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Graefe's Archive for Clinical and Experimental Ophthalmology

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Open Access 01-02-2021 | Glaucoma | Glaucoma

Imaging video plethysmography shows reduced signal amplitude in glaucoma patients in the area of the microvascular tissue of the optic nerve head

Authors: Ralf-Peter Tornow, Radim Kolar, Jan Odstrcilik, Ivana Labounkova, Folkert Horn

Published in: Graefe's Archive for Clinical and Experimental Ophthalmology | Issue 2/2021

Abstract

Purpose

To measure parameters of the cardiac cycle-induced pulsatile light absorption signal (plethysmography signal) of the optic nerve head (ONH) and to compare parameters between normal subjects and patients with different stages of glaucoma.

Patients and methods

A recently developed video ophthalmoscope was used to acquire short video sequences (10 s) of the ONH. After image registration and trend correction, the pulsatile changing light absorption at the ONH tissue (excluding large vessels) was calculated. The changing light absorption depends on the pulsatile changing blood volume. Various parameters, including peak amplitude, steepness, time-to-peak, full width at half maximum (FWHM), and pulse duration, were calculated for averaged individual pulses (heartbeats) of the plethysmography signal. This method was applied to 19 healthy control subjects and 91 subjects with ocular hypertension, as well as different stages of primary open-angle glaucoma (17 subjects with ocular hypertension, 24 with preperimetric glaucoma, and 50 with perimetric glaucoma).

Results

Compared to the normal subjects, significant reductions (p < 0.001) in peak amplitude and steepness were observed in the group of perimetric glaucoma patients, but no significant difference was found for time-to-peak, FWHM, and pulse duration. Peak amplitude and steepness showed high correlations with RNFL thickness (p < 0.001).

Conclusions

The presented low-cost video-ophthalmoscope permits measurement of the plethysmographic signal of the ONH tissue and calculation of different blood flow-related parameters. The reduced values of the amplitude and steepness parameters in perimetric glaucoma patients suggest decreased ONH perfusion and blood volume. This outcome is in agreement with results from other studies using OCT angiography and laser speckle flowgraphy, which confirm reduced capillary density in these patients.

Registration site: www.clinicaltrials.gov, Trial registration number: NCT00494923

Flammer J, Orgül S, Costa VP et al (2002) The impact of ocular blood flow in glaucoma. Prog Retin Eye Res 21:359–393CrossRefPubMed

Schubert G (1936) Untersuchung des Blutsauerstoffgehaltes und der Durchblutung des Auges auf lichtelektrischem Wege. Albrecht Von Graefes Arch Ophthalmol 135:558–560. https://doi.org/10.1007/BF01853424CrossRef

Trokel S (1964) Measurement of ocular blood flow and volume by reflective densitometry. Arch Ophthalmol 71:88–92CrossRefPubMed

Trokel S (1964) Photometric study of ocular blood flow in man. Arch Ophthalmol 71:528–530CrossRefPubMed

Beintema DK, Mook GA, Worst JGF (1964) Recording of arm-to-retina circulation-time by means of fundus reflectometry. Ophthalmologica 148:163–168CrossRefPubMed

Matsuo H, Kogure F, Takahasi K (1966) Studies of the photoelectric plethysmogram of the eye. Procceedings XX Int Congr Ophthalmol 1966 178–182

Tornow RP, Kopp O, Schultheiss B (2003) Time course of fundus reflection changes according to the cardiac cycle. In: Invest. Ophthalmol. Vis. Sci. pp 1296-ARVO Abstract

Tornow RP, Kopp O (2006) Time course and frequency spectrum (0 to 12,5 Hz) of fundus reflection. In: Invest. Ophthalmol. Vis. Sci. pp 3753-ARVO Abstract

Lovasik JV, Gagnon M, Kergoat H (1994) A novel noninvasive videographic method for quantifying changes in the chromaticity of the optic nerve head with changes in the intraocular pressure, pulsatile choroidal blood flow and visual neural function in humans. Surv Ophthalmol 38(Suppl):S35–S51CrossRefPubMed

10.

Morgan WH, Hazelton ML, Betz-Stablein BD et al (2014) Photoplethysmographic measurement of various retinal vascular pulsation parameters and measurement of the venous phase delay. Investig Ophthalmol Vis Sci 55:5998–6006. https://doi.org/10.1167/iovs.14-15104CrossRef

11.

Hassan H, Jaidka S, Dwyer VM, Hu S (2018) Assessing blood vessel perfusion and vital signs through retinal imaging photoplethysmography. Biomed Opt Express 9:2351. https://doi.org/10.1364/boe.9.002351CrossRefPubMedPubMedCentral

12.

Briers JD (1996) Laser Doppler and time-varying speckle: a reconciliation. J Opt Soc Am A 13:345. https://doi.org/10.1364/josaa.13.000345CrossRef

13.

Briers JD (2001) Laser Doppler, speckle and related techniques for blood perfusion mapping and imaging. Physiol Meas 22:R35–R66. https://doi.org/10.1088/0967-3334/22/4/201CrossRefPubMed

14.

Michelson G, Schmauss B (1995) Two dimensional mapping of the perfusion of the retina and optic nerve head. Br J Ophthalmol 79:1126–1132. https://doi.org/10.1136/bjo.79.12.1126CrossRefPubMedPubMedCentral

15.

Wang RK, Jacques SL, Ma Z et al (2007) Three dimensional optical angiography. Opt Express 15:4083. https://doi.org/10.1364/oe.15.004083CrossRefPubMed

16.

Jia Y, Morrison JC, Tokayer J et al (2012) Quantitative OCT angiography of optic nerve head blood flow. Biomed Opt Express 3:3127. https://doi.org/10.1364/boe.3.003127CrossRefPubMedPubMedCentral

17.

Zhang A, Zhang Q, Chen C-L, Wang RK (2015) Methods and algorithms for optical coherence tomography-based angiography: a review and comparison. J Biomed Opt 20:100901. https://doi.org/10.1117/1.jbo.20.10.100901CrossRefPubMedPubMedCentral

18.

Gao SS, Jia Y, Zhang M et al (2016) Optical coherence tomography angiography. Investig Ophthalmol Vis Sci 57:OCT27–OCT36. https://doi.org/10.1167/iovs.15-19043CrossRef

19.

Hagag AM, Gao SS, Jia Y, Huang D (2017) Optical coherence tomography angiography: technical principles and clinical applications in ophthalmology. Taiwan J Ophthalmol 7:115–129. https://doi.org/10.4103/tjo.tjo_31_17CrossRefPubMedPubMedCentral

20.

Gräfe MGO, Gondre M, de Boer JF (2019) Precision analysis and optimization in phase decorrelation OCT velocimetry. Biomed Opt Express 10:1297. https://doi.org/10.1364/boe.10.001297CrossRefPubMedPubMedCentral

21.

Chen C-L, Bojikian KD, Gupta D et al (2016) Optic nerve head perfusion in normal eyes and eyes with glaucoma using optical coherence tomography-based microangiography. Quant Imaging Med Surg 6:125. https://doi.org/10.21037/QIMS.2016.03.05CrossRefPubMedPubMedCentral

22.

Wang X, Jiang C, Ko T et al (2015) Correlation between optic disc perfusion and glaucomatous severity in patients with open-angle glaucoma: an optical coherence tomography angiography study. Graefes Arch Clin Exp Ophthalmol 253:1557–1564. https://doi.org/10.1007/s00417-015-3095-yCrossRefPubMed

23.

Rao HL, Kadambi SV, Weinreb RN et al (2017) Diagnostic ability of peripapillary vessel density measurements of optical coherence tomography angiography in primary open-angle and angle-closure glaucoma. Br J Ophthalmol 101. https://doi.org/10.1136/bjophthalmol-2016-309377

24.

Chihara E, Dimitrova G, Amano H, Chihara T (2017) Discriminatory power of superficial vessel density and prelaminar vascular flow index in eyes with glaucoma and ocular hypertension and normal eyes. Investig Ophthalmol Vis Sci 58:690–697. https://doi.org/10.1167/iovs.16-20709CrossRef

25.

Lommatzsch C, Rothaus K, Koch JM et al (2018) Vessel density in OCT angiography permits differentiation between normal and glaucomatous optic nerve heads. Int J Ophthalmol 11:835–843. https://doi.org/10.18240/ijo.2018.05.20CrossRefPubMedPubMedCentral

26.

Konishi N, Tokimoto Y, Kohra K, Fujii H (2002) New laser speckle flowgraphy system using CCD camera. Opt Rev. https://doi.org/10.1007/s10043-002-0163-4

27.

Luft N, Wozniak PA, Aschinger GC et al (2016) Ocular blood flow measurements in healthy white subjects using laser speckle flowgraphy. PLoS One 11:e0168190. https://doi.org/10.1371/journal.pone.0168190CrossRefPubMedPubMedCentral

28.

Mursch-Edlmayr AS, Luft N, Podkowinski D et al (2018) Laser speckle flowgraphy derived characteristics of optic nerve head perfusion in normal tension glaucoma and healthy individuals: a Pilot study. Sci Rep 8:5343. https://doi.org/10.1038/s41598-018-23149-0CrossRefPubMedPubMedCentral

29.

Yokoyama Y, Aizawa N, Chiba N et al (2011) Significant correlations between optic nerve head microcirculation and visual field defects and nerve fiber layer loss in glaucoma patients with myopic glaucomatous disk. Clin Ophthalmol 5:1721–1727. https://doi.org/10.2147/OPTH.S23204CrossRefPubMedPubMedCentral

30.

Shiga Y, Kunikata H, Aizawa N et al (2016) Optic nerve head blood flow, as measured by laser speckle flowgraphy, is significantly reduced in preperimetric glaucoma. Curr Eye Res 41:1447–1453. https://doi.org/10.3109/02713683.2015.1127974CrossRefPubMed

31.

Shiga Y, Omodaka K, Kunikata H et al (2013) Waveform analysis of ocular blood flow and the early detection of normal tension glaucoma. Investig Ophthalmol Vis Sci 54:7699–7706. https://doi.org/10.1167/iovs.13-12930CrossRef

32.

Tornow R-P, Odstrcilik J, Kolar R (2018) Time-resolved quantitative inter-eye comparison of cardiac cycle-induced blood volume changes in the human retina. Biomed Opt Express 9:6237. https://doi.org/10.1364/boe.9.006237CrossRefPubMedPubMedCentral

33.

Tornow RP, Kolar R, Odstrcilik J (2015) Non-mydriatic video ophthalmoscope to measure fast temporal changes of the human retina. In: Progress in Biomedical Optics and Imaging - Proceedings of SPIE. p 954006

34.

Jonas JB, Gusek GC, Naumann GOH (1988) Optic disc morphometry in chronic primary open-angle glaucoma - I. Morphometric intrapapillary characteristics. Graefes Arch Clin Exp Ophthalmol. https://doi.org/10.1007/BF02169199

35.

Jonas JB, Budde WM, Panda-Jonas S (1999) Ophthalmoscopic evaluation of the optic nerve head. Surv Ophthalmol. https://doi.org/10.1016/S0039-6257(98)00049-6

36.

Skuta GL (1992) Automated static perimetry. Am J Ophthalmol 114:110–111. https://doi.org/10.1016/s0002-9394(14)77431-8CrossRef

37.

Bendschneider D, Tornow RP, Horn FK et al (2010) Retinal nerve fiber layer thickness in normals measured by spectral domain oct. J Glaucoma 19. https://doi.org/10.1097/IJG.0b013e3181c4b0c7

38.

Kolar R, Tornow RP, Odstrcilik J, Liberdova I (2016) Registration of retinal sequences from new video-ophthalmoscopic camera. Biomed Eng Online 15:57. https://doi.org/10.1186/s12938-016-0191-0CrossRefPubMedPubMedCentral

39.

Odstrcilik J, Kolar R, Harabis V, Tornow RP (2015) Classification-based blood vessel segmentation in retinal images. In: Computational Vision and Medical Image Processing V. CRC Press, pp 95–100

40.

Lévêque P-MM, Zéboulon P, Brasnu E et al (2016) Optic disc vascularization in glaucoma: value of spectral-domain optical coherence tomography angiography. J Ophthalmol 2016:1–9. https://doi.org/10.1155/2016/6956717CrossRef

41.

Van Melkebeke L, Barbosa-Breda J, Huygens M, Stalmans I (2018) Optical coherence tomography angiography in glaucoma: a review. Ophthalmic Res. https://doi.org/10.1159/000488495

42.

Takeyama A, Ishida K, Anraku A et al (2018) Comparison of optical coherence tomography angiography and laser speckle flowgraphy for the diagnosis of normal-tension glaucoma. J Ophthalmol 2018:1–9. https://doi.org/10.1155/2018/1751857CrossRef

43.

Lawrence C, Schlegel WA (1966) Ophthalmic pulse studies. I. Influence of intraocular pressure. Investig Ophthalmol 5:515–525

44.

Michelson G, Patzelt A, Harazny J (2002) Flickering light increases retinal blood flow. In: Retina, 2002/06/11. pp 336–343

45.

Crittin M, Riva CE (2004) Functional imaging of the human papilla and peripapillary region based on flicker-induced reflectance changes. Neurosci Lett 360:141–144. https://doi.org/10.1016/j.neulet.2004.02.063CrossRefPubMed

46.

Best M, Plechaty G, Harris L, Galin MA (1971) Ophthalmodynamometry and ocular pulse studies in carotid occlusion. Arch Ophthalmol 85:334–338CrossRefPubMed

47.

Perkins ES (1985) The ocular pulse and intraocular pressure as a screening test for carotid artery stenosis. Br J Ophthalmol 69:676–680CrossRefPubMedPubMedCentral

48.

Kinsner W, Yan Y (1990) A model of the carotid vascular system with stenosis at the carotid bifurcation. Math Comput Model 14:582–585. https://doi.org/10.1016/0895-7177(90)90249-MCrossRef

49.

Rina M, Shiba T, Takahashi M et al (2015) Pulse waveform analysis of optic nerve head circulation for predicting carotid atherosclerotic changes. Graefes Arch Clin Exp Ophthalmol. https://doi.org/10.1007/s00417-015-3123-y

50.

Knecht PB, Menghini M, Bachmann LM et al (2012) The ocular pulse amplitude as a noninvasive parameter for carotid artery stenosis screening: a test accuracy study. Ophthalmology 119:1244–1249. https://doi.org/10.1016/j.ophtha.2011.12.040CrossRefPubMed

51.

Pinto LA, Vandewalle E, de Clerck E et al (2012) Ophthalmic artery Doppler waveform changes associated with increased damage in glaucoma patients. Investig Ophthalmol Vis Sci 53:2448–2453. https://doi.org/10.1167/iovs.11-9388CrossRef

52.

Millasseau SC, Guigui FG, Kelly RP et al (2000) Noninvasive assessment of the digital volume pulse. Comparison with the peripheral pressure pulse. Hypertens (Dallas, Tex 1979) 36:952–956. https://doi.org/10.1161/01.hyp.36.6.952CrossRef

53.

Levine RA, Demirel S, Fan J et al (2006) Asymmetries and visual field summaries as predictors of glaucoma in the ocular hypertension treatment study. Invest Ophthalmol Vis Sci 47:3896–3903. https://doi.org/10.1167/iovs.05-0469CrossRefPubMed

54.

Sullivan-Mee M, Ruegg CC, Pensyl D et al (2013) Diagnostic precision of retinal nerve fiber layer and macular thickness asymmetry parameters for identifying early primary open-angle glaucoma. Am J Ophthalmol 156:567–577.e1. https://doi.org/10.1016/j.ajo.2013.04.037CrossRefPubMed

55.

Hou H, Moghimi S, Zangwill LM et al (2018) Inter-eye asymmetry of optical coherence tomography angiography vessel density in bilateral glaucoma, glaucoma suspect, and healthy eyes. Am J Ophthalmol 190:69–77. https://doi.org/10.1016/j.ajo.2018.03.026CrossRefPubMedPubMedCentral

Title: Imaging video plethysmography shows reduced signal amplitude in glaucoma patients in the area of the microvascular tissue of the optic nerve head
Authors: Ralf-Peter Tornow
Radim Kolar
Jan Odstrcilik
Ivana Labounkova
Folkert Horn
Publication date: 01-02-2021
Publisher: Springer Berlin Heidelberg
Keyword: Glaucoma
Published in: Graefe's Archive for Clinical and Experimental Ophthalmology / Issue 2/2021
Print ISSN: 0721-832X
Electronic ISSN: 1435-702X
DOI: https://doi.org/10.1007/s00417-020-04934-y

Keynote webinar | Spotlight on sleep in brain health

Springer Medicine

Imaging video plethysmography shows reduced signal amplitude in glaucoma patients in the area of the microvascular tissue of the optic nerve head

Abstract

Purpose

Patients and methods

Results

Conclusions

Keynote webinar | Spotlight on sleep in brain health

Springer Medicine

Abstract

Purpose

Patients and methods

Results

Conclusions

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