Changes in retinal vessel oxygen saturation using automated retinal oximetry in patients with significant carotid stenosis

doi:10.21203/rs.3.rs-4684944/v1

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Changes in retinal vessel oxygen saturation using automated retinal oximetry in patients with significant carotid stenosis

https://doi.org/10.21203/rs.3.rs-4684944/v1

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Purpose: To evaluate the dynamics of changes in retinal oximetry parameters in patients with haemodynamically significant carotid stenosis

Methods: In this case-control study we examined 74 eye artery pairs in 37 patients with significant carotid stenosis over 50 % using retinal oximetry. 14 eye artery pairs were excluded due to contraindications for oximetry or presenting carotid occlusion. From the remaining 60 eye artery pairs, 39 stenotic eye artery pairs were analyzed against the control group of 21 non-stenotic eye artery pairs.

Results-Primary analysis of the data showed a trend to increased arterial saturation, decreased venular saturation and increased venular diameter. in all groups. The AV difference, the most sensitive parameter, however was only statistically significant for the 80 % stenosis patients. For each group, the cutoff value for the AV difference was chosen for calculation of the odds ratio (OR) of stenosis. Highest OR was found in the 80 % (9.0, p=0.007) with the threshold value of AV difference 38.72 %.

Conclusion: The impact of carotid stenosis on retinal perfusion was confirmed with the highest predictive value for stenosis above 80 %. The relative decrease in the AV difference and normalisation of other parameters in stenoses over 90 % can be explained by collateral circulation via the external carotid artery. The relationship between the AV difference and degree of stenosis is non linear which points to the contribution of other mechanisms to reduced post-stenotic blood flow adaptation.

This case-control study was conducted between 2021 and 2023 as a clinical trial approved by the Ethics Committee of the university hospital Olomouc, registered under ClinicalTrials.gov, ID: NCT06085612 All patients participated in the study willingly, providing informed consent in accordance with the Declaration of Helsinki. All methods used were carried out in accordance with relevant guideelines and regulations.

Biological sciences/Neuroscience

Biological sciences/Neuroscience/Diseases of the nervous system

Biological sciences/Neuroscience/Neuro vascular interactions

Biological sciences/Neuroscience/Visual system

Health sciences/Neurology/Neurological disorders/Cerebrovascular disorders

Health sciences/Neurology/Neurological disorders/Neurovascular disorders

Ischaemic stroke

Carotid ultrasound

Retinal oximetry

Arteriovenous difference

What is known

Carotid stenosis over 50 % due to atherosclerotic processs is a significant cause of devastating ischaemic stroke.. Only 15 % of large ischaemic strokes are preceeded by small ischaemic event. Identifying high risk stenoses suitable for revascularisation treatment seems crucial. Retinal oximetry is a noninvasive diagnostic method capable of evaluating retinal oxygen metabolism changes in presence of various systaemic diseases. Its changes in carotid stenosis have been studied before, confirming the increased oxygen intake in stenotic basin.

What is new

Our study aimed to investigate further relationship between reduced blood flow and detectable changes in retina. However the results showed that the increased oxygen extraction isnt the only mechanism of action and depending on the severity of other systaemic diseases, the results measured via oximetry may change significantly. Further research is needed in this field to better evaluate the oxygen metabolism in retinal and brain tissue.

Ischaemic strokes are the second most frequent cause of death and long-term invalidity, worldwide (1) and according to one study 15% are due to atherosclerotic stenosis of the internal carotid artery by over 50%. (2)

Treatment of Carotid stenosis

Significant carotid stenosis can be reduced by carotid endarterectomy. This one-time procedure can diminish the risk of ischaemic stroke to the level of a healthy person depending on concomitant risk factors. Compared to atrial fibrillation or small vessel cerebral disease which usually require life-long treatment with medication, this single-step procedure is unique. (3)

Despite the complex pathogenesis of atherosclerosis, only 2 criteria have proven to be clinically significant in making the decision whether to undergo surgical treatment of stenosis -severity and prior clinical symptoms.

Stenosis under 50% does not represent significant stroke risk. Asymptomatic hemodynamically significant stenosis over 50% has a 1 -year relative risk of stroke of only 1.5 compared to individuals with no stenosis and the risk does not vary for stenosis of 50–70% and over 70%. (4)

The ratio however greatly increases when presented with clinical symptoms. Symptomatic stenosis is defined as a stenosis with ischaemic event (amaurosis fugax, transient ischaemic attack – TIA – or minor stroke) up to 6 months prior to stenosis detection

5 -year risk of stroke recurrence in these symptomatic stenoses varies from 10% to more than 50% depending on other factors such as plaque characteristics, patient’s age, type of symptoms and the time from the last symptomatic event. (5)

This means that the symptoms of the stenosis are the key variable in predicting stroke recurrence. However, classic symptoms – TIA, amaurosis fugax or minor stroke – are detectable in only 15% of cases. (6) 85% of strokes diagnosed present as the first ischaemic event ever which seems highly unlikely. So far, the only method capable of detecting clinically asymptomatic ischaemic strokes is MRI which is unsuitable as a screening method. (7) Detecting the clinically asymptomatic yet subclinically active stenoses is now recognised to be crucial for stroke prevention.

Automated retinal oximetry

Automated retinal oximetry allows for nonivansive evaluation of retinal blood vessel oxygen saturation and blood vessel diameter. These vessels are the terminal branches of the carotid basin. Retinal oximetry relies on the different absorption qualities of oxyhaemoglobin and deoxyhaemoglobin. While oxyhaemoglobin does not absorb wavelengths of 570 nanometers, deoxyhaemoglobin does. Both molecules absorb the wavelength 600nm. (8) The instrument takes two monochromatic pictures of the retina. From the measured values of absorbance, it can mathematically extrapolate the arterial and venous blood oxygen saturation and arteriovenous saturation difference. Based on these parameters we are able to estimate retinal oxygen consumption. These parameters can provide information about the altered blood flow in the stenotic basin. (9)

So far only one study has evaluated the changes in retinal oximetry in patients with significant carotid stenosis. (10) This study included 16 patients with stenosis over 50%. Decreased retinal arterial diameter, increased arterial oxygen saturation and arteriovenous difference was observed in the stenotic group compared to both healthy controls and the contralateral nonstenotic side in the same patient.

The blood flow changed significantly with increasing stenosis, with a huge difference in perfusion in stenosis 50% -69% and over 70% respectively 80%. It is reasonable to assume that the biggest changes will occur with greater degrees of stenoses.

Aims of this study

The aim of this study was to evaluate the impact of varying degrees of carotid stenosis on retinal oximetry parameters while eliminating other factors influencing the retinal perfusion such as systemic disease. In stenoses over 90%, we evaluated the impact of retrograde ophthalmic flow on retinal oximetry parameters (specifically their normalisation when retinal perfusion is supplied via ECA instead of ICA).

These parameters may provide more detailed information on the retinal and by extension, cerebral perfusion reserve and the risk of developing a major ischaemic event.

This case-control study was conducted between 2021 and 2023. Data from 37 patients with significant carotid stenosis over 50% were collected in the Neurology and Ophthalmology Departments of the hospital forming 74 eye artery pairs undergoing retinal oximetry evaluation. Front his pool 4 patients presented bilateral stenosis forming the stenotic group of 41 eye artery pairs in stenotic group and 33 eye artery pairs in non-stenotic group. 2 eye artery pairs from the stenotic group and 12 eye artery pairs from the non-stenotic group were excluded from the study due to contraindications of retinal oximetry as listed below. Stenotic group then consisted of 39 eye artery pairs. The 21 remaining non-stenotic eye artery pairs were used as a control group. In this way there were similar characteristics of the control group in terms of age, sex and cardiovascular comorbidity factors.

Sample characteristics are summarized in Table 1.

Table 1

– Baseline sample characteristics, 39 eye artery pairs in proband group, 21 eye artery pairs in control group, 14 eye artery pairs excluded due to contraindications for automated retinal oximetry. 2 in stenotic group, 12 in non-stenotic group
Number of patients	37
Mean age +/- SD	70.3+/-7,25
Females (%)	13 (33,3%)
Bilateral stenosis	4 (10,25%) (3 males)
Stenosis 50–69%	12 (30,1%)
Stenosis 70–79%	14 (35,9%)
Stenosis 80–89%	7 (17,9%)
Stenosis 90–99%	6 (15,4%)
Left sided stenosis	16 (41%)
Right sided stenosis	23 (59%)
Orthograde ophthalmic flow	34 (1 in group of 90% stenosis)
Retrograde ophthalmic flow	5 (1 in group of 80% stenosis, rest in 90% stenosis)

The patients selected were both inpatient and outpatient. These had known stenosis or on first examination due to clinical symptoms. Ultrasonographic investigation took place prior to the retinal oximetry examination in the Neurology Department Neurosonology Laboratory.

An extended ultrasonographic protocol was used to determine the severity of the stenosis according to the diagnostic criteria given in Grants Radiology Guidelines. (11) Multiple factors were used to assess the severity of the stenosis depending on patient anatomical differences, with the in-stenosis PSV and in-stenosis/post-stenosis PSV ratio as the key factor. Examination was carried out on the machine GE-Logiq-S8, linear probe 9L-D frequency 2–8 MHz, sector probe M5S-D, frequency 1,8 − 4,4 MHz.

The patients were referred to the Ophthalmology Department, where they underwent detailed ophthalmological examination including history of ophthalmologic diseases, physical examination, assessment of visual acuity, front segment on the slit lamp, optic coherent tomography with retinal nerve fibre layer measurement and automated retinal oximetry.

Examinations preceeding the retinal oximetry were used to exclude patients with diseases ineligible for oximetry. These included high-degree refractive error, advanced cataract, glaucoma and diabetic retinal changes like proliferative angiopathy and the exudative form of macular degeneration. Patients treated with anti-vascular endothelial growth factor drugs undergoing laser photocoagulation or pars plana vitrectomy had to be excluded as well. (12, 13)

The retinal oximetry examination took place in standard conditions in a dark room, eliminating visible light spectrum bias. A fundus photograph was taken at 50° width, centered on the temporal edge of the optic nerve. Flash intensity 50 Ws was used. At least 2 photographs of the same eye were taken. The higher quality photograph was later used for analysis.

The quality of the fundus photographs was evaluated automatically and only images with values exceeding 5 out of 10 were considered eligible.

The measuring area was marked by 2 concentric circles in 1.5 pupilar diameter (PD) and 3PD, focussed on the center of the optic nerve papilla. Segments of examined blood vessels longer than 100 pixels (approximatelly 0.9 mm) were selected for the oxygen saturation analysis. An automated analytic protocol was used to calculate the oxygen saturation. All eligible vessels in all measured quadrants were used but physiological crossing of blood vessels were excluded manually from the evaluation due to the risk of mixing of the absorbance spectrum of the two types of blood vessels.

An example of evaluated photographs is shown in Fig. 1

The machine type was Retinal Oximeter Oxymap T1 (Oxymap ehf. Reykjavik, Iceland) that is paired with the retinal camera TRC-50DX, (Topcon Corporation, Tokyo, Japan). For the analysis, an oxymap software (version 2.5.2; Oxymap Inc. Reykjavik, Iceland) was used. All investigated parameters included blood vessel oxygen saturation, differentiating arteries from veins. Blood vessel diameter was also noted.

The full details of the study protocol are described in Polidar et al. Biomed Pap Med Fac Univ Palacky Olomouc Czech Repub. 2024 (14)

STATISTICAL ANALYSIS

The data were processed using Mann Whitney U tests given the sample characteristics. The 4 patient groups with 50%, 70%, 80% and 90%. stenosis were analyzed separately and compared to non-stenotic groups and analysis of the AV differences. In each group the optimal cut-off value for the AV difference was chosen using linear logistic regression. This value was used to calculate the odds ratio of the stenosis grades and its sensitivity and specificity in associating with stenosis severity.

Stenotic group was compared to non-stenotic group in 4 subgroups of stenosese over 50%, 70%, 80% and 90% respectively.

The first group with stenosis over 50% included all 39 eye artery pairs. In 70% group there were 27 pairs, 80% 13 pairs and 90% 6 artery-eye pairs.

The AV difference was statistically significantly higher in the 80% stenosis vessels than the non-stenotic blood vessels (36.5% vs 39.0%; p-value 0.008)

It remained significant even in the control group formed of 47 eye artery pairs of any stenosis under 79% (35,9% vs 39,0%; p-value 0,028).

On the other hand, no statistically significant difference in any of the parameters of retinal oximetry was found for the threshold stenoses of 50%, 70% and 90%. There was a trend of increased AV difference, arterial saturation, decreased venular saturation and increased venular diameter in all stenotic subgroups compared to the control group.

Possible reasons are discussed below.

All groups showed significant difference in PSV and EDV values showing reliability of the ultrasonographic examination and stenosis evaluation.

A logistic regression analysis was used to test the reliability of the AV difference as the most sensitive parameter for predicting the odds ratio for the carotid stenosis in the same stenosis threshold groups.

For the stenosis of 50%, the cut-off value of AV difference of 38,96% was used with low sensitivity and medium specificity (44% vs. 85%). This value showed odds ratio of stenosis over 50% 4,379 (95% CI: 1,101–17,42; p = 0,036).

For the stenosis of 70%, a cut-off value for an AV difference of 38,9% was used, with sensitivity 48% and specificity 85%. Odds ratio for the 70% stenosis was 5,262; 95% CI: 1,246–22,23; p = 0,024.

For the stenosis of 80%, AV diff. was statistically significant, p-value 0.008. The cut-off value for the AV difference 38.712% was used with a sensitivity 69% and specificity 80%. Odds ratio for the 80% stenosis was 9,000; 95%CI: 1,801–44,96; p = 0,007

For the same severity threshold using the control group consisting of both non-stenotic and under 79% stenosis patients, the AV difference remained statistically significant with p-value 0.0028. 36.34% was chosen as a cutoff value with a sensitivity of 92% and specificity 52%. Odds ratio for the 80% stenosis with this broadened control group was 14.3; 1.713– 119; p = 0.014.

For the stenosis of 90%, no significant values were measured. The sample consisted of 6 patients in the stenotic group.

Results for each group are summarized in graphs 1–5 and Tables 2–6

Table 2

Analysis of measured values in stenosis over 50% vs. control group
	Control group (n = 21)			Stenosis over 50% (n = 39)			Mann-Whitney U test p-value
	Median	Min	Max	Median	Min	Max	Mann-Whitney U test p-value
ACI PSV	78,5	42	150	258	129	661	< 0,0001
ACI EDV	24	4	56	63	13	396	< 0,0001
A SatO2 (%)	97,7	90,7	102,4	97,7	91,6	103,2	0,968
V SatO2 (%)	62,4	52,2	75,1	61,3	41,3	70,8	0,239
A Diameter (approx. µm)	113,3	86,0	132,3	108,8	90,3	137,3	0,548
V diameter	160,5	119,7	204,3	160,8	112,0	191,7	0,866
A-V diff.	36,5	26,9	42,4	37,1	23,6	53,6	0,096

Table 3

Analysis of measured values in stenosis over 70% vs. control group
	Control group (n = 21)			Stenosis over 70% (n = 27)			Mann-Whitney U test p-value
	Median	Min	Max	Median	Min	Max	Mann-Whitney U test p-value
ACI PSV	78,5	42,0	150,0	285,0	200,0	661,0	< 0,0001
ACI EDV	24,0	4,0	56,0	80,0	32,0	396,0	< 0,0001
A SatO2 (%)	97,7	90,7	102,4	97,7	91,6	101,9	0,983
V SatO2 (%)	62,3	52,2	75,1	60,8	44,4	70,8	0,268
A Diameter (approx. µm)	113,3	86,0	132,3	109,0	90,3	137,3	0,628
V diameter	160,5	119,7	204,3	162,8	112,0	191,7	0,923
A-V diff.	36,5	26,9	42,4	38,9	23,6	53,6	0,098

Table 4

Analysis of measured values in stenosis over 80% vs. control group
	Control group (n = 21)			Stenosis over 80% (n = 13)			Mann-Whitney U test p-value
	Median	Min	Max	Median	Min	Max	Mann-Whitney U test p-value
ACI PSV	78,5	42	150	400	252	661	< 0,0001
ACI EDV	24	4	56	132	34	396	< 0,0001
A SatO2 (%)	97,7	90,7	102,4	97,7	94,0	101,4	0,713
V SatO2 (%)	62,4	52,2	75,1	57,6	52,6	68,2	0,113
A Diameter (approx. µm)	113,3	86,0	132,3	110,5	90,3	133,0	0,985
V diameter	160,5	119,7	204,3	168,3	130,0	191,7	0,699
A-V diff.	36,5	26,9	42,4	39,0	32,6	42,6	0,008

Table 5

Analysis of measured values in stenosis over 90% vs. control group
	Control group (n = 21)			Stenosis over 90% (n = 6)			Mann-Whitney U test p-value
	Median	Min	Max	Median	Min	Max	Mann-Whitney U test p-value
ACI PSV	78,5	42	150	509	265	661	< 0,0001
ACI EDV	24	4	56	188,5	132	396	< 0,0001
A SatO2 (%)	97,7	90,7	102,4	98,6	95,8	101,4	0,543
V SatO2 (%)	62,4	52,2	75,1	59,2	56,3	63,2	0,273
A Diameter (approx. µm)	113,3	86,0	132,3	113,0	105,0	133,0	0,447
V diameter	160,5	119,7	204,3	171,6	130,0	191,7	0,855
A-V diff.	36,5	26,9	42,4	38,9	36,8	41,9	0,051

Table 6

– Analysis of measured values in stenosis over 80% vs. control group of stenosis under 80% and nonstenotic vessels
	Control group under 80% (n = 47)			Stenosis over 80% (n = 13)			Mann-Whitney U test p-value
	Median	Min	Max	Median	Min	Max	Mann-Whitney U test p-value
ACI PSV	171,5	42	357	400	252	661	< 0,0001
ACI EDV	34	4	164	132	34	396	< 0,0001
A SatO2 (%)	97,7	90,7	103,2	97,7	94,0	101,4	0,499
V SatO2 (%)	62,6	41,3	75,1	57,6	52,6	68,2	0,143
A Diameter (approx. µm)	108,9	86,0	137,3	110,5	90,3	133,0	0,628
V diameter	159,1	112,0	204,3	168,3	130,0	191,7	0,337
A-V diff.	35,9	23,6	53,6	39,0	32,6	42,6	0,028

Our primary aim was fulfilled, confirming greater oxygen extraction as one of the mechanisms of compensating for reduced blood flow in significant carotid stenosis. The results however differ from publications such as Zhang et al, 2021. Possible reasons are adumbrated below.

The relationship between AV difference and severity of stenosis is not straightforward, due to other factors including arterial or venous saturation and vascular diameter. Further, in the ultrasound assessment of the stenosis itself, multiple variables are used with emphasis on peak systolic velocity as crucial. According to the Hagen-Poisseuille law, the blood flow velocity is exponentially dependent on the reduced diameter of the vessel, directly on the dynamic viscosity of the blood and indirectly on blood vessel resistance. These parameters may be very variable in real life patients. Due to the exponential relationship of blood flow velocity to blood vessel diameter, the sensitivity and specificity of this parameter increases greatly with the increasing severity of the stenosis.

Another factor lies in systemic conditions that may influence either blood flow or retinal oxygen metabolism. An example would be a patient with chronic heart failure and low cardiac output. Such a patient would have overall slower blood flow velocity than a healthy person. This is why we see varying blood flow patterns with the same degree of stenoses.

Then, there are number of diseases that impact the amount of oxygen in the blood such as chronic obstructive pulmonary disease (15) or the affinity of haemoglobin for oxygen as in diabetes mellitus ((16). Some neurological diseases too such as Alzheimer disease and multiple sclerosis may also influence the retinal oxygen demands altering the results of the oximetry (17, 18)

Even though we endeavoured to control for these factors by using the nonstenotic sides from the same patient pool, we cannot rule out these sources of variability.

Combining these two factors we can see why in lower degrees of stenosis, retinal oximetry might yield a wide spectrum of results.

One interesting observation is that when a collateral circulation is formed, the oximetry results seem to pseudonormalize. By analyzing the group of 90% stenosis we see that the oximetry parameters tend to normalize. This might be explained by a significant part of the collateral circulation in the retinal blood supply. 5 out of 6 patients retinal perfusion relied on the external carotid artery reversing the blood flow in the ophthalmic artery.

As mentioned, clinical warning signs such as minor stroke, amaurosis fugax and TIA preceed large ischaemic stroke in only 15% cases, meaning 85% of large strokes represent the first manifestation of the atherosclerotic process. Since a large stroke of this origin is preventable by a one-time procedure, increasing our knowledge of atherosclerotic mechanisms and the clinical consequences is crucial. Retinal oximetry might provide more information about the severity of the atherosclerotic process in an individual leading to better clinical evaluation and indications for revascularisation treatment.

CT – Computerised Tomography, TIA – transient ischaemic attack, ICA-internal carotid artery, ECA, external carotid artery, CCA – common carotid artery, OA-ophthalmic artery, MRI – magnetic resonance imaging, AV – arteriovenous, PSV – peak systolic velocity, EDV – end diastolic velocity

CONFLICT OF INTERESTS:

The authors declare that there are no conflicts of interest regarding publication of this article

Author Contribution

Petr Polidar – First author, responsible for study organisation and design, patient enrollment, ultrasonographic examination and manuscript organisationEmail: [email protected] Král – Corresponding author, responsible for patient enrollment, study design and organisation, data collection and ultrasonographic examination Email: [email protected] Pašková – Co-author, responsible for study organisation and design, patient enrollment and retinal oximetry evaluation Email: [email protected] Karhanová – Co-author, responsible for patient enrollment, study design and organisation, data collection and retinal oximetry evaluation Email: [email protected]áš Mudroch-Co-author, responsible for study organisation and design, patient enrollment and retinal oximetry evaluation Email: [email protected] Šín– Co-Author, responsible for patient enrollment, study design, data collection and retinal oximetry evaluationEmail: [email protected]áš Dorňák – Co-author, responsible for patient enrollment, study design and organisation, data collection Email: [email protected] Schreiberová – Co-author, responsible for patient enrollment, study design and organisation, data collection and retinal oximetry evaluation Email: [email protected] Divišová – Co-author, responsible for patient enrollment, study design and organisation, data collectionEmail [email protected]áš Veverka – Co-author, responsible for patient enrollment, study design and organisation, data collectionEmail [email protected] Franc – Co-author, responsible for patient enrollment, study design and organisation, data collectionEmail: [email protected] Šaňák – Co-author, responsible for patient enrollment, study design and organisation, data collectionEmail: [email protected]

Acknowledgement

Oulton Alexander – Department of neurosciences, Palacký University, Olomouc, Czech Republic Faculty of Medicine and Dentistry, Language proofreading Email: [email protected]

Data Availability

The data that support the findings of this study are available from the corresponding author, [Michal Král], upon reasonable request.For the purpose of article evaluation the dataset was uploaded as a supplementary material with submission

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Graphs 1 to 5 are available in the Supplementary Files section

No competing interests reported.

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Changes in retinal vessel oxygen saturation using automated retinal oximetry in patients with significant carotid stenosis

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Abstract

Figures

Key Message

INTRODUCTION

Treatment of Carotid stenosis

Automated retinal oximetry

Aims of this study

MATERIALS AND METHODS

STATISTICAL ANALYSIS

RESULTS

Results for each group are summarized in graphs 1–5 and Tables 2–6

DISCUSSION

Abbreviations

Declarations

CONFLICT OF INTERESTS:

Author Contribution

Acknowledgement

Data Availability

References

Graphs

Additional Declarations

Supplementary Files

Status:

Version 1