O R I G I N A L P A P E R
Quantitative assessment of the effect of acute anaerobic
exercise on macular perfusion via swept-source optical
coherence tomography angiography in young football
players
Yalc¸ın Karakucuk .Nilsel Okudan.Banu Bozkurt .Muaz Belviranlı. Tug˘ba Sezer.Sona Gorc¸uyeva
Received: 12 September 2019 / Accepted: 7 February 2020 / Published online: 15 February 2020 Ó Springer Nature B.V. 2020
Abstract
Aim To evaluate the effect of acute anaerobic exercise on macular perfusion measured by swept-source optical coherence tomography angiography (SS-OCTA) in young football players.
Materials and methods Football players with ages between 18 and 20 years were included into the study. After a detailed ophthalmological examination, phys-iological parameters including height (cm), body weight (kg), body fat percentage (%), systemic blood pressure (BP) (mmHg), hematocrit values (%), oxygen saturation pO2 (%) and heart rate (bpm) were recorded. Intraocular pressure (IOP) (mmHg) and SS-OCTA using DRI OCT Triton (Topcon, Tokyo, Japan) were measured immediately before and after Wingate test.
Results Out of 20, 16 participants completed the study. All participants were males with a mean age of 18.12 ± .34 years. Systolic BP, hematocrit and heart rate increased, while pO2and IOP decreased remark-ably after Wingate test (p \ .01). After anaerobic exercise, there was an increase in mean FAZ area in superficial capillary plexus (FAZs) which was not significant (p = .13), while decrease in FAZ area in deep capillary plexus (FAZd) (mm2) was remarkable
(p = .04). No changes were observed in mean vessel density (VD) (%) in superficial capillary plexus (VDs), deep capillary plexus (VDd), choriocapillaris (VDcc), central macular thickness (CMT) (lm) and subfoveal choroidal thickness (SFCT) (lm) after Wingate test (p [ .05). FAZd and some of the VD parameters showed a significant correlation with BP (p \ .05).
Conclusion Acute anaerobic exercise seems not to alter either mean VD in retina and choroid or CMT and SFCT. Among OCTA parameters, only FAZd decreased remarkably.
Keywords Acute anaerobic exercise Macular perfusion Swept-source optical coherence
angiography (SS-OCTA) Young football players Vascular density
Introduction
Acute anaerobic exercise causes changes in systemic circulation leading to increased heart rate and blood flow to the heart, dilatation of vessels supplying the heart and the skeletal muscles and vasoconstriction in the skin and splanchnic tissues [1]. These changes are mediated by the activation of sympathetic nervous system and supported by metabolic factors secreted from active cells [2–7].
Y. Karakucuk (&) N. Okudan B. Bozkurt M. Belviranlı T. Sezer S. Gorc¸uyeva
Selcuk Universitesi Tip Fakultesi, Konya, Turkey e-mail: drkarakucuk83@gmail.com
Retina and choroid are highly vascularized with a complex distribution of blood vessels. The macular microvasculature supplies blood to the inner retina through superficial capillary plexus (SCP) and deep capillary plexus (DCP) [8]. The SCP is located in retinal nerve fiber layer, while DCP consists of two plexuses, located at the inner and outer borders of the inner nuclear layer. The choroidal circulation coming from choriocapillaris (CC) plays a major role in the blood supply of the outer retina by diffusion [8]. Sympathetic nervous system regulates choroidal blood vessels, whereas vasculature of retina is controlled by the local factors which are released from the endothe-lial cells [9, 10]. Hence, we can expect changes in microcirculation of retina and choroid after exercise.
Optical coherence tomography angiography (OCTA) is a noninvasive method of imaging which does rapid evaluation of the retina and choroidal vascular structures without using any contrast. It is based on the principle of decorrelation, in which the signals of red blood cells on B-scan images are seen to fluctuate in each specific area of the retina [11]. OCTA has the advantage of demonstrating the retinal vascu-lar structure layer by layer, thereby facilitating the separate differentiation of the SCP, DCP and CC [11]. Further advantage of OCTA is that allergic reactions do not develop as contrast dye is not used [12].
In the literature, there are very few studies about the effect of exercise on the vasculature of choroid and retina and the results are inconclusive [13–15]. This study was conducted to evaluate the effect of acute anaerobic exercise on macular perfusion measured by swept-source-OCTA (SS-OCTA) in young football players and to determine the association between the changes in OCTA parameters and in physiological parameters after acute anaerobic exercise.
Materials and methods Study design and population
This was a prospective study conducted among young football players aged 18–20 years old, who had undergone routine health checkups at Selcuk Univer-sity, Faculty of Medicine in Konya, Turkey, from April 2019 and May 2019. The study was approved by the Ethics Committee of Selcuk University (Prot. No: 2019/60), and all procedures were done in accordance
with the Declaration of Helsinki. Informed consent was obtained from each participant and confidentiality was maintained.
All participants underwent a detailed ophthalmo-logical examination at the Department of Ophthal-mology, Selcuk University, Faculty of Medicine including best-corrected visual acuity (BCVA), slit-lamp biomicroscopy, at least three intraocular pressure (IOP) measurements with automated non-contact tonometer (Topcon, Computerized Tonometer CT-1/ CT-1P, Hasunma-cho, Itabashi UK, Tokyo, Japan) and fundus examination. Participants were excluded if they had refractive error of either [ 1 diopters (D) of myopia, hyperopia or astigmatism, any cardiovascular system disease that would affect microcirculation, arterial hypertension, history of local or systemic medications, history of ocular trauma or surgery, glaucoma, any congenital or acquired retinal disorder (including retinal vascular disease), history of smok-ing or alcohol consumption.
Height, body weight and body fat percentage were recorded. Systemic blood pressure (BP), hematocrit values, oxygen saturation, heart rate and IOP were measured immediately before and after the exercise. Heart rate (Polar Ò S810i Electro Oy, Kempele, Finland), systemic BP, hematocrit values and oxygen saturation pO2 (Transend Oxy Shuttle, Sensor Medics Co., Anaheim, California, USA) were measured. Optical coherence tomography angiography technique
The subjects were asked before the baseline OCTA measurements to ensure that for at least 2 h previ-ously, no caffeine or drugs had been taken, and any participants who did not meet these criteria were excluded from the study. All participants were asked to rest for 10 min before baseline measurements.
SS-OCTA measurements were taken within imme-diately before and after the Wingate test. To avoid diurnal variations, all the OCTA scans were performed between 11:00 and 13:00.
The Triton SS-OCTA (DRI OCT Triton, Topcon, Tokyo, Japan) uses a wavelength of 1050 nm with a scan speed of 100,000 A-scans per second. The instrument employs an active eye tracker that follows the eye movement and detects blinking and adjusts the scan position accordingly, thereby reducing motion artifact during OCTA imaging. Scans were taken from
6 9 6 mm cubes centered on the fovea. All OCTA scans were performed by one experienced operator (Y.K.). The macular scans were automatically segmented by the OCTA software (IMAGEnet 6V.1.14.8538) into four ‘‘en face’’ OCT slabs: (1) SCP from 2.6 mm beneath the internal limiting membrane to the 15.6 mm beneath the interface of the inner plexiform layer and inner nuclear layer (IPL/INL), (2) DCP from the 15.6 mm beneath the IPL/INL to 70.2 mm beneath the IPL/INL, (3) outer retinal slab from 70.2 mm beneath the IPL/INL to the Bruch’s membrane (BM) and (4) CC from the BM to 10.4 mm beneath the BM [16,17]. High-quality images with a quality index C 70 [16] were taken for statistical analysis.
GNU image manipulation program (GIMP) 2.8.14 was used for quantitative analysis of one measurement of total FAZ area including both superficial and deep values, FAZs, FAZd, VDs, VDd and VDcc. The foveal avascular zone (FAZ) area was defined as the area inside the central border of the capillary network, which was outlined manually for the SCP and DCP by the ‘‘Scissors’’ tool of the GIMP software in accor-dance with the study of Kuehlewein et al [18]. VD was calculated as the percentage area occupied by flowing blood vessels in the selected region. A binary vessel image is extracted from the OCTA en face image, and VD is then calculated by the percentage of white pixels of vessels in the defined sectors on the binary image. SFCT and CMT measurements were taken manually using enhanced HD line scans. Both eyes of each participant were used in the study. Eyes were not eligible if there were any sign of pathologic alteration in structural OCT scans or OCTA images or if the quality of the images were poor.
Wingate test
Following the baseline measurements, all participants underwent Wingate test at the Division of Sports Physiology, Selcuk University, Faculty of Medicine. The Wingate anaerobic test is a short-term maximal intensity cycle ergometer test used to measure the mechanical power output.
For all participants, the exercise was scheduled between 11.00 and 13.00 to exclude possible physi-ological diurnal changes in ocular blood flow. The test is done by pedaling with maximal (all-out) effort for 30 s against a constant braking force. The Wingate anaerobic test was performed on an Ergometric 894E
Peak Bike (Monark Exercise AB, Varberg, Sweden) against a resistance of 75 g kg body weight-1 (4.41 joules pedal revolution-1kg body weight-1). The participants were allowed to pedal unloaded and instructed to reach a pedaling rate of 100 revolutions per minute. The predetermined load was applied to the flywheel automatically by the Monark anaerobic test software and the participants were verbally encour-aged to maintain as high a pedaling rate as possible throughout the 30-s test duration.
Mean-power output and peak-power output were determined by Monark anaerobic test software 2.0. According to this software, peak-power output is the highest power achieved at any given 5-s period. Mean-power output is the average Mean-power of the entire test. Fatigue index was defined by the following formula:
FI = (highest speed - lowest speed)/highest speed 9 100. The procedures of the study are given in detail as a flowchart in Fig. 1.
Statistical analysis
The statistical analysis was performed using SPSS (statistical package for the social sciences) software version 15 for Windows; SPSS, Inc. Shapiro–Wilk test was used to check the normality of the data. Physi-ological parameters, IOP and SS-OCTA parameters before and after Wingate test were compared either with paired t test for data or Wilcoxon signed rank test according to the normality test. Only one eye of the subjects was used in the statistics. The correlations between the changes in physiological and SS-OCTA parameters were evaluated using bivariate correlation test and a p value \ .05 was taken as statistically significant.
Results
Of the 20 young male football players, 18 participants were eligible to be included into the study. Two were excluded because of systemic drug use and history of ocular trauma (Fig. 1). Two participants dropped out of the study, since they experienced nausea, vomiting and hypotension. Table 1shows baseline characteris-tics of the participants. Mean age of the subjects was 18.12 ± 0.34 years (18–20 years). The mean BMI was 22.50 ± 1.84, and three subjects had BMI above the normal range.
The data were normally distributed for most of the parameters except for diastolic BP, oxygen saturation, FAZs, FAZd, VDs inferior and VDd inferior. The mean parameters before and after Wingate test are given in Table2. Systolic BP, hematocrit and heart rate increased, while pO2and IOP decreased remark-ably after Wingate test (p \ .001) (Table2).
After anaerobic exercise, there was an increase in mean area of FAZs (before 246.66 ± 92.67; after 264.65 ± 101.66), a decrease in one measurement of the total FAZ area including both superficial and deep values (before 313.67 and after 306.03), which were not significant (p = .13 and p = .40, respectively),
Fig. 1 Flowchart of the study
Table 1 Baseline characteristics of the study participants
Variable Mean ± SD
Age (year) 18.12 ± 0.34
Height(m) 1.78 ± 0.04
Weight (kg) 71.06 ± 6.19
Body fat (%) 13.36 ± 2.35
Body mass index (%) 22.50 ± 1.84
Peak-power output (W) 1161.87 ± 150.05
Mean-power output (W) 609.73 ± 57.96
while a decrease in FAZd (before 380.69 ± 140.33; after = 347.41 ± 127.76) was remarkable (p = .04) (Table2) (Fig.2a–d). No changes were observed in mean VD in the SCP, DCP and CC, CMT and SFCT after Wingate test (Table2).
The correlations between changes in physiological parameters and OCTA parameters are given in Table3. FAZd showed significant correlations with systolic and diastolic BP (r = .45 and .40, respec-tively) (p \ .05). Among VD parameters, the change in VDs superior (r = .47, p = .01), VDs temporal (r = .385, p = .03) and VDd superior (r = .36, p = .04) showed significant correlations with systemic BP. The change in SFCT was found to be correlated with the change in diastolic BP (r = .42, p = .02).
Discussion
As known physiological changes may occur during exercise, these changes may vary in aerobic and anaerobic conditions depending on the type and duration of the exercise. Systemic vascular changes may be due to redistribution of blood supply and blood being diverted to other organs and skeletal muscles during exercise because of the increase in energy requirement [14,15].
Heart rate, systolic BP and diastolic BP increase and oxygen saturation decreases to compensate for systemically increased energy consumption during exercise [14,15]. In the present study, we observed that systolic and diastolic BP, hematocrit and pulse Table 2 Comparison of
parameters before and after the exercise
Bold font indicates statistical significance Bpm beats per minute, IOP intraocular pressure, FAZs superficial foveal avascular zone, FAZd deep foveal avascular zone, VDs superficial vascular density, VDd deep vascular density, VDcc coriocapillar vascular density, CMT central macular thickness, SFCT subfoveal choroidal thickness
*Analysis done using Paired t test
#Analysis done using
Wilcoxon signed rank test
Parameters Pre-exercise Post-exercise p value
Systolic BP (mmHg) 111.56 ± 9.44 146.56 ± 19.98 .001 Diastolic BP (mmHg) 70.31 ± 6.70 73.44 ± 7.24 .11# pO2(%) 97.06 ± 1.12 85.62 ± 2.13 .001# Hematocrit (%) 44.56 ± 2.58 45.75 ± 2.65 .001 Heart rate (bpm) 66.19 ± 9.74 134.69 ± 14.35 .001 IOP (mmHg) 16.28 ± 2.59 13.66 ± 2.66 .001 FAZs (mm2) 246.66 ± 92.67 264.65 ± 101.66 .13# FAZd (mm2) 380.69 ± 140.33 347.41 ± 127.77 .04# VDs central (%) 22.84 ± 4.27 22.19 ± 4.04 .13* VDs superior(%) 50.36 ± 2.69 50.21 ± 3.76 .77* VDs temporal(%) 47.53 ± 3.34 46.79 ± 3.89 .13* VDs inferior(%) 49.87 ± 3.77 49.87 ± 5.23 .88# VDs nasal(%) 45.98 ± 3.88 45.60 ± 3.92 .51* VDd central(%) 19.07 ± 4.11 19.59 ± 3.99 .27* VDd superior(%) 51.52 ± 2.70 51.94 ± 3.48 .34* VDd temporal(%) 49.14 ± 3.77 48.53 ± 3.49 .22* VDd inferior(%) 52.20 ± 2.81 52.44 ± 4.05 .30# VDd nasal(%) 49.90 ± 2.90 49.47 ± 4.37 .42* VDcc central(%) 55.06 ± 2.39 55.76 ± 2.37 .18* VDcc superior(%) 54.03 ± 1.76 53.34 ± 1.64 .08* VDcc temporal(%) 54.35 ± 1.85 54.28 ± 1.88 .83* VDcc inferior(%) 54.37 ± 1.79 54.15 ± 1.79 .60* VDcc nasal(%) 54.18 ± 2.21 53.70 ± 1.91 .16* CMT (lm) 194.28 ± 24.51 193.16 ± 18.50 .46# SFCT (lm) 355.41 ± 77.84 354.69 ± 57.25 .88#
increased and pO2 values decreased significantly which were consistent with the literature. Assessment of the effect of exercise on normal healthy eyes may be a guide for the progression and regression of many retinal and choroidal diseases.
There are some studies investigating the effect of exercise on macular perfusion but most of them are aerobic exercises [13–15]. Alnawaiseh et al. [14] examined the effect of specific training programs such as sit-ups, push-ups, squats, lunges and rope skipping on systemic and macular perfusion in 13 healthy volunteers. They reported that after the aerobic exercises, VD decreased in the parafoveal region and whole of superficial plexus which was most remark-able in the superior and temporal regions. The change in systolic BP was significantly associated with the change in VDs. They concluded that this may be due to redistribution of blood supply and blood being diverted to other organs and skeletal muscles during exercise because of the increase in energy requirement [14]. In another study, Kim et al. [15] evaluated 32
healthy subjects before and after continuously cycling for 20 min and reported that VD in whole reduced statistically significantly in SCP, while VDd did not change.
Wingate test is a simple, noninvasive test that can be applied to everybody, even children and the disabled to exam athletes’ anaerobic performance. Anaerobic performance is a term that is of great importance for sports branches that are completed in a short time or require explosive force, because the performance of the athlete can be influenced and varied by individual and environmental factors. Stud-ies evaluating perfusion changes in the retina and choroid under anaerobic conditions are nonexistent. So, we designed this study to investigate how anaer-obic conditions affect the perfusion of the eye. Macular perfusion parameters including VDs, VDd, VDcc, FAZs, FAZd, SFCT and CMT were evaluated before and after Wingate test. In order to avoid diurnal and individual variations that might affect the results, Wingate test was performed between 11.00 am and Fig. 2 Swept-source
optical coherence tomography angiography images showing a decrease in FAZ area in deep capillary plexus (FAZd) after anaerobic exercise. aand b show the raw images of the same patients before and after anaerobic exercise, respectively. c FAZd area measurement indicated with green line was 307.617 lm2 before anaerobic exercise. dFAZd area measurement indicated with green line was 283.711 lm2after anaerobic exercise
Table 3 Correlations between the changes in physiological parameters, IOP and SS-OCTA parameters
Systolic BP (mmHg) Diastolic BP (mmHg) pO2 (%) Hematocrit (%) Heart rate (bpm)
IOP (mmHg) r .162 - .101 .019 .037 .108 p .38 .58 .92 .84 .56 FAZs (%) r - .05 .106 .041 - .028 - .095 p .78 .56 .82 .88 .60 FAZd (%) r - .455 - .4 .076 - .114 - .304 p .01 .02 .68 .54 .09 VDs central (%) r .138 .05 .036 - .07 .154 p .45 .78 .85 .71 .40 VDs superior (%) r .467 .061 - .157 - .287 - .195 p .01 .74 .40 .11 .28 VDs temporal (%) r .385 - 0.65 - .083 - .327 - .128 p .03 .73 .65 .07 .48 VDs inferior (%) r .293 .118 - .132 .059 - .071 p .10 .52 .47 .75 .70 VDs nasal (%) r .158 - .004 .126 - .075 - .216 p .39 .99 .49 .68 .24 VDd central (%) r - .015 - .275 .018 - .049 .083 p .93 .13 .92 .79 .65 VDd superior (%) r .362 .207 - .19 - .104 - .028 p .04 .26 .30 .57 .88 VDd temporal (%) r .169 - .013 - .058 - .204 .23 p .36 .94 .75 .26 .21 VDd inferior (%) r .129 .181 - .018 .177 .014 p 0.48 .32 .92 .33 .94 VDd nasal (%) r - .056 .039 .121 - .01 .136 p .76 .83 .51 .96 .46 VDcc central (%) r .195 .239 .02 .15 - .161 p .29 .19 .91 .41 .38 VDcc superior (%) r .124 .158 .129 - .081 .218 p .50 .39 .48 .66 .23 VDcc temporal (%) r .077 - .176 .067 - .215 - .234 p .67 .33 .72 .24 .20 VDcc inferior (%) r .06 - .106 .22 - .001 .097 p .74 .56 .23 .99 .60 VDcc nasal r - .133 - .252 - .042 - .255 - .087 p .47 .17 .82 .16 .64 CMT (lm) r - .164 - .264 .107 - .21 - .242 p .37 .14 .56 .25 .18 SFCT (lm) r .272 .423 .038 .222 .055 p .13 .02 .84 .22 .76
Analysis was done using bivariate correlation test Bold font indicates statistical significance
IOP intraocular pressure, SS-OCTA swept-source optical coherence angiography, FAZs superficial foveal avascular zone, FAZd deep foveal avascular zone, VDs superficial vascular density, VDd deep vascular density, VDcc coriocapillar vascular density, CMT central macular thickness, SFCT subfoveal choroidal thickness
1.00 pm and only 16 football players with similar ages were included in the study. No statistical changes were observed in mean VD in the SCP, DCP and CC after Wingate exercise. There was a moderate correlation between change in systolic BP and change in VDs in the superior and temporal regions and VDd in the superior regions. Despite changes in systemic BP, oxygen saturation and hematocrit level, lack of changes in VDs, VDd and VDcc show that the local compensatory mechanisms seem to be sufficient to maintain retinal and choroidal blood flow during acute anaerobic exercise. This, in turn, supports the hypoth-esis that retinal vascularization is auto-regulated by the local factors released from endothelial cells [9,10]. Kim et al. [15] and Alnawaiseh et al. [14] could not find a remarkable change in FAZ parameter after aerobic exercise. In the present study, baseline FAZs tended to increase after Wingate test; however, this increase was not statistically significant, while, FAZd decreased remarkably after exercise (p \ .05). This might be partially explained by the study of Srienc et al. [19] that reported that local control of blood flow in the retina allows necessary oxygen and nutrients to be efficiently supplied to active neurons, without increasing the supply to inactive retinal regions. In the current study, however, the reduction in FAZd may be attributed to the activation of inactive retinal regions in the anaerobic state to feed deeply located photore-ceptors and supply more oxygen.
The ocular blood circulation has a complex balance system to sustain constant blood flow and oxygen supply to the tissue, in spite of variations in systemic SBP [20]. The choroid, which is highly vascularized tissue of the body, supplies nutrients and oxygen to the outer retina, which is comprised of photoreceptors. The complicated adjustment of blood flow in the choroid subsequently alters ocular perfusion pressure [21]. Blood flow in the tissues remains steady during significant alterations in systemic arterial blood pres-sure or perfusion prespres-sure, even under normal condi-tions by regulatory mechanisms including neural control and local mechanisms. During an acute increase in blood pressure, retinal blood flow displays autoregulatory behavior, and choroidal blood flow for baroregulation, which is seen in cerebral circulation [22,23]. Usui et al. and Jung et al. [24,25] showed a negative correlation between SBP and SFCT. In this study, no changes were observed in CMT and SFCT after Wingate test, which might be due to fact that
Wingate test is an anaerobic test that only takes 30 s and blood flow is not diverted from the cerebral circulation to peripheral organs yet. Therefore, there was a positive correlation between diastolic BP and SFCT. Besides, choroidal nutrition and oxygen sup-plementation can also be maintained with local factors during acute anaerobic exercise.
Decrease in cerebral blood velocity following maximal anaerobic exercise contributes to visual cognitive deficits in the peripheral visual field, decrease in cognitive functions and result in syncope. This may be due to exacerbated after high-intensity exercise by the presence of a hyperventilation-induced hypocapnic cerebral vasoconstriction [26].
The change of IOP during exercise is particularly important for the progression of optic nerve damage in patients with glaucoma. In the literature, there are some studies showing changes in IOP related to various aerobic exercises. Konstantinos et al. [27] reported that aerobic jogging exercise reduced IOP in 25 healthy individuals. According to Qureshi et al. [28], all forms of physical aerobic exercise such as jogging, bicycling and walking reduced IOP. How-ever, Jasien et al. [29] showed that yoga exercise with head-down position was associated with a rapid rise in IOP both in healthy and glaucoma eyes. Vieira et al. [30] reported that IOP increased significantly during bench press exercise and they explained the rise in IOP by breath holding during exercise. To our knowledge, the effect of Wingate test on IOP has not been evaluated before. In this study, IOP decreased remark-ably after Wingate exercise in short term.
This was one of the few studies to study macular perfusion using OCTA in response to Wingate exer-cise, which is an acute anaerobic exercise. One of the limitations of this study is that we only included only young, healthy and active athletes. Hence, findings cannot be interpreted to people with ocular patholo-gies or older persons. A control group who did not exercise between the two measurements would be ideal to conclude whether the differences between the measurements were related to exercise or due to low repeatability in the measurements. In the study of Baek et al. [31], intra-visit repeatability (.75–.94) and inter-visit reproducibility (.84–.986) for retinal vessel density measurements obtained with SS-OCTA showed excellent reliability. Therefore, the change in FAZ area seems to be related to the exercise. The measurements were scheduled at the same time of day
(between 11.00 and 13.00) in all participants to exclude physiological diurnal changes as much as possible, since diurnal variability is generally expected in many physiological parameters of the eye. However, in the same study of Baek et al. [31] peripapillary RVD and macular RVD parameters showed no diurnal variations in healthy subjects and in glaucoma group, only macular temporal RVD showed a statistically significant variation (p \ .05).
Conclusion
Acute anaerobic exercise seems not to alter either mean VD in retina and choroid or CMT and SFCT. Among OCTA parameters, only FAZ area in DCP decreased remarkably. It is necessary to perform additional studies with varied groups of patients with elder ages and ocular and systemic pathologies, such as systemic hypertension, diabetes, glaucoma and age-related macular degeneration to get much evidence on the effect of different exercises on the retinal and choroidal circulation.
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