invest Ophthalmol Vis Sci 58:BIO227–BIO233CrossRefPubMed Stefánsson E, Olafsdottir OB, Einarsdottir AB, Eliasdottir TS, Eysteinsson T, Vehmeijer W, Vandewalle E, Bek T, Hardarson SH (2017) Retinal oximetry discovers novel biomarkers in retinal and brain diseases. Invest Ophthalmol Vis Sci 58:BIO227–BIO233CrossRefPubMed
17.
go back to reference Salem SA, Salem NM, Nandi AK (2007) Segmentation of retinal blood vessels using a novel clustering algorithm (RACAL) with a partial supervision strategy. Med Biol Eng Comput 45:261–273CrossRefPubMed Salem SA, Salem NM, Nandi AK (2007) Segmentation of retinal blood vessels using a novel clustering algorithm (RACAL) with a partial supervision strategy. Med Biol Eng Comput 45:261–273CrossRefPubMed
18.
go back to reference Matsopoulos GK, Mouravliansky NA, Delibasis KK, Nikita KS (1999) Automatic retinal image registration scheme using global optimization techniques. IEEE Trans Inf Technol Biomed 3:47–60CrossRefPubMed Matsopoulos GK, Mouravliansky NA, Delibasis KK, Nikita KS (1999) Automatic retinal image registration scheme using global optimization techniques. IEEE Trans Inf Technol Biomed 3:47–60CrossRefPubMed
19.
go back to reference Laliberté F, Gagnon L, Sheng Y (2003) Registration and fusion of retinal images—an evaluation study. IEEE Trans Med Imaging 22:661–673CrossRefPubMed Laliberté F, Gagnon L, Sheng Y (2003) Registration and fusion of retinal images—an evaluation study. IEEE Trans Med Imaging 22:661–673CrossRefPubMed
20.
go back to reference Kobatake H, Yoshinaga Y (1996) Detection of spicules on mammogram based on skeleton analysis. IEEE Trans Med Imaging 15:235–245CrossRefPubMed Kobatake H, Yoshinaga Y (1996) Detection of spicules on mammogram based on skeleton analysis. IEEE Trans Med Imaging 15:235–245CrossRefPubMed
21.
go back to reference Jin XC, Ong SH, Jayasooriah J (1995) A domain operator for binary morphological processing. IEEE Trans Image Process 4:1042–1046CrossRefPubMed Jin XC, Ong SH, Jayasooriah J (1995) A domain operator for binary morphological processing. IEEE Trans Image Process 4:1042–1046CrossRefPubMed
22.
go back to reference Kobatake H, Hashimoto S (1999) Convergence index filter for vector fields. IEEE Trans Image Process 8:1029–1038CrossRefPubMed Kobatake H, Hashimoto S (1999) Convergence index filter for vector fields. IEEE Trans Image Process 8:1029–1038CrossRefPubMed
24.
go back to reference Türksever C, Orgül S, Todorova MG (2015) Reproducibility of retinal oximetry measurements in healthy and diseased retinas. Acta Ophthalmol 93:e439–e445CrossRefPubMed Türksever C, Orgül S, Todorova MG (2015) Reproducibility of retinal oximetry measurements in healthy and diseased retinas. Acta Ophthalmol 93:e439–e445CrossRefPubMed
25.
go back to reference Told R, Boltz A, Schmetterer L, Garhöfer G, Sacu S, Schmidt-Erfurth U, Pollreisz A (2018) Method comparison of two non-invasive dual-wavelength spectrophotometric retinal oximeters in healthy young subjects during normoxia. Acta Ophthalmol. https://doi.org/10.1111/aos.13719 Told R, Boltz A, Schmetterer L, Garhöfer G, Sacu S, Schmidt-Erfurth U, Pollreisz A (2018) Method comparison of two non-invasive dual-wavelength spectrophotometric retinal oximeters in healthy young subjects during normoxia. Acta Ophthalmol. https://​doi.​org/​10.​1111/​aos.​13719
Metadata
Title
Development of a novel noninvasive system for measurement and imaging of the arterial phase oxygen density ratio in the retinal microcirculation
Authors
Shinichiro Ishikawa
Yukiyasu Yoshinaga
Daichi Kantake
Daisuke Nakamura
Noriko Yoshida
Toshio Hisatomi
Yasuhiro Ikeda
Tatsuro Ishibashi
Hiroshi Enaida
Publication date
01-03-2019
Publisher
Springer Berlin Heidelberg
Published in
Graefe's Archive for Clinical and Experimental Ophthalmology / Issue 3/2019
Print ISSN: 0721-832X
Electronic ISSN: 1435-702X
DOI
https://doi.org/10.1007/s00417-018-04211-z

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