October 2015
Volume 56, Issue 11
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Retina  |   October 2015
Retinal Blood Flow and Retinal Blood Oxygen Saturation in Mild to Moderate Diabetic Retinopathy
Author Affiliations & Notes
  • Faryan, Tayyari
    Retina Research Group, School of Optometry and Vision Science, University of Waterloo, Waterloo, Ontario, Canada
  • Lee-Anne, Khuu
    Department of Ophthalmology and Vision Sciences, University of Toronto, Toronto, Ontario, Canada
  • John G. Flanagan
    Retina Research Group, School of Optometry and Vision Science, University of Waterloo, Waterloo, Ontario, Canada
    Department of Ophthalmology and Vision Sciences, University of Toronto, Toronto, Ontario, Canada
  • Shaun, Singer
    Department of Ophthalmology and Vision Sciences, University of Toronto, Toronto, Ontario, Canada
  • Michael H. Brent
    Department of Ophthalmology and Vision Sciences, University of Toronto, Toronto, Ontario, Canada
  • Christopher, Hudson
    Retina Research Group, School of Optometry and Vision Science, University of Waterloo, Waterloo, Ontario, Canada
    Department of Ophthalmology and Vision Sciences, University of Toronto, Toronto, Ontario, Canada
  • Correspondence: Christopher Hudson, University of Waterloo, School of Optometry and Vision Science, 200 University Avenue West, Waterloo, ON, Canada, N2L 3G1; chudson@uwaterloo.ca
  • Faryan Tayyari, University of Waterloo, School of Optometry and Vision Science, 200 University Avenue West, Waterloo, ON, Canada, N2L 3G1; ftayyari@uwaterloo.ca
Investigative Ophthalmology & Visual Science October 2015, Vol.56, 6796-6800. doi:10.1167/iovs.15-17481
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      Faryan, Tayyari, Lee-Anne, Khuu, John G. Flanagan, Shaun, Singer, Michael H. Brent, Christopher, Hudson; Retinal Blood Flow and Retinal Blood Oxygen Saturation in Mild to Moderate Diabetic Retinopathy. Invest. Ophthalmol. Vis. Sci. 2015;56(11):6796-6800. doi: 10.1167/iovs.15-17481.

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

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Abstract

Purpose: The aim of this study was to evaluate the relationship between retinal blood flow (RBF) and retinal blood oxygen saturation (SO2) in mild to moderate nonproliferative diabetic retinopathy (NPDR) and in age-matched controls.

Methods: One eye of each of 15 healthy subjects (68 ± 6 years) and 13 subjects with mild to moderate NPDR (67 ± 10 years) was dilated. None of the patients with NPDR had received treatment for their retinopathic changes or had any evidence of sight-threatening characteristics. Doppler Fourier-domain optical coherence tomography blood flow was measured using the prototype RTVue system; six separate measurements each comprising an upper and a lower nasal pupil scan were acquired. Six hyperspectral retinal measurements were acquired using a noninvasive hyperspectral retinal camera (prototype H-8.5 HR Camera).

Results: Total RBF was significantly lower in NPDR when compared to controls (42.7 ± 7.5 vs. 33.0 ± 9.2 μL/min; P = 0.004). Mean retinal arterial and venular SO2 were higher in NPDR than in controls (94.7 ± 2.4% vs. 92.9 ± 1.6%, P = 0.02; 62.5 ± 5.7% vs. 56.3 ± 4.7%, P = 0.003). This study showed a correlation between RBF and arteriolar SO2 in both controls (r = 0.58, P = 0.02) and NPDR (r = 0.54, P = 0.05), but no correlation between venular RBF and venular SO2 in controls (r = 0.24, P = 0.83) or in NPDR (r = 0.23, P = 0.45). The arteriovenous difference (AV difference) was lower in the NPDR group when compared to controls (30.6 ± 6 vs. 36.7 ± 5.3, P = 0.008).

Conclusions: This study found a lower total RBF and a lower AV difference in the NPDR group, suggesting a reduced oxygen uptake from the retina in people with relatively early diabetic retinopathy.

Diabetic retinopathy (DR) is a primary source of visual loss in the world, including North America.1 Diabetic retinopathy appears to be allied closely to disturbances in the vasculature. Hence, many studies have directly investigated the inner retinal blood flow (RBF). However, the results of inner RBF disturbance in DR have been generally contradictory,211 although many studies indicate some aspect of disturbance. 
Elevated RBF has been classically proposed to ultimately cause the progress of DR, probably because of amplified frictional forces (i.e., shear stress) on the endothelial cells lining the walls of retinal vessels.12 However, the exact nature of the blood flow disruption is debatable, perhaps due to the variety of methods used to measure retinal hemodynamics, the diverse stages of retinopathy considered, and the diversity of the diabetic groups.13 From a clinical perspective, the assessment of ocular hemodynamics proposes an improved DR severity classification and perhaps a flag for new treatment opportunities. In addition, retinal hypoxia is thought to promote the production of vascular endothelial growth factor and consequently neovascularization. Assessment of retinal oxygenation in patients with diabetes may help to evaluate the severity of DR and the response to treatments. 
It has been suggested that change in blood circulation leads to functional damage and broad retinal tissue impairment and disturbance during diseases such as DR.14 In this respect, it will be critical to study the oxygen distribution or consumption of the retina and its alteration in response to DR, since RBF or retinal blood oxygen saturation (SO2) alone represents only part of the required information to calculate retinal oxygen utilization. Measurement of these alterations could be used to improve the early detection and management of diseases such as diabetes/DR. Simultaneous RBF measurement and retinal hemoglobin oxygenation are required to assess absolute values of oxygen delivered to the retina,15,16 which is not noninvasively possible at the moment. 
Assessing oxygen tension in the retina has been achieved using O2-sensitive microelectrodes introduced into the eye.1721 While this technique is precise and can accurately define oxygen utilization, the invasive nature of the technique limits its usage to animal models and disqualifies it from clinical purpose. Alternative methods using the introduction of a phosphorescent dye have been utilized to derive oxygen concentration in the optic nerve head and retinal vessels.19,22 Nonetheless, the use of such a dye in humans is not accepted due to toxicity concerns. Imaging techniques established on oxygenated hemoglobin and deoxyhemoglobin and their spectral changes have been used in humans to noninvasively assess oxygen saturation in retinal vessels.18,2327 Oxygen saturation in retinal vessels has been found to be greater in DR in contrast to control subjects.15,2831 Assessment of oxygenation in the retina may facilitate the early detection of DR. The aim of this study was to investigate total RBF and retinal blood oxygen saturation in NPDR. 
Methods
Sample
This study received approval by the University of Waterloo Office of Research Ethics and the Research Ethics Board of the University Health Network, University of Toronto, Canada. Informed consent was obtained from each subject after explanation of the nature and possible consequences of the study according to the tenets of the Declaration of Helsinki. The sample consisted of 28 volunteers in two groups of subjects with mild to moderate NPDR (n = 13; mean age 67; SD 10 years; Table 1) and age-matched healthy controls (n = 15; mean age 68; SD 6 years; Table 1). One eye of each subject was selected for the study. All subjects had a corrected visual acuity of 20/40 or better. Subjects were excluded if they had a family history of any ocular disease apart from DR. None of the patients with NPDR had received treatment of any kind for their retinopathic changes or had any evidence of diabetic macular edema or any other sight-threatening characteristic. Subjects taking medications with known side effects on hemodynamics and subjects with rheumatologic diseases were disqualified to enter the study. None of the subjects smoked or had any respiratory diseases. The NPDR participants had early signs of retinopathy such as microaneuryms and a few scattered dot hemorrhages, but there was no presence of macular edema, ischemic-related signs such as venous beading, deep blot hemorrhages, or intraretinal microvascular abnormalities or imminent neovascularization. Subjects abstained from consuming caffeine 12 hours before the study. 
Table 1
 
Group Mean Age, Male-to-Female Ratio, and Glycosylated Hemoglobin
Table 1
 
Group Mean Age, Male-to-Female Ratio, and Glycosylated Hemoglobin
Assessment of Retinal Blood Flow
Doppler Fourier-domain optical coherence tomography (Doppler FD-OCT) is used to measure RBF. This novel imaging method offers RBF assessment using a physical phenomenon called Doppler phase shift.32 The principle of the Doppler phase shift has been incorporated into the commercially available Doppler FD-OCT (Optovue, Inc., Freemont, CA, USA). Doppler FD-OCT produces high-resolution cross-sectional images of the retina. This instrument uses a laser light source of 841 nm with bandwidth of 49 nm and an incident power of 500 μW on the cornea. These factors deliver an axial resolution of 5.4 μm in tissue.33 System transverse resolution was 20 μm.34 
In contrast to morphologic FD-OCT systems that generate structural images, the prototype Doppler FD-OCT evaluates the Doppler phase shift between two consecutive A-scans. Light reflected from moving particles undergoes Doppler phase shift. 
Flow velocity is determined by    
where v is the flow velocity in an OCT voxel, and ΔΦ = ϕ1 − ϕ2 is the Doppler phase shift. Φ1 and Φ2 are the phase of voxels in the same position in consecutive OCT axial scans, λ0 is the source center wavelength, n is the refractive index of the medium, T is the time interval between consecutive scans, and θ is the Doppler angle defined by the OCT beam axis relative to the line perpendicular to blood vessel flow axis.35 
Assessment of Retinal Blood Oxygen Saturation
The principle of the oximeter has been described elsewhere,36 but briefly, a prototype custom-built fundus camera (H-8.5 HR Camera; Optina Diagnotics, Inc., Montreal, QC, Canada) is the foundation of the hyperspectral imaging system that incorporates a tunable laser source (TLS) as the light source. The TLS, built on Bragg grating filtering technology (Photon ETC, Montreal, QC, Canada), makes it possible to transfer wavelengths with a half peak bandwidth of 2 nm (range, 400–1000 nm). The TLS permits rapid wavelength presentation from the stable and powerful super-continuum light source (Leukos-SM-30-OEM; Leukos Innovative Optical Systems, Limoges, France). The imaging system is administered by using PhySpec (Photon ETC), a software program that operates the Bragg tunable filter (BTF) and charge-coupled device camera to permit factors such as operator-defined wavelength range and wavelength interval. A low-power white light source (delivering approximately 100 mW over 420–2400 nm) and the BTF are utilized to eliminate the use of conventional flash lamp, and consequently all images are obtained at low light levels, thus decreasing any potential change of the ocular metabolites and photopigment status.36 Multispectral retinal images were taken using specific wavelengths (i.e., 548, 569, 586, 600, 605, and 610 nm) at an exposure time of 80 ms for each wavelength. However, the notion of the optical density ratio introduced by Beach et al.23 of the two monochromatic wavelengths (586 and 605 nm) was performed to calculate retinal blood oxygen saturation. 
Image Processing
The imaging system is based on using PhySpec (Photon ETC), and the cubes are normalized and corrected for wavelength-dependent optical scaling and slight involuntary eye movements by means of this software. The 570 nm was selected as reference image for scaling since the vessels were most distinct at this wavelength. The optic nerve head (ONH) portion of the image was chosen as the reference region, and all images in the cube were aligned correspondingly. Furthermore, a Gaussian filter was utilized for boosting the details of each cube. 
Procedures
Refraction, logMAR visual acuity, Goldmann applanation tonometry, and resting blood pressure were assessed prior to dilation of the study eye. The pupil of the study eye was dilated using Mydriacyl 1% (Alcon, Mississauga, ON, Canada) at the beginning of each visit to achieve an adequate view of the fundus for the RBF image acquisition and retinal blood oxygen saturation measurements. A minimum of six separate FD-OCT Doppler measurements (i.e., each separate measurement comprising an upper nasal pupil scan and a lower nasal pupil scan) and six blood oxygen saturation measurements were acquired on the first-degree arterioles and venules. 
Analysis
Differences in outcome variables between controls and NPDR subjects were assessed with Student's t-tests. A Pearson correlation analysis was performed to examine the relationship between RBF and retinal blood oxygen saturation. In all analyses, 2-tailed P < 0.05 indicated statistical significance. 
Results
The results of this study showed that the total RBF was significantly lower in diabetic patients (33.0 vs. 42.7 μL/min; P = 0.004, Fig. 1). 
Figure 1
 
Box plots representing total retinal blood flow in control and NPDR patients (42.7 vs. 33.0 μL/min; P = 0.004). The asterisk represents extremes, and the small circles represent outliers. The error bars show standard deviation.
Figure 1
 
Box plots representing total retinal blood flow in control and NPDR patients (42.7 vs. 33.0 μL/min; P = 0.004). The asterisk represents extremes, and the small circles represent outliers. The error bars show standard deviation.
The mean SO2 values in the arterioles and venules for the control participants and NPDR subjects are shown in Table 2
Table 2
 
Group Mean Values for Blood Oxygen Saturation and Total Retinal Blood Flow for Nonproliferative Diabetic Retinopathy and Aged-Matched Controls
Table 2
 
Group Mean Values for Blood Oxygen Saturation and Total Retinal Blood Flow for Nonproliferative Diabetic Retinopathy and Aged-Matched Controls
The results of this study showed that mean retinal arteriolar blood oxygen saturation was higher in diabetic patients when compared to the healthy controls (94.7 ± 2.4% vs. 92.9 ± 1.6%, P = 0.025). There was also a significant difference in venular blood oxygen saturation between NPDR and control subjects (62.5 ± 5.7% vs. 56.3 ± 4.7%, P = 0.003). The arteriovenous difference (AV difference) was significantly lower in NPDR subjects when compared to controls (30.6 ± 6.0% vs. 36.7 ± 5.3%, P = 0.008). 
This study revealed a correlation between total RBF and arteriolar oxygen saturation in both controls (r = 0.58, P = 0.02; Fig. 2) and NPDR (r = 0.54, P = 0.05; Fig. 2); however, the study revealed no correlation between total RBF and venular oxygen saturation in either controls (r = 0.24, P = 0.83; Fig. 3) or NPDR (r = 0.23, P = 0.45; Fig. 3). 
Figure 2
 
Arteriolar retinal blood oxygen saturation as a function of total retinal blood flow (retinal venular blood flow) in control (r = 0.58, P = 0.02) and NPDR group (r = 0.54, P = 0.05).
Figure 2
 
Arteriolar retinal blood oxygen saturation as a function of total retinal blood flow (retinal venular blood flow) in control (r = 0.58, P = 0.02) and NPDR group (r = 0.54, P = 0.05).
Figure 3
 
Venular retinal blood oxygen saturation as a function of total retinal blood flow (retinal venular blood flow) in control (r = 0.24, P = 0.83) and NPDR group (r = 0.23, P = 0.45).
Figure 3
 
Venular retinal blood oxygen saturation as a function of total retinal blood flow (retinal venular blood flow) in control (r = 0.24, P = 0.83) and NPDR group (r = 0.23, P = 0.45).
Figure 2 represents retinal venular blood flow as a function of retinal arteriolar blood oxygen saturation in both control and NPDR groups, and Figure 3 illustrates retinal venular blood flow as a function of retinal venular blood oxygen saturation in both control and NPDR groups. 
Discussion
It has been shown that DR is associated with early retinal vascular dysregulation. Therefore, many studies have investigated the inner RBF. Nevertheless, the results for inner RBF disturbance in DR have been contradictory,211 although most indicate some aspect of disturbance. It has been reported that NPDR patients or patients without retinopathy have disturbances in RBF at different times of the day due to change in their plasma glucose, which was suggested as a possible cause of microvascular changes in DR.37 To the best of our knowledge, this is the first study that investigates the relationship between RBF and retinal oxygen saturation. The results of this study showed lower total RBF in people with NPDR when compared to controls (P = 0.004). The AV difference was also significantly lower in NPDR subjects when compared to controls. The lower total RBF and the lower AV difference exhibited by the NPDR group suggest a reduced oxygen uptake from the retina in people with relatively early DR. The study also showed an association between total RBF and arteriolar oxygen saturation; however, it did not reveal any correlation between total RBF and retinal venular blood oxygen saturation. Bearing in mind the small sample size, the study does not eliminate the possibility of an association between retinal venular blood oxygen saturation and total RBF. The lack of correlation between venular RBF and venular oxygen saturation might be explained either by an absence of any effect or by insufficient study power. Therefore, further studies are required to substantiate any correlation between total RBF and arteriolar and venular oxygen saturation. 
The combination of retinal oxygen saturation and RBF can be used to extract more information about retinal metabolism, since    
Theoretically, each gram of hemoglobin binds 1.39 mL oxygen. The oxygen saturation curve represents a PaO2 (arterial oxygen tension) as a function of SaO2 (arterial SO2); 0.003 stands for the oxygen solubility coefficient in human plasma (TRBF = Total RBF [μL/min]). 
The direction of the change in total RBF in DR is controversial.5,3840 The present study showed a reduction in RBF when comparing NPDR subjects with controls. Our oximetry data are in agreement with Hardarson's thesis results.41 Hardarson interpreted this result to occur due to impaired diffusion of oxygen to the adjacent tissue through the thickened arteriolar walls of diabetic subjects or because of damaged capillary network. Hardarson also suggested several other possibilities, such as increased total RBF, decreased oxygen consumption due to cell death, and technical artifact. Higher blood flow would be inclined to reduce the release of oxygen from hemoglobin and therefore would result in reduced diffusion of oxygen across the arteriolar walls.41 
Measured changes in total RBF might represent contributions from different parts of the retina with both decreased and increased RBF. Lack of association between RBF and SO2 might be as a result of the fact that both retinal and choroidal circulations provide oxygen and nutrient supply to the retina. The retina could take oxygen from choroid; hence the RBF and the retinal blood oxygen saturation are not associated. A limitation of the current oximetry techniques is that tissue oxygen saturation measurements are not feasible yet. Another challenge is that simultaneous measurement of RBF and retinal oxygen saturation is not possible yet. 
In summary, the results of this work revealed a lower total RBF and a lower AV difference exhibited by the NPDR group when compared to age-matched controls, suggesting a reduced oxygen uptake from the retina in people with relatively early DR. The work also revealed a relationship between retinal arteriolar blood oxygen saturation and RBF. 
Acknowledgments
The authors thank Susith Kulasekara, Ayda Shahidi, and Sunni Patel for their general assistance. 
Supported by the Ontario Research Fund for Research Excellence (RE-04-034) and an anonymous donor. Optina, Inc. provided financial and in-kind support and student stipend funding. 
Disclosure: F. Tayyari, None; L.-A. Khuu, None; J.G. Flanagan, None; S. Singer, None; M.H. Brent, None; C. Hudson, Optovue, Inc. (F), Optina (F, R) 
References
Zimmet P, Alberti KG, Global Shaw J. and societal implications of the diabetes epidemic. Nature. 2001; 414: 782–787.
Ferris FL,III Patz A. Macular edema. A complication of diabetic retinopathy. Surv Ophthalmol. 1984; 28 (suppl): 452–461.
Bertram B, Wolf S, Arend O, Schulte K, Reim M. Retinal circulation and current blood glucose value in diabetic retinopathy [in German]. Klin Monbl Augenheilkd. 1992; 200: 654–657.
Bursell SE, Clermont AC, Kinsley BT, Simonson DC, Aiello LM, Wolpert HA. Retinal blood flow changes in patients with insulin-dependent diabetes mellitus and no diabetic retinopathy. Invest Ophthalmol Vis Sci. 1996; 37: 886–897.
Feke GT, Buzney SM, Ogasawara H, et al. Retinal circulatory abnormalities in type 1 diabetes. Invest Ophthalmol Vis Sci. 1994; 35: 2968–2975.
Gilmore ED, Hudson C, Nrusimhadevara RK, et al. Retinal arteriolar diameter, blood velocity, and blood flow response to an isocapnic hyperoxic provocation in early sight-threatening diabetic retinopathy. Invest Ophthalmol Vis Sci. 2007; 48: 1744–1750.
Gilmore ED, Hudson C, Nrusimhadevara RK, et al. Retinal arteriolar hemodynamic response to an acute hyperglycemic provocation in early and sight-threatening diabetic retinopathy. Microvasc Res. 2007; 73: 191–197.
Grunwald JE, Riva CE, Baine J, Brucker AJ. Total retinal volumetric blood flow rate in diabetic patients with poor glycemic control. Invest Ophthalmol Vis Sci. 1992; 33: 356–363.
Grunwald JE, DuPont J, Riva CE. Retinal haemodynamics in patients with early diabetes mellitus. Br J Ophthalmol. 1996; 80: 327–331.
Guan K, Hudson C, Wong T, et al. Retinal hemodynamics in early diabetic macular edema. Diabetes. 2006; 55: 813–818.
Patel V, Rassam S, Newsom R, Wiek J, Kohner E. Retinal blood flow in diabetic retinopathy. BMJ. 1992; 305: 678–683.
Kohner EM, Patel V, Rassam SM. Role of blood flow and impaired autoregulation in the pathogenesis of diabetic retinopathy. Diabetes. 1995; 44: 603–607.
Schmetterer L, Wolzt M. Ocular blood flow and associated functional deviations in diabetic retinopathy. Diabetologia. 1999; 42: 387–405.
Delori FC. Noninvasive technique for oximetry of blood in retinal vessels. Appl Opt. 1988; 27: 1113–1125.
Hammer M, Vilser W, Riemer T, et al. Diabetic patients with retinopathy show increased retinal venous oxygen saturation. Graefes Arch Clin Exp Ophthalmol. 2009; 247: 1025–1030.
Pittman RN, Duling BR. A new method for the measurement of percent oxyhemoglobin. J Appl Physiol. 1975; 38: 315–320.
Stefánsson E, Jensen PK, Eysteinsson T, et al. Optic nerve oxygen tension in pigs and the effect of carbonic anhydrase inhibitors. Invest Ophthalmol Vis Sci. 1999; 40: 2756–2761.
Buerk DG, Atochin DN, Riva CE. Simultaneous tissue PO2, nitric oxide, and laser Doppler blood flow measurements during neuronal activation of optic nerve. Adv Exp Med Biol. 1998; 454: 159–164.
Cranstoun SD, Riva CE, Munoz JL, Pournaras CJ. Continuous measurements of intra-vascular pO2 in the pig optic nerve head. Klin Monbl Augenheilkd. 1997; 210: 313–315.
Riva CE, Pournaras CJ, Poitry-Yamate CL, Petrig BL. Rhythmic changes in velocity, volume, and flow of blood in the optic nerve head tissue. Microvasc Res. 1990; 40: 36–45.
Linsenmeier RA, Braun RD, McRipley MA, et al. Retinal hypoxia in long-term diabetic cats. Invest Ophthalmol Vis Sci. 1998; 39: 1647–1657.
Shonat RD, Wilson DF, Riva CE, Cranstoun SD. Effect of acute increases in intraocular pressure on intravascular optic nerve head oxygen tension in cats. Invest Ophthalmol Vis Sci. 1992; 33: 3174–3180.
Beach JM, Schwenzer KJ, Srinivas S, Kim D, Tiedeman JS. Oximetry of retinal vessels by dual-wavelength imaging: calibration and influence of pigmentation. J Appl Physiol (1985). 1999; 86: 748–758.
Hickam JB, Frayser R, Ross JC. A study of retinal venous blood oxygen saturation in human subjects by photographic means. Circulation. 1963; 27: 375–385.
Schweitzer D, Thamm E, Hammer M, Kraft J. A new method for the measurement of oxygen saturation at the human ocular fundus. Int Ophthalmol. 2001; 23: 347–353.
Schweitzer D, Hammer M, Kraft J, Thamm E, Konigsdorffer E, Strobel J. In vivo measurement of the oxygen saturation of retinal vessels in healthy volunteers. IEEE Trans Biomed Eng. 1999; 46: 1454–1465.
Tiedeman JS, Kirk SE, Srinivas S, Beach JM. Retinal oxygen consumption during hyperglycemia in patients with diabetes without retinopathy. Ophthalmology. 1998; 105: 31–36.
Hardarson SH, Stefánsson E. Retinal oxygen saturation is altered in diabetic retinopathy. Br J Ophthalmol. 2012; 96: 560–563.
Jørgensen CM, Hardarson SH, Bek T. The oxygen saturation in retinal vessels from diabetic patients depends on the severity and type of vision-threatening retinopathy. Acta Ophthalmol. 2014; 92: 34–39.
Khoobehi B, Firn K, Thompson H, Reinoso M, Beach J. Retinal arterial and venous oxygen saturation is altered in diabetic patients. Invest Ophthalmol Vis Sci. 2013; 54: 7103–7106.
Hammer M, Heller T, Jentsch S, et al. Retinal vessel oxygen saturation under flicker light stimulation in patients with nonproliferative diabetic retinopathy. Invest Ophthalmol Vis Sci. 2012; 53: 4063–4068.
Wang Y, Bower BA, Izatt JA, Tan O, Huang D. In vivo total retinal blood flow measurement by Fourier domain Doppler optical coherence tomography. J Biomed Opt. 2007; 12: 041215.
Wang Y, Lu A, Gil-Flamer J, Tan O, Izatt JA, Huang D. Measurement of total blood flow in the normal human retina using Doppler Fourier-domain optical coherence tomography. Br J Ophthalmol. 2009; 93: 634–637.
Wang Y, Bower BA, Izatt JA, Tan O, Huang D. Retinal blood flow measurement by circumpapillary Fourier domain Doppler optical coherence tomography. J Biomed Opt. 2008; 13: 064003.
Tayyari F, Yusof F, Vymyslicky M, et al. Variability and repeatability of quantitative, Fourier domain-OCT Doppler blood flow in young and elderly healthy subjects. Invest Ophthalmol Vis Sci. 2014; 55: 7716–7725.
Patel SR, Flanagan JG, Shahidi AM, Sylvestre JP, Hudson C. A prototype hyperspectral system with a tunable laser source for retinal vessel imaging. Invest Ophthalmol Vis Sci. 2013; 54: 5163–5168.
Pemp B, Polska E, Garhöfer G, Bayerle-Eder M, Kautzky-Willer A, Schmetterer L. Retinal blood flow in type 1 diabetic patients with no or mild diabetic retinopathy during euglycemic clamp. Diabetes Care. 2010; 33: 2038–2042.
Kohner EM, Hamilton AM, Saunders SJ, Sutcliffe BA, Bulpitt CJ. The retinal blood flow in diabetes. Diabetologia. 1975; 11: 27–33.
Bursell SE, Clermont AC, Kinsley BT, Simonson DC, Aiello LM, Wolpert HA. Retinal blood flow changes in patients with insulin-dependent diabetes mellitus and no diabetic retinopathy. Invest Ophthalmol Vis Sci. 1996; 37: 886–897.
Bertram B, Wolf S, Fiehofer S, Schulte K, Arend O, Reim M. Retinal circulation times in diabetes mellitus type 1. Br J Ophthalmol. 1991; 75: 462–465.
Hardarson SH. Retinal oximetry. Acta Ophthalmol. 2013; 91 Thesis 2: 1–47.
Figure 1
 
Box plots representing total retinal blood flow in control and NPDR patients (42.7 vs. 33.0 μL/min; P = 0.004). The asterisk represents extremes, and the small circles represent outliers. The error bars show standard deviation.
Figure 1
 
Box plots representing total retinal blood flow in control and NPDR patients (42.7 vs. 33.0 μL/min; P = 0.004). The asterisk represents extremes, and the small circles represent outliers. The error bars show standard deviation.
Figure 2
 
Arteriolar retinal blood oxygen saturation as a function of total retinal blood flow (retinal venular blood flow) in control (r = 0.58, P = 0.02) and NPDR group (r = 0.54, P = 0.05).
Figure 2
 
Arteriolar retinal blood oxygen saturation as a function of total retinal blood flow (retinal venular blood flow) in control (r = 0.58, P = 0.02) and NPDR group (r = 0.54, P = 0.05).
Figure 3
 
Venular retinal blood oxygen saturation as a function of total retinal blood flow (retinal venular blood flow) in control (r = 0.24, P = 0.83) and NPDR group (r = 0.23, P = 0.45).
Figure 3
 
Venular retinal blood oxygen saturation as a function of total retinal blood flow (retinal venular blood flow) in control (r = 0.24, P = 0.83) and NPDR group (r = 0.23, P = 0.45).
Table 1
 
Group Mean Age, Male-to-Female Ratio, and Glycosylated Hemoglobin
Table 1
 
Group Mean Age, Male-to-Female Ratio, and Glycosylated Hemoglobin
Table 2
 
Group Mean Values for Blood Oxygen Saturation and Total Retinal Blood Flow for Nonproliferative Diabetic Retinopathy and Aged-Matched Controls
Table 2
 
Group Mean Values for Blood Oxygen Saturation and Total Retinal Blood Flow for Nonproliferative Diabetic Retinopathy and Aged-Matched Controls
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