June 2015
Volume 56, Issue 6
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Multidisciplinary Ophthalmic Imaging  |   June 2015
Correlation Between Peripapillary Choroidal Thickness and Retinal Vessel Oxygen Saturation in Young Healthy Individuals and Glaucoma Patients
Author Affiliations & Notes
  • Karel Van Keer
    Department of Ophthalmology University Hospitals Leuven, Leuven, Belgium
  • Luís Abegão Pinto
    Department of Ophthalmology University Hospitals Leuven, Leuven, Belgium
    Department of Ophthalmology, Faculty of Medicine of Lisbon University, Lisbon, Portugal
    Visual Sciences Study Center, Faculty of Medicine of Lisbon University, Lisbon, Portugal
  • Koen Willekens
    Department of Ophthalmology University Hospitals Leuven, Leuven, Belgium
  • Ingeborg Stalmans
    Department of Ophthalmology University Hospitals Leuven, Leuven, Belgium
    Department of Ophthalmology Neurosciences, Laboratory of Ophthalmology, KU Leuven, Leuven, Belgium
  • Evelien Vandewalle
    Department of Ophthalmology University Hospitals Leuven, Leuven, Belgium
Investigative Ophthalmology & Visual Science June 2015, Vol.56, 3758-3762. doi:10.1167/iovs.14-16225
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      Karel Van Keer, Luís Abegão Pinto, Koen Willekens, Ingeborg Stalmans, Evelien Vandewalle; Correlation Between Peripapillary Choroidal Thickness and Retinal Vessel Oxygen Saturation in Young Healthy Individuals and Glaucoma Patients. Invest. Ophthalmol. Vis. Sci. 2015;56(6):3758-3762. doi: 10.1167/iovs.14-16225.

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      © ARVO (1962-2015); The Authors (2016-present)

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Abstract

Purpose.: To investigate the correlation between peripapillary choroidal thickness (CT) and retinal vessel oxygen saturation (SO2) in young healthy individuals and open-angle glaucoma (OAG) patients.

Methods.: Fifty-four young healthy volunteers (aged 21.6 ± 1.1 years) and 48 OAG patients (aged 72.0 ± 9.1 years, visual field mean deviation −9.0 ± 8.1 dB) were included. Peripapillary CT was obtained using enhanced depth imaging optical coherence tomography (EDI-OCT). Arterial (SaO2) and venous (SvO2) retinal oxygen saturation were measured by a spectrophotometric retinal oximeter.

Results.: Arterial and SvO2 retinal oxygen saturation were significantly higher in the glaucoma group (95.1 ± 3.3% vs. 92.3 ± 3.0% and 60.8 ± 6.3% vs. 55.4 ± 4.6%, P < 0.001, respectively), while arteriovenous oxygen difference was significantly lower (34.4 ± 6.0% vs. 36.8 ± 3.8%, P = 0.014). Arterial and SvO2 retinal oxygen saturation were positively correlated with peripapillary CT in the healthy group (Spearman's ρ = 0.48, P < 0.001 and ρ = 0.41, P = 0.002, respectively), but not in the glaucoma group (P > 0.05). Multivariate analysis confirmed that these findings were independent of age, intraocular pressure, and mean arterial blood pressure and revealed a negative correlation between arteriovenous oxygen difference and CT in the healthy group (β = −0.337, P = 0.03).

Conclusions.: In this study, we found a significant positive correlation between retinal vessel SO2 and peripapillary CT in young healthy individuals, but not in open-angle glaucoma patients. Further research is warranted to investigate whether the lack of correlation reflects a disturbance in the blood flow regulation in glaucoma patients. (ClinicalTrials.gov number, NCT01840202.)

Per unit tissue weight, the retina consumes more oxygen than any other mammalian tissue.1 Since blood is not transparent, the degree to which the retina can be supplied by overlying retinal vessels is functionally limited. To meet its extreme oxygen demand, the human retina is therefore largely dependent upon the underlying choroid.2 
Except for a common origin from the ophthalmic artery, the retinal and choroidal blood vessels do not show many similarities. The choroidal circulation, receiving 65% to 85% of the ocular blood flow, has the highest blood flow in the human body, more than 10-fold higher than that of the brain per unit tissue weight.3 This is reflected in an arteriovenous (AV) oxygen difference of only 3%, which is needed to maintain the steep concentration gradient necessary for oxygen to diffuse across the barriers of Bruch's membrane and the retinal pigment epithelium. The retinal circulation, on the other hand, accounts for a mere 5% of the ocular blood flow and has a AV oxygen difference of 30%.2 The regulation of blood flow of the retinal and choroidal circulation is also substantially different. In most human tissues, the regulation of blood flow is under dual control: central control by the autonomic nervous system, and local control in response to accumulation of vasoactive metabolites in the vicinity of blood vessels. This is not true for the retina. Proximal to the lamina cribrosa, the ophthalmic artery and its branches are richly innervated by the autonomic nervous system. From that point on, however, the retinal circulation is not innervated.4 This implies that the retinal vasculature is dependent only upon local autoregulation.5 In contrast, the choroidal vasculature is densely innervated but is separated too far from the retina to “sense” its metabolic needs through vasoactive substances.6,7 This means that the retina primarily relies upon adaptation of the retinal vasculature (autoregulation) in cases of increased metabolic demand or reduced ocular perfusion pressure. However, the adaptive capacity of the retinal circulation is not without limits.8,9 While disturbances of the retinal circulation, such as central or branch retinal artery occlusion, are often clinically evident on fundoscopy, alterations of choroidal blood flow are difficult to assess using conventional imaging techniques and therefore much less studied. 
The advent of enhanced depth imaging optical coherence tomography (EDI-OCT), a technique using spectral-domain optical coherence tomography allowing for a detailed noninvasive evaluation of the choroid in vivo, has sparked renewed interest in the role of the choroid in the pathogenesis of various ocular diseases.10 Using EDI-OCT, choroidal thickness (CT) has been shown to be abnormal in several ocular conditions, including age-related macular degeneration,11 high myopia,12 central serous chorioretinopathy,13 polypoidal choroidal vasculopathy,14 glaucoma,15 inherited retinal diseases,16 and Vogt-Koyanagi-Harada disease.17 In some of these diseases, an impaired retinal oxygenation is believed to be involved in the pathophysiological process.1821 In particular, in glaucoma, disturbances in ocular blood flow and vascular autoregulation are thought to be an important factor in the disease process. Several publications have revealed alterations in the retinal, choroidal, and retrobulbar circulation in glaucoma patients.2225 
Spectrophotometric retinal oximetry is an emerging imaging technique capable of providing reproducible in vivo, noninvasive measurements of the retinal vessel oxygen saturation (SO2) using dual-wavelength fundus photographs.26,27 Previous studies on retinal oximetry in glaucoma patients demonstrated an increased retinal venous oxygen saturation (SvO2) and a decreased AV oxygen difference in glaucomatous eyes with advanced visual field defects compared to those with milder or no defects.2830 
Our aim in this study was to assess and compare the correlation between peripapillary CT and retinal vessel SO2 in young healthy individuals and in glaucoma patients. 
Methods
Study Population
For the healthy group, individuals between 18 and 28 years of age were invited to participate in this cross-sectional study at the Department of Ophthalmology at the University of Leuven. On the basis of a questionnaire, subjects with a personal history of any ophthalmological disease or ophthalmic surgery or family history of ophthalmological diseases including choroidal/retinal dystrophies were excluded. Glaucoma patients were recruited from a larger study conducted at the glaucoma clinic of the University Hospitals Leuven (NCT01840202). The diagnosis of glaucoma was made by glaucoma specialists (IS, EV) and was defined as having characteristic glaucomatous optic disc changes and corresponding visual field defects. Individuals with a personal history of ocular trauma, intraocular surgery (except clear cornea cataract surgery or glaucoma surgery performed more than 6 month before visit), systemic diseases with possible direct ocular involvement (e.g., diabetes mellitus, thyroid dysfunction, hemoglobinopathies), neurological diseases, ametropia exceeding ±4 diopters, or use of direct vasodilators were not included. 
Prior to any investigation, all participants signed a written informed consent form in accordance with the tenets of the Declaration of Helsinki. The study was approved by the local ethics committee (Medical Ethical Board of the University Hospitals Leuven, Belgium). 
Sample size calculations were based on a presumed moderate correlation between CT and SO2 of at least 0.4.31 For a power of 0.8 with an α of 0.05 (two-sided), the required sample size was at least 47 subjects per group. We included over 120% of the calculated sample size to compensate for exclusion because of inadequate image quality.32 
Experimental Design
After consenting to participate in the study, all subjects underwent routine ophthalmic examination including slit-lamp biomicroscopy and Goldmann applanation tonometry, followed by CT measurements with a spectral-domain OCT (Cirrus HD-OCT, model 4000; Carl Zeiss Meditec, Dublin, CA, USA). In the glaucoma patients, the eye with the worse visual field damage was included; in the healthy individuals, one eye was randomly selected. The tomographic data from peripapillary centered high-definition (HD) 5-line raster scans were obtained using the EDI mode included in the Cirrus 6.5 software. Only scans with a minimum signal strength of 6 out of 10 and clear visualization of the choroid–scleral interface were retained for further analysis. Using the provided Cirrus HD-OCT analysis software, CT was measured as the perpendicular distance from the outer edge of the hyperreflective retinal pigment epithelium to the choroid–scleral interface (Fig. A). Mean CT was calculated as the average of measurements in the temporal, superior, nasal, and inferior direction at 500 μm from the optic disc margin. Systolic and diastolic blood pressures were measured using an automated sphygmomanometer on the upper arm (Omron HEM-7001-E; Omron, Kyoto, Japan). 
Figure
 
(A) Choroidal thickness measurements at 500 μm from the optic disc margin. (B) Arterial and venous oxygen saturation measurements in each quadrant on a pseudo-color image from the Oxymap oximeter (see text for details). SN, superonasal; ST, superotemporal; IT, inferotemporal; IN, inferonasal.
Figure
 
(A) Choroidal thickness measurements at 500 μm from the optic disc margin. (B) Arterial and venous oxygen saturation measurements in each quadrant on a pseudo-color image from the Oxymap oximeter (see text for details). SN, superonasal; ST, superotemporal; IT, inferotemporal; IN, inferonasal.
Pupils were dilated with phenylephrine 5% (Neosynephrine-POS; Ursapharm, Saarbrucken, Germany) and tropicamide 0.5% (Tropicol; Théa Pharma, Wetteren, Belgium). After 2 minutes of dark adaptation, retinal vessel SO2 levels were measured using the Oxymap T1 oximeter (Oxymap ehf., Reykjavik, Iceland) in the selected eye. This spectrophotometric retinal oximeter consists of an image splitter, bandpass filters, and two digital cameras (Insight IN1800; Diagnostic Instruments, Inc., Sterling Heights, MI, USA) attached to a conventional fundus camera (TRC-50DX; Topcon Co., Tokyo, Japan), enabling the simultaneous acquisition of monochromatic retinal images at two different wavelengths. While 570-nm light is absorbed equally by oxygenated and deoxygenated hemoglobin, 600-nm light is absorbed less by oxygenated hemoglobin. Based on this principle, the provided software is able to calculate the SO2 for each individual vessel. The principles of retinal oximetry are described in more detail elsewhere.33 To assess the quality of the retinal fundus photographs, we used criteria that our research group has published before.32 For each eye, the best-quality optic disc-centered fundus image was rated using four criteria: focus, contrast, glare, and shadow. A pass/fail system was used. Pictures that did not pass one of the four criteria were excluded. Image analysis was performed with the Oxymap Analyzer software version 2.4.0 using a standard protocol.29 First-degree retinal vessels with a width of more than 6 pixels and a length between 50 and 200 pixels were selected from the color-coded saturation map. Second-degree vessels were analyzed only if first-degree vessels did not meet the criteria. Around the optic disc, an area of 15 pixels as well as branching vessels and their origin was manually excluded. Arterial and venous SO2 were averaged over the four quadrants (Fig. B). 
Statistical Analysis
Demographics and measured parameters were analyzed with descriptive statistics (mean ± standard deviation). Differences between the healthy individuals and the OAG patients were compared by unpaired sample t-test. The relationship between retinal vessel SO2 parameters and CT was assessed using Spearman's rank correlation coefficients and multivariate linear regression analysis after adjusting for age, intraocular pressure, and mean arterial blood pressure. Statistical significance was based on two-sided P values of <0.05. All statistical analyses were performed using SPSS 20.0 for Mac (SPSS, Inc., Chicago, IL, USA). 
Results
Of the 121 subjects initially recruited (63 young healthy individuals, 58 open-angle glaucoma [OAG] patients, all Caucasian), 15 (12%, 7 in healthy group, 8 in OAG group) were rejected from further analysis because of inadequate quality of the oximetry images, and 4 additional cases (3%, 2 in each group) were omitted due to inability to clearly identify the choroid–scleral junction on OCT images. Thus, 54 healthy individuals and 48 OAG patients were included in the final analysis. The demographic and clinical characteristics of both groups are shown in Table 1
Table 1
 
Characteristics of the Study Population
Table 1
 
Characteristics of the Study Population
Average SaO2, SvO2, and AV difference were 92.3 ± 3.0%, 55.4 ± 4.6%, and 36.8 ± 3.8% in the healthy group and 95.1 ± 3.3%, 60.8 ± 6.3%, and 34.4 ± 6.0% in the OAG group (Table 2). Both SaO2 and SvO2 were significantly higher in the OAG group (P < 0.001). Choroidal thickness was significantly thinner in the OAG group (157.8 ± 47.0 μm vs. 106.9 ± 50.4 μm, P < 0.001). 
Table 2
 
Peripapillary Choroidal Thickness and Retinal Vessel Oxygen Saturation
Table 2
 
Peripapillary Choroidal Thickness and Retinal Vessel Oxygen Saturation
In the healthy individuals, a significant correlation was observed between both SaO2 and SvO2 and CT (Spearman's ρ = 0.48, P < 0.001 and ρ = 0.41, P = 0.002, respectively). In contrast, no significant association was observed in the OAG group. The observed correlations in the healthy group remained statistically significant after adjusting for age, intraocular pressure, and mean arterial blood pressure (β = 0.429, P = 0.003 for SaO2; β = 0.528, P < 0.001 for SvO2). While not significantly correlated in univariate analysis, AV difference showed a significant negative relationship with CT in multivariate analysis (β = −0.337, P = 0.03). The correlation coefficients are summarized in Table 3
Table 3
 
Retinal Vessel Oxygen Saturation and Correlation With Choroidal Thickness
Table 3
 
Retinal Vessel Oxygen Saturation and Correlation With Choroidal Thickness
Discussion
A mismatch between choroidal and retinal circulation may play an important role in numerous ocular diseases. To our knowledge, this is the first study to correlate CT with SO2. As a proof of concept, we compared this correlation between two very different populations: young healthy individuals and OAG patients. 
First, we observed a significant difference in SaO2, SvO2, and AV differences between the two groups. In accordance with previous studies on oximetry in glaucoma, we found a significantly higher SvO2 and a lower AV difference in the OAG patients.2830 The reduced AV difference in glaucomatous eyes is thought to reflect a decrease in oxygen consumption secondary to tissue atrophy.30 Whereas SaO2 did not differ significantly in the aforementioned studies, we also observed a significantly higher SaO2 in the OAG group. It should be emphasized that the two groups differ greatly in age (among other potential confounding factors, as described in more detail below). Current literature provides conflicting results regarding the influence of age on retinal oximetry levels.3335 However, most papers show a negative correlation between SvO2 and age, and none of them found a negative correlation of AV difference with age. The differences we observed are therefore less likely to be merely age related. We also found a significantly thinner CT in the OAG group. While the correlation between peripapillary CT and glaucoma is uncertain, there is large consensus in the literature regarding the effect of age on CT.15,36,37 The difference in CT we observed matches very closely the linear decrease in CT of 11 μm/decade described by Roberts et al.15 
Second, we found a significant positive correlation between peripapillary CT and retinal vessel SO2 in young healthy individuals but not in glaucoma patients. To explain these findings, one must note that the relative contribution of the retinal and the choroidal circulation to the retinal oxygen supply is not fixed, but rather a dynamic interplay.38 As mentioned before, the retina relies primarily upon autoregulation of the retinal vasculature in cases of increased metabolic demand or reduced ocular perfusion pressure. The choroidal blood vessels are highly innervated by the autonomic nervous system, but are separated too far from the retina to respond to the local accumulation of vasoactive metabolites. It could therefore be hypothesized that conditions interfering with either the autoregulation or the autonomic nervous regulation could render the retina at a higher risk of ischemic damage. Since glaucoma has been associated with disturbances in both types of regulation, we chose to compare the correlation between CT and SO2 in young healthy individuals and glaucoma patients.19,39 In the healthy group, we observed a positive correlation between CT and both arterial and venous SO2. Studies have demonstrated that when oxygen is abundant, the relative contribution of the retinal circulation in the retinal oxygen supply diminishes, resulting in a higher saturation in the retinal arteries and veins.40 With the retinal oxygen consumption and blood flow remaining unchanged, this shift toward the choroidal circulation would also result in a lower AV difference in the retinal circulation. Although not all studies are consistent on the direct correlation between CT and choroidal blood flow, a plausible explanation of our findings could therefore be that in patients with a thicker choroid, proportionally more oxygen is delivered to the retina via the choroidal circulation.4144 In the healthy individuals, both arterial and venous SO2 were positively correlated with CT. Interestingly, AV difference showed a negative correlation in multivariate analysis, supporting the hypothesis that the relative contribution of the retinal circulation is less in patients with a thicker choroid. In the OAG patients, no such relationship was observed. This lack of correlation could reflect a disturbance in blood flow regulation in glaucoma patients. To further investigate this hypothesis, age-matched studies measuring also retinal, choroidal, and retrobulbar blood flow are needed. 
It is noteworthy that in both groups, systolic blood pressure is slightly higher than would be expected. In the healthy group these findings are presumably largely caused by the “white-coat effect,” since none of the healthy individuals had a personal history of arterial hypertension. However, other factors that were not recorded in this study, such as body mass index, should also be considered. 
This study has several limitations. First, there are large demographic differences between the two groups. Besides age-related changes, the expected higher prevalence of comorbidity and medication use could have possibly influenced our findings. The use of direct vasodilators was an exclusion criterion in both groups. Nonetheless, conclusions about this comparison should be taken cautiously. Second, blood flow in the retinal, choroidal, and retrobulbar circulation was not measured in this study, leaving important questions on the relative influence of these different vascular beds on the correlation unanswered. Last, axial length data, known to be correlated with CT, were not available.45 In order to minimize this bias, subjects with an ametropia exceeding ±4 diopters were not included in this study. 
In conclusion, our data confirm findings of other publications regarding differences in retinal oximetry and peripapillary CT measurements between young healthy individuals and OAG patients. This is the first study to demonstrate a significant positive correlation between peripapillary choroidal thickness and retinal vessel SO2 in young healthy individuals. This correlation was not found in the OAG group. Our current understanding of the intriguing interplay between the retinal and choroidal vasculature in health and disease is far from complete. Further studies are needed to investigate whether the lack of correlation between SO2 and CT reflects a disturbance in the regulation of blood flow in glaucoma patients. 
Acknowledgments
Disclosure: K. Van Keer, None; L. Abegão Pinto, None; K. Willekens, None; I. Stalmans, None; E. Vandewalle, None 
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Figure
 
(A) Choroidal thickness measurements at 500 μm from the optic disc margin. (B) Arterial and venous oxygen saturation measurements in each quadrant on a pseudo-color image from the Oxymap oximeter (see text for details). SN, superonasal; ST, superotemporal; IT, inferotemporal; IN, inferonasal.
Figure
 
(A) Choroidal thickness measurements at 500 μm from the optic disc margin. (B) Arterial and venous oxygen saturation measurements in each quadrant on a pseudo-color image from the Oxymap oximeter (see text for details). SN, superonasal; ST, superotemporal; IT, inferotemporal; IN, inferonasal.
Table 1
 
Characteristics of the Study Population
Table 1
 
Characteristics of the Study Population
Table 2
 
Peripapillary Choroidal Thickness and Retinal Vessel Oxygen Saturation
Table 2
 
Peripapillary Choroidal Thickness and Retinal Vessel Oxygen Saturation
Table 3
 
Retinal Vessel Oxygen Saturation and Correlation With Choroidal Thickness
Table 3
 
Retinal Vessel Oxygen Saturation and Correlation With Choroidal Thickness
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