Assessment of the conjunctival microcirculation in adult patients with cyanotic congenital heart disease compared to healthy controls

Paul Brennan; Min Jing; Andrew McNeil; Agnes Awuah; Mailey Jonathan; Bronagh  Kelly; D Finlay; Kevin Blighe; James McLaughlin; M. Andrew Nesbit; Emanuele Trucco; Christopher  Lockhart; Tara C. B. Moore; Mark Spence

doi:10.1016/j.mvr.2021.104167

Assessment of the conjunctival microcirculation in adult patients with cyanotic congenital heart disease compared to healthy controls

Paul Brennan, Min Jing, Andrew McNeil, Agnes Awuah, Mailey Jonathan, Bronagh Kelly, D Finlay, Kevin Blighe, James McLaughlin, M. Andrew Nesbit, Emanuele Trucco, Christopher Lockhart, Tara C. B. Moore, Mark Spence

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Abstract

Purpose: Congenital heart disease (CHD) is the most common live birth defect and a proportion of these patients have chronic hypoxia. Chronic hypoxia leads to secondary erythrocytosis resulting in microvascular dysfunction and increased thrombosis risk. The conjunctival microcirculation is easily accessible for imaging and quantitative assessment. It has not previously been studied in adult CHD patients with cyanosis (CCHD).
Methods: We assessed the conjunctival microcirculation and compared CCHD patients and matched healthy controls to determine if there were differences in measured microcirculatory parameters. We acquired images using an iPhone 6s and slit-lamp biomicroscope. Parameters measured included diameter, axial velocity, wall shear rate and blood volume flow. The axial velocity was estimated by applying the 1D+T continuous wavelet transform (CWT). Results are for all vessels as they were not sub-classified into arterioles or venules.
Results: 11 CCHD patients and 14 healthy controls were recruited to the study. CCHD patients were markedly more hypoxic compared to the healthy controls (84% vs 98%, p= 0.001). A total of 736 vessels (292 vs 444) were suitable for analysis. Mean microvessel diameter (D) did not significantly differ between the CCHD patients and controls (20.4 ±2.7μm vs 20.2 ±2.6μm, p=0.86). Axial velocity (Va) was lower in the CCHD patients (0.47 ±0.06mm/s vs 0.53 ±0.05mm/s, p=0.03). Blood volume flow (Q) was lower for CCHD patients (121 ±30pl/s vs 145 ±50pl/s, p=0.65) with the greatest differences observed in vessels >22μm diameter (216 ±121pl/s vs 258 ±154pl/s, p=0.001). Wall shear rate (WSR) was significantly lower for the CCHD group (153 ±27s^-1 vs 174 ±22s^-1, p=0.04).
Conclusions: This iPhone and slit-lamp combination assessment of conjunctival vessels found lower axial velocity, wall shear rate and in the largest vessel group, lower blood volume flow in chronically hypoxic patients with congenital heart disease. With further study this assessment method may have utility in the evaluation of patients with chronic hypoxia.

Original language	English
Article number	104167
Number of pages	9
Journal	Microvascular Research
Volume	136
Early online date	7 Apr 2021
DOIs	https://doi.org/10.1016/j.mvr.2021.104167
Publication status	Published (in print/issue) - 31 Jul 2021

Bibliographical note

Funding Information:
This project was funded by the Heart Trust fund, Royal Victoria Hospital , Belfast; the Regional Medical Cardiology Centre (RMCC), Royal Victoria Hospital , Belfast; Northern Ireland Chest Heart and Stroke (NICHS) and the Ulster University located in Northern Ireland, United Kingdom. The work for image processing and microcirculatory parameters estimation was part-funded by Interreg SEUPB funding associated with Eastern Corridor for Medical Engineering (ECME).

Funding Information:
This project was funded by the Heart Trust fund, Royal Victoria Hospital, Belfast; the Regional Medical Cardiology Centre (RMCC), Royal Victoria Hospital, Belfast; Northern Ireland Chest Heart and Stroke (NICHS) and the Ulster University located in Northern Ireland, United Kingdom. The work for image processing and microcirculatory parameters estimation was part-funded by Interreg SEUPB funding associated with Eastern Corridor for Medical Engineering (ECME).

Publisher Copyright:
© 2021 Elsevier Inc.

Copyright:
Copyright 2021 Elsevier B.V., All rights reserved.

Keywords

Conjunctival microcirculation
Cyanotic congenital heart disease
Axial velocity estimation
Microvascular physiology
1D + T continuous wavelet transform (CWT)

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10.1016/j.mvr.2021.104167

Microvascular_Rearch_R3_2021Author Accepted Manuscript, 0.98 MBLicence: CC BY-NC-ND

Cite this

Brennan, P., Jing, M., McNeil, A., Awuah, A., Jonathan, M., Kelly, B., Finlay, D., Blighe, K., McLaughlin, J., Nesbit, M. A., Trucco, E., Lockhart, C., Moore, T. C. B., & Spence, M. (2021). Assessment of the conjunctival microcirculation in adult patients with cyanotic congenital heart disease compared to healthy controls. Microvascular Research, 136, Article 104167. https://doi.org/10.1016/j.mvr.2021.104167

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title = "Assessment of the conjunctival microcirculation in adult patients with cyanotic congenital heart disease compared to healthy controls",

abstract = "Purpose: Congenital heart disease (CHD) is the most common live birth defect and a proportion of these patients have chronic hypoxia. Chronic hypoxia leads to secondary erythrocytosis resulting in microvascular dysfunction and increased thrombosis risk. The conjunctival microcirculation is easily accessible for imaging and quantitative assessment. It has not previously been studied in adult CHD patients with cyanosis (CCHD). Methods: We assessed the conjunctival microcirculation and compared CCHD patients and matched healthy controls to determine if there were differences in measured microcirculatory parameters. We acquired images using an iPhone 6s and slit-lamp biomicroscope. Parameters measured included diameter, axial velocity, wall shear rate and blood volume flow. The axial velocity was estimated by applying the 1D+T continuous wavelet transform (CWT). Results are for all vessels as they were not sub-classified into arterioles or venules. Results: 11 CCHD patients and 14 healthy controls were recruited to the study. CCHD patients were markedly more hypoxic compared to the healthy controls (84% vs 98%, p= 0.001). A total of 736 vessels (292 vs 444) were suitable for analysis. Mean microvessel diameter (D) did not significantly differ between the CCHD patients and controls (20.4 ±2.7μm vs 20.2 ±2.6μm, p=0.86). Axial velocity (Va) was lower in the CCHD patients (0.47 ±0.06mm/s vs 0.53 ±0.05mm/s, p=0.03). Blood volume flow (Q) was lower for CCHD patients (121 ±30pl/s vs 145 ±50pl/s, p=0.65) with the greatest differences observed in vessels >22μm diameter (216 ±121pl/s vs 258 ±154pl/s, p=0.001). Wall shear rate (WSR) was significantly lower for the CCHD group (153 ±27s-1 vs 174 ±22s-1, p=0.04). Conclusions: This iPhone and slit-lamp combination assessment of conjunctival vessels found lower axial velocity, wall shear rate and in the largest vessel group, lower blood volume flow in chronically hypoxic patients with congenital heart disease. With further study this assessment method may have utility in the evaluation of patients with chronic hypoxia.",

keywords = "Conjunctival microcirculation, Cyanotic congenital heart disease, Axial velocity estimation, Microvascular physiology, 1D + T continuous wavelet transform (CWT)",

author = "Paul Brennan and Min Jing and Andrew McNeil and Agnes Awuah and Mailey Jonathan and Bronagh Kelly and D Finlay and Kevin Blighe and James McLaughlin and Nesbit, {M. Andrew} and Emanuele Trucco and Christopher Lockhart and Moore, {Tara C. B.} and Mark Spence",

note = "Funding Information: This project was funded by the Heart Trust fund, Royal Victoria Hospital , Belfast; the Regional Medical Cardiology Centre (RMCC), Royal Victoria Hospital , Belfast; Northern Ireland Chest Heart and Stroke (NICHS) and the Ulster University located in Northern Ireland, United Kingdom. The work for image processing and microcirculatory parameters estimation was part-funded by Interreg SEUPB funding associated with Eastern Corridor for Medical Engineering (ECME). Funding Information: This project was funded by the Heart Trust fund, Royal Victoria Hospital, Belfast; the Regional Medical Cardiology Centre (RMCC), Royal Victoria Hospital, Belfast; Northern Ireland Chest Heart and Stroke (NICHS) and the Ulster University located in Northern Ireland, United Kingdom. The work for image processing and microcirculatory parameters estimation was part-funded by Interreg SEUPB funding associated with Eastern Corridor for Medical Engineering (ECME). Publisher Copyright: {\textcopyright} 2021 Elsevier Inc. Copyright: Copyright 2021 Elsevier B.V., All rights reserved.",

year = "2021",

month = jul,

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doi = "10.1016/j.mvr.2021.104167",

language = "English",

volume = "136",

journal = "Microvascular Research",

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Brennan, P, Jing, M, McNeil, A, Awuah, A, Jonathan, M, Kelly, B, Finlay, D, Blighe, K, McLaughlin, J , Nesbit, MA, Trucco, E, Lockhart, C, Moore, TCB & Spence, M 2021, 'Assessment of the conjunctival microcirculation in adult patients with cyanotic congenital heart disease compared to healthy controls', Microvascular Research, vol. 136, 104167. https://doi.org/10.1016/j.mvr.2021.104167

TY - JOUR

T1 - Assessment of the conjunctival microcirculation in adult patients with cyanotic congenital heart disease compared to healthy controls

AU - Brennan, Paul

AU - Jing, Min

AU - McNeil, Andrew

AU - Awuah, Agnes

AU - Jonathan, Mailey

AU - Kelly, Bronagh

AU - Finlay, D

AU - Blighe, Kevin

AU - McLaughlin, James

AU - Nesbit, M. Andrew

AU - Trucco, Emanuele

AU - Lockhart, Christopher

AU - Moore, Tara C. B.

AU - Spence, Mark

N1 - Funding Information: This project was funded by the Heart Trust fund, Royal Victoria Hospital , Belfast; the Regional Medical Cardiology Centre (RMCC), Royal Victoria Hospital , Belfast; Northern Ireland Chest Heart and Stroke (NICHS) and the Ulster University located in Northern Ireland, United Kingdom. The work for image processing and microcirculatory parameters estimation was part-funded by Interreg SEUPB funding associated with Eastern Corridor for Medical Engineering (ECME). Funding Information: This project was funded by the Heart Trust fund, Royal Victoria Hospital, Belfast; the Regional Medical Cardiology Centre (RMCC), Royal Victoria Hospital, Belfast; Northern Ireland Chest Heart and Stroke (NICHS) and the Ulster University located in Northern Ireland, United Kingdom. The work for image processing and microcirculatory parameters estimation was part-funded by Interreg SEUPB funding associated with Eastern Corridor for Medical Engineering (ECME). Publisher Copyright: © 2021 Elsevier Inc. Copyright: Copyright 2021 Elsevier B.V., All rights reserved.

PY - 2021/7/31

Y1 - 2021/7/31

N2 - Purpose: Congenital heart disease (CHD) is the most common live birth defect and a proportion of these patients have chronic hypoxia. Chronic hypoxia leads to secondary erythrocytosis resulting in microvascular dysfunction and increased thrombosis risk. The conjunctival microcirculation is easily accessible for imaging and quantitative assessment. It has not previously been studied in adult CHD patients with cyanosis (CCHD). Methods: We assessed the conjunctival microcirculation and compared CCHD patients and matched healthy controls to determine if there were differences in measured microcirculatory parameters. We acquired images using an iPhone 6s and slit-lamp biomicroscope. Parameters measured included diameter, axial velocity, wall shear rate and blood volume flow. The axial velocity was estimated by applying the 1D+T continuous wavelet transform (CWT). Results are for all vessels as they were not sub-classified into arterioles or venules. Results: 11 CCHD patients and 14 healthy controls were recruited to the study. CCHD patients were markedly more hypoxic compared to the healthy controls (84% vs 98%, p= 0.001). A total of 736 vessels (292 vs 444) were suitable for analysis. Mean microvessel diameter (D) did not significantly differ between the CCHD patients and controls (20.4 ±2.7μm vs 20.2 ±2.6μm, p=0.86). Axial velocity (Va) was lower in the CCHD patients (0.47 ±0.06mm/s vs 0.53 ±0.05mm/s, p=0.03). Blood volume flow (Q) was lower for CCHD patients (121 ±30pl/s vs 145 ±50pl/s, p=0.65) with the greatest differences observed in vessels >22μm diameter (216 ±121pl/s vs 258 ±154pl/s, p=0.001). Wall shear rate (WSR) was significantly lower for the CCHD group (153 ±27s-1 vs 174 ±22s-1, p=0.04). Conclusions: This iPhone and slit-lamp combination assessment of conjunctival vessels found lower axial velocity, wall shear rate and in the largest vessel group, lower blood volume flow in chronically hypoxic patients with congenital heart disease. With further study this assessment method may have utility in the evaluation of patients with chronic hypoxia.

AB - Purpose: Congenital heart disease (CHD) is the most common live birth defect and a proportion of these patients have chronic hypoxia. Chronic hypoxia leads to secondary erythrocytosis resulting in microvascular dysfunction and increased thrombosis risk. The conjunctival microcirculation is easily accessible for imaging and quantitative assessment. It has not previously been studied in adult CHD patients with cyanosis (CCHD). Methods: We assessed the conjunctival microcirculation and compared CCHD patients and matched healthy controls to determine if there were differences in measured microcirculatory parameters. We acquired images using an iPhone 6s and slit-lamp biomicroscope. Parameters measured included diameter, axial velocity, wall shear rate and blood volume flow. The axial velocity was estimated by applying the 1D+T continuous wavelet transform (CWT). Results are for all vessels as they were not sub-classified into arterioles or venules. Results: 11 CCHD patients and 14 healthy controls were recruited to the study. CCHD patients were markedly more hypoxic compared to the healthy controls (84% vs 98%, p= 0.001). A total of 736 vessels (292 vs 444) were suitable for analysis. Mean microvessel diameter (D) did not significantly differ between the CCHD patients and controls (20.4 ±2.7μm vs 20.2 ±2.6μm, p=0.86). Axial velocity (Va) was lower in the CCHD patients (0.47 ±0.06mm/s vs 0.53 ±0.05mm/s, p=0.03). Blood volume flow (Q) was lower for CCHD patients (121 ±30pl/s vs 145 ±50pl/s, p=0.65) with the greatest differences observed in vessels >22μm diameter (216 ±121pl/s vs 258 ±154pl/s, p=0.001). Wall shear rate (WSR) was significantly lower for the CCHD group (153 ±27s-1 vs 174 ±22s-1, p=0.04). Conclusions: This iPhone and slit-lamp combination assessment of conjunctival vessels found lower axial velocity, wall shear rate and in the largest vessel group, lower blood volume flow in chronically hypoxic patients with congenital heart disease. With further study this assessment method may have utility in the evaluation of patients with chronic hypoxia.

KW - Conjunctival microcirculation

KW - Cyanotic congenital heart disease

KW - Axial velocity estimation

KW - Microvascular physiology

KW - 1D + T continuous wavelet transform (CWT)

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U2 - 10.1016/j.mvr.2021.104167

DO - 10.1016/j.mvr.2021.104167

M3 - Article

C2 - 33838207

SN - 0026-2862

VL - 136

JO - Microvascular Research

JF - Microvascular Research

M1 - 104167

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Assessment of the conjunctival microcirculation in adult patients with cyanotic congenital heart disease compared to healthy controls

Abstract

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