Disc Hemorrhages Are Associated With Localized Three-Dimensional Neuroretinal Rim Thickness Progression in Open-Angle Glaucoma

Milica A. Margeta; Kitiya Ratanawongphaibul; Edem Tsikata; Michele Zemplenyi; Courtney L. Ondeck; Janice Kim; Anne L. Coleman; Fei Yu; Johannes F. de Boer; Teresa C. Chen

doi:10.1016/j.ajo.2021.06.021

Disc Hemorrhages Are Associated With Localized Three-Dimensional Neuroretinal Rim Thickness Progression in Open-Angle Glaucoma

Milica A. Margeta, Kitiya Ratanawongphaibul, Edem Tsikata, Michele Zemplenyi, Courtney L. Ondeck, Janice Kim, Anne L. Coleman, Fei Yu, Johannes F. de Boer, Teresa C. Chen^*

^*Corresponding author for this work

Research output: Contribution to Journal › Article › Academic › peer-review

Abstract

Purpose: To evaluate the relationship between the occurrence of optic disc hemorrhages (DH) and glaucoma progression as determined by multiple glaucoma testing modalities. Design: Prospective cohort study. Methods: A longitudinal study was undertaken of 124 open-angle glaucoma patients who had yearly disc photography, visual fields (VFs), spectral-domain optical coherence tomography (SD-OCT), retinal nerve fiber layer (RNFL) thickness scans, and optic nerve volume scans (Spectralis), all performed on the same day over a 5-year period. The minimum distance band (MDB) thickness, a 3-dimensional (3D) neuroretinal rim parameter, was calculated from optic nerve volume scans. Patients were classified as glaucoma progressors or glaucoma nonprogressors using event-based analysis. Results: Of 124 open-angle glaucoma patients, 19 (15.3%) had 1 or more DHs on yearly disc photographs. Presence of a DH was associated with localized 3D neuroretinal rim thickness progression (superior MDB progression; odds ratio: 3.96; P = .04) but not with global or inferior MDB progression (P = .14 and .81, respectively), DP progression (P = .08), VF progression (P = .45), or RNFL global, inferior, or superior progression (P = .17, 26, and .76, respectively). In the majority of patients with MDB progression (14/17 or 82%), the progression was noted before or concurrently with the first instance of DH. Conclusions: Glaucoma progression detected by high-density 3D SD-OCT neuroretinal rim measurements preceded DH occurrence in the majority of patients. These findings support the hypothesis that DHs are indicators of ongoing glaucoma progression rather than discrete events that cause subsequent progression.

Original language	English
Pages (from-to)	188-198
Number of pages	11
Journal	American Journal of Ophthalmology
Volume	234
Early online date	29 Jun 2021
DOIs	https://doi.org/10.1016/j.ajo.2021.06.021
Publication status	Published - Feb 2022

Bibliographical note

Funding Information:
Funding/Support: Teresa C. Chen is supported by a Harvard Catalyst National Institutes of Health award UL1 RR 025758, the Massachusetts Lions Eye Research Fund, an American Glaucoma Society Mid-Career Award, the Fidelity Charitable Fund, Department of Defense Small Business Innovation Research award DHP15-016. Milica A Margeta is supported by NIH/National Eye Instituted grants K12 EY016335 and K08 EY030160, American Glaucoma Society Young Clinician Scientist Award, and Research to Prevent Blindness Career Development Award.

Funding Information:
Funding/Support: Teresa C. Chen is supported by a Harvard Catalyst National Institutes of Health award UL1 RR 025758, the Massachusetts Lions Eye Research Fund, an American Glaucoma Society Mid-Career Award, the Fidelity Charitable Fund, Department of Defense Small Business Innovation Research award DHP15-016. Milica A Margeta is supported by NIH/National Eye Instituted grants K12 EY016335 and K08 EY030160, American Glaucoma Society Young Clinician Scientist Award, and Research to Prevent Blindness Career Development Award. Financial Disclosure: Johannes F. de Boer is the chair of the Scientific Advisory Board of the Center for Biomedical Optical Coherence Tomography Research and Translation (Harvard Medical School), and licenses to NIDEK Inc, Terumo Corp, Ninepoint Medical, and Heidelberg Engineering outside the submitted work. All other authors have reported that they have no relationships relevant to the contents of this paper to disclose.

Publisher Copyright:
© 2021 The Author(s)

Funding

Funding/Support: Teresa C. Chen is supported by a Harvard Catalyst National Institutes of Health award UL1 RR 025758, the Massachusetts Lions Eye Research Fund, an American Glaucoma Society Mid-Career Award, the Fidelity Charitable Fund, Department of Defense Small Business Innovation Research award DHP15-016. Milica A Margeta is supported by NIH/National Eye Instituted grants K12 EY016335 and K08 EY030160, American Glaucoma Society Young Clinician Scientist Award, and Research to Prevent Blindness Career Development Award. Funding/Support: Teresa C. Chen is supported by a Harvard Catalyst National Institutes of Health award UL1 RR 025758, the Massachusetts Lions Eye Research Fund, an American Glaucoma Society Mid-Career Award, the Fidelity Charitable Fund, Department of Defense Small Business Innovation Research award DHP15-016. Milica A Margeta is supported by NIH/National Eye Instituted grants K12 EY016335 and K08 EY030160, American Glaucoma Society Young Clinician Scientist Award, and Research to Prevent Blindness Career Development Award. Financial Disclosure: Johannes F. de Boer is the chair of the Scientific Advisory Board of the Center for Biomedical Optical Coherence Tomography Research and Translation (Harvard Medical School), and licenses to NIDEK Inc, Terumo Corp, Ninepoint Medical, and Heidelberg Engineering outside the submitted work. All other authors have reported that they have no relationships relevant to the contents of this paper to disclose.

Funders	Funder number
Fidelity Charitable Fund	DHP15-016
Harvard Catalyst National Institutes of Health	UL1 RR 025758
National Institutes of Health
National Eye Institute	K08 EY030160, K12 EY016335
National Eye Institute
Research to Prevent Blindness
Harvard Medical School
Massachusetts Lions Eye Research Fund
American Glaucoma Society

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Margeta, M. A., Ratanawongphaibul, K., Tsikata, E., Zemplenyi, M., Ondeck, C. L., Kim, J., Coleman, A. L., Yu, F., de Boer, J. F., & Chen, T. C. (2022). Disc Hemorrhages Are Associated With Localized Three-Dimensional Neuroretinal Rim Thickness Progression in Open-Angle Glaucoma. American Journal of Ophthalmology, 234, 188-198. https://doi.org/10.1016/j.ajo.2021.06.021

@article{4762d4747d1248a0a74199a933d82901,

title = "Disc Hemorrhages Are Associated With Localized Three-Dimensional Neuroretinal Rim Thickness Progression in Open-Angle Glaucoma",

abstract = "Purpose: To evaluate the relationship between the occurrence of optic disc hemorrhages (DH) and glaucoma progression as determined by multiple glaucoma testing modalities. Design: Prospective cohort study. Methods: A longitudinal study was undertaken of 124 open-angle glaucoma patients who had yearly disc photography, visual fields (VFs), spectral-domain optical coherence tomography (SD-OCT), retinal nerve fiber layer (RNFL) thickness scans, and optic nerve volume scans (Spectralis), all performed on the same day over a 5-year period. The minimum distance band (MDB) thickness, a 3-dimensional (3D) neuroretinal rim parameter, was calculated from optic nerve volume scans. Patients were classified as glaucoma progressors or glaucoma nonprogressors using event-based analysis. Results: Of 124 open-angle glaucoma patients, 19 (15.3%) had 1 or more DHs on yearly disc photographs. Presence of a DH was associated with localized 3D neuroretinal rim thickness progression (superior MDB progression; odds ratio: 3.96; P = .04) but not with global or inferior MDB progression (P = .14 and .81, respectively), DP progression (P = .08), VF progression (P = .45), or RNFL global, inferior, or superior progression (P = .17, 26, and .76, respectively). In the majority of patients with MDB progression (14/17 or 82%), the progression was noted before or concurrently with the first instance of DH. Conclusions: Glaucoma progression detected by high-density 3D SD-OCT neuroretinal rim measurements preceded DH occurrence in the majority of patients. These findings support the hypothesis that DHs are indicators of ongoing glaucoma progression rather than discrete events that cause subsequent progression.",

author = "Margeta, {Milica A.} and Kitiya Ratanawongphaibul and Edem Tsikata and Michele Zemplenyi and Ondeck, {Courtney L.} and Janice Kim and Coleman, {Anne L.} and Fei Yu and {de Boer}, {Johannes F.} and Chen, {Teresa C.}",

note = "Funding Information: Funding/Support: Teresa C. Chen is supported by a Harvard Catalyst National Institutes of Health award UL1 RR 025758, the Massachusetts Lions Eye Research Fund, an American Glaucoma Society Mid-Career Award, the Fidelity Charitable Fund, Department of Defense Small Business Innovation Research award DHP15-016. Milica A Margeta is supported by NIH/National Eye Instituted grants K12 EY016335 and K08 EY030160, American Glaucoma Society Young Clinician Scientist Award, and Research to Prevent Blindness Career Development Award. Funding Information: Funding/Support: Teresa C. Chen is supported by a Harvard Catalyst National Institutes of Health award UL1 RR 025758, the Massachusetts Lions Eye Research Fund, an American Glaucoma Society Mid-Career Award, the Fidelity Charitable Fund, Department of Defense Small Business Innovation Research award DHP15-016. Milica A Margeta is supported by NIH/National Eye Instituted grants K12 EY016335 and K08 EY030160, American Glaucoma Society Young Clinician Scientist Award, and Research to Prevent Blindness Career Development Award. Financial Disclosure: Johannes F. de Boer is the chair of the Scientific Advisory Board of the Center for Biomedical Optical Coherence Tomography Research and Translation (Harvard Medical School), and licenses to NIDEK Inc, Terumo Corp, Ninepoint Medical, and Heidelberg Engineering outside the submitted work. All other authors have reported that they have no relationships relevant to the contents of this paper to disclose. Publisher Copyright: {\textcopyright} 2021 The Author(s)",

year = "2022",

month = feb,

doi = "10.1016/j.ajo.2021.06.021",

language = "English",

volume = "234",

pages = "188--198",

journal = "American Journal of Ophthalmology",

issn = "0002-9394",

publisher = "Elsevier USA",

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TY - JOUR

T1 - Disc Hemorrhages Are Associated With Localized Three-Dimensional Neuroretinal Rim Thickness Progression in Open-Angle Glaucoma

AU - Margeta, Milica A.

AU - Ratanawongphaibul, Kitiya

AU - Tsikata, Edem

AU - Zemplenyi, Michele

AU - Ondeck, Courtney L.

AU - Kim, Janice

AU - Coleman, Anne L.

AU - Yu, Fei

AU - de Boer, Johannes F.

AU - Chen, Teresa C.

N1 - Funding Information: Funding/Support: Teresa C. Chen is supported by a Harvard Catalyst National Institutes of Health award UL1 RR 025758, the Massachusetts Lions Eye Research Fund, an American Glaucoma Society Mid-Career Award, the Fidelity Charitable Fund, Department of Defense Small Business Innovation Research award DHP15-016. Milica A Margeta is supported by NIH/National Eye Instituted grants K12 EY016335 and K08 EY030160, American Glaucoma Society Young Clinician Scientist Award, and Research to Prevent Blindness Career Development Award. Funding Information: Funding/Support: Teresa C. Chen is supported by a Harvard Catalyst National Institutes of Health award UL1 RR 025758, the Massachusetts Lions Eye Research Fund, an American Glaucoma Society Mid-Career Award, the Fidelity Charitable Fund, Department of Defense Small Business Innovation Research award DHP15-016. Milica A Margeta is supported by NIH/National Eye Instituted grants K12 EY016335 and K08 EY030160, American Glaucoma Society Young Clinician Scientist Award, and Research to Prevent Blindness Career Development Award. Financial Disclosure: Johannes F. de Boer is the chair of the Scientific Advisory Board of the Center for Biomedical Optical Coherence Tomography Research and Translation (Harvard Medical School), and licenses to NIDEK Inc, Terumo Corp, Ninepoint Medical, and Heidelberg Engineering outside the submitted work. All other authors have reported that they have no relationships relevant to the contents of this paper to disclose. Publisher Copyright: © 2021 The Author(s)

PY - 2022/2

Y1 - 2022/2

N2 - Purpose: To evaluate the relationship between the occurrence of optic disc hemorrhages (DH) and glaucoma progression as determined by multiple glaucoma testing modalities. Design: Prospective cohort study. Methods: A longitudinal study was undertaken of 124 open-angle glaucoma patients who had yearly disc photography, visual fields (VFs), spectral-domain optical coherence tomography (SD-OCT), retinal nerve fiber layer (RNFL) thickness scans, and optic nerve volume scans (Spectralis), all performed on the same day over a 5-year period. The minimum distance band (MDB) thickness, a 3-dimensional (3D) neuroretinal rim parameter, was calculated from optic nerve volume scans. Patients were classified as glaucoma progressors or glaucoma nonprogressors using event-based analysis. Results: Of 124 open-angle glaucoma patients, 19 (15.3%) had 1 or more DHs on yearly disc photographs. Presence of a DH was associated with localized 3D neuroretinal rim thickness progression (superior MDB progression; odds ratio: 3.96; P = .04) but not with global or inferior MDB progression (P = .14 and .81, respectively), DP progression (P = .08), VF progression (P = .45), or RNFL global, inferior, or superior progression (P = .17, 26, and .76, respectively). In the majority of patients with MDB progression (14/17 or 82%), the progression was noted before or concurrently with the first instance of DH. Conclusions: Glaucoma progression detected by high-density 3D SD-OCT neuroretinal rim measurements preceded DH occurrence in the majority of patients. These findings support the hypothesis that DHs are indicators of ongoing glaucoma progression rather than discrete events that cause subsequent progression.

AB - Purpose: To evaluate the relationship between the occurrence of optic disc hemorrhages (DH) and glaucoma progression as determined by multiple glaucoma testing modalities. Design: Prospective cohort study. Methods: A longitudinal study was undertaken of 124 open-angle glaucoma patients who had yearly disc photography, visual fields (VFs), spectral-domain optical coherence tomography (SD-OCT), retinal nerve fiber layer (RNFL) thickness scans, and optic nerve volume scans (Spectralis), all performed on the same day over a 5-year period. The minimum distance band (MDB) thickness, a 3-dimensional (3D) neuroretinal rim parameter, was calculated from optic nerve volume scans. Patients were classified as glaucoma progressors or glaucoma nonprogressors using event-based analysis. Results: Of 124 open-angle glaucoma patients, 19 (15.3%) had 1 or more DHs on yearly disc photographs. Presence of a DH was associated with localized 3D neuroretinal rim thickness progression (superior MDB progression; odds ratio: 3.96; P = .04) but not with global or inferior MDB progression (P = .14 and .81, respectively), DP progression (P = .08), VF progression (P = .45), or RNFL global, inferior, or superior progression (P = .17, 26, and .76, respectively). In the majority of patients with MDB progression (14/17 or 82%), the progression was noted before or concurrently with the first instance of DH. Conclusions: Glaucoma progression detected by high-density 3D SD-OCT neuroretinal rim measurements preceded DH occurrence in the majority of patients. These findings support the hypothesis that DHs are indicators of ongoing glaucoma progression rather than discrete events that cause subsequent progression.

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JF - American Journal of Ophthalmology

ER -

Disc Hemorrhages Are Associated With Localized Three-Dimensional Neuroretinal Rim Thickness Progression in Open-Angle Glaucoma

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