Download Choroidal blood flow during isometric exercises.

Choroidal Blood Flow During Isometric Exercises
Charles E. Riva*-\ Patrick Titze*^ Mark Hero,* Armand Movaffaghy*
and Benno L. Petrig*
Purpose. To investigate the response of choroidal bloodflowin the foveal region of the human
eye to increases in mean perfusion pressure (PPm = mean ophthalmic artery pressure intraocular pressure; IOP) induced by isometric exercises.
Methods. Using laser-Doppler flowmetry, changes in velocity (ChBVel), number (ChBVol),
and flux (ChBF) of red blood cells in the choroidal vascular system in the foveal region of
the fundus were measured in both eyes of 11 normal subjects (ages 18 to 57 years) during
isometric exercises.
Results. During 90 seconds of squatting, PPm increased by an average of 67%, from 46 to 77
mm Hg. This resulted in a significant increase of 12% in ChBFm (the mean of ChBF during
the heart cycle), mainly caused by an increase in ChBVelm. A further increase in PPm to a
value approximately 85% above baseline resulted in a 40% increase in ChBFm. A significant
negative correlation was found between the changes in ChBVelm and ChBVolm during squatting.
Conclusions. Previous studies have demonstrated that during isometric exercise, blood pressures in the ophthalmic and brachial arteries rise in parallel. These observations and the
current results indicate that an increase in PPm up to 67% induces an increase in choroidal
vascular resistance that limits the increase in choroidal blood flow to approximately 12%.
This regulatory process fails when PPm is further increased. Invest Ophthalmol Vis Sci.
1997; 38:2338-2343.
Isometric exercises increase heart rate, arterial pressure, and sympathetic nerve activity.1"3 The effect of
this type of exercises on blood flow in vessels supplying
muscle groups, 4 the skin,5 or larger body regions 6 has
been studied extensively. Few investigations, however,
have been devoted to the ocular circulation. Results
of studies in cats and monkeys7"9 have demonstrated
an efficient regulation of blood flow through the optic
nerve, uvea, and retina in the face of acute increases
in arterial blood pressure. In humans, such a regulation has been shown in the ophthalmic artery, iris,10
and retina."
The purpose of this work was to investigate the
From the *lnstilut de Recherche en Ophtalmologie, Sion and f Medical School of the
University of Lausanne, Switzerland.
Presented at 1996 Meeting of the Association for Research in Ophthalmology and
Vision, Fort Laudeidale, Florida, April 27-May 3.
Supported in part by the Swiss National Science Foundation (grant #3200043157.95) and Loterie Rornande, Lousanne, Switzerland.
Submitted for publication December 6, 1996; revised May 30, 1997; accepted June
3, 1997.
Proprietary interest category: N.
Reprint requests: Charles E. Riva, Institut de Recherche en Ophtalmologie, Av.
Grand-Champsec 64, Case Postale 4168, 1950 Sion 4, Switzerland.
2338
time course and magnitude of the response of choroidal blood flow in the foveal region of the human fundus to increases in arterial blood pressure induced by
the static exercise of squatting.
MATERIALS AND METHODS
Subjects
Measurements were obtained from 22 eyes of 11
healthy male volunteers, ranging in age from 18 to 57
years. Their average systolic/diastolic brachial artery
blood pressures at rest were 119/80 mm Hg. The experiment was performed first for measurements in
one eye, chosen at random, and were repeated some
days later for measurements in the other eye. Subjects
had no history of systemic or ocular diseases, and the
results of ocular examinations were normal. Spherical
refraction ranged from —3 to +3 diopters. Mean intraocular pressure (IOP) was 12.4 ± 2.4 mm Hg. Subjects
were asked to abstain from drinking coffee and smoking for 24 hours before the study. The pupils were
Investigative Ophthalmology & Visual Science, October 1997, Vol. 38, No. 11
Copyright © Association for Research in Vision and Ophthalmology
Downloaded From: http://iovs.arvojournals.org/pdfaccess.ashx?url=/data/journals/iovs/933419/ on 05/12/2017
2339
Choroidal Blood Flow
dilated with one to two drops of 1% tropicamide. Brachial artery blood pressure was measured, using an
electronic sphygmomanometer. The procedures were
approved by the University of Lausanne Medical Faculty Ethical Committee and followed the tenets of the
Declaration of Helsinki. Informed consent was obtained from all subjects, after the nature and possible
consequences of the study were fully explained to
each.
Measurement of ChBF
The method for measuring choroidal red blood cell
flux (ChBF) in the foveal region has been published
recently.12 Briefly, subjects were asked to fixate at a
diode laser beam (wavelength = 811 nm, 100 fiW at
the cornea), which was delivered to the eye through
a fundus camera (model TRC, Tokyo, Japan). Light
scattered by moving red blood cells in the tissue volume sampled by the incident laser beam was detected
at the fundus image plane of the camera by an optical
fiber. The diameter of the beam at the fundus of an
emmetropic eye was approximately 300 fxm. Relative
ChBF was determined by analyzing the laser-Doppler
flowmetry signal with a NeXT computer (Redwood
City, CA),13 using an algorithm based on Bonner and
Nossal's photon diffusion theory.14 This algorithm is
equivalent to the one implemented in commercial laser-Doppler flowmetry systems (BPM403A; Vasamedics, Minneapolis, MN; PeriFlux PF3; Perimed, Stockholm, Sweden). It provides, in addition to ChBF, a
relative, continuous measurement of the velocity
(ChBVel), the volume (ChBVol) of blood within the
sampled tissue volume, and the DC level of the photocurrent. The latter is proportional to the total
amount of light reaching the detector and is used to
monitor the alignment of the camera with the eye of
the subject. The algorithm also automatically excludes
the Doppler signal during blinks, thereby minimizing
potential artifacts. The flow parameters are related to
each other through the relationship ChBF = k X
ChBVel X ChBVol, wherein k represents an instrumental constant.
Pulsatility of ChBF, PUCI,BF, was defined as (1 —
ChBF<li:isl/ChBFsysl), where ChBFcli:isl and ChBFsysl are
the values of ChBF at end diastole and peak systole,
respectively. PUCI,BVCI and Puciiiwoi were defined in a
similar way. For determining Pu, each flow parameter
was measured every 46 ms. Serial data points were
then averaged in phase with the heart pulse, which
was continuously recorded. All data points within a
chosen time segment, which have the same phase,
were averaged together. This procedure was repeated
for all phases, producing an average waveform representative of each flow parameter. For calculation of
Pu of a given flow parameter, the systolic and diastolic
values of this parameter were taken as the maximum
and minimum of the average waveform, respectively.
Isometric Exercises
Squatting was used as the isometric exercise. Systolic
and diastolic brachial artery blood pressures were
measured by sphygmomanometry, at rest and at various times during the experiment. Mean perfusion
pressure, PPin, was calculated as: PPin = 2/3(MAP) —
IOP. IOP is the intraocular pressure. Mean blood pressure (MAP) = BPdiMl + 73(BPsysl-BPdiasl), where BPdiM1
and BPsysl are the blood pressures during diastole and
systole, respectively.
Heart rate was continuously recorded with an earlobe transducer. Intraocular pressure was measured,
using a TONO-Pen XL (Mentor, MD), before, at the
end of the exercise, and immediately after the end of
the exercise. Before the subjects were asked to perform the squatting exercise, two baseline measurements of the flow parameters were performed, each
of at least 15 seconds' duration, while the subject was
sitting.
Sensitivity of the Technique
Sensitivity, S, of each flow p a r a m e t e r — t h a t is, the
m i n i m u m c h a n g e that can be detected by the techn i q u e — w a s calculated u n d e r n o r m a l conditions, using two successive 10-second baseline (bl) recordings,
a n d d u r i n g squatting, using the last two 10-second
segments of squatting. T o calculate Sbi u n d e r normal
conditions (baseline) for a given flow p a r a m e t e r , x,
we d e t e r m i n e d the difference, A 1 = ^ b | 2 — xJbn between the m e a n of both segments in eye i. After det e r m i n i n g the standard deviation <rbi of the A' s , Sbi was
obtained using the formula
2Xl00XtXab,
N/nX(.Vbl
in which n is the number of eyes measured and / is
the two-tailed critical value of the ^-distribution for n1 degrees of freedom, at die 0.05 level of significance.
The same procedure was used to calculate Ssq at the
end of squatting.
Statistics. Mean changes in the blood flow parameters, perfusion pressure, and flow pulsatility were assessed for significance by ±95% confidence intervals
of the mean, corresponding to a significance level of
0.05.
RESULTS
Figure 1 shows a sample time course of ChBVel,
ChBVol, and ChBF at baseline, during squatting and
during the return to normal physiologic conditions.
Downloaded From: http://iovs.arvojournals.org/pdfaccess.ashx?url=/data/journals/iovs/933419/ on 05/12/2017
Investigative Ophthalmology & Visual Science, October 1997, Vol. 38, No. 11
2340
MAP(mmHg)
120/80
IOP(mmHg)
11
160/110 185/120 200/140
14
160/95
150/90
9
10
ChBVel
ChBVol
ChBF
Time Constant n 1 sec
10 seconds of recording centered at this time. Average
heart rate increased from 73 to 107 bpm. During
squatting, PPm increased by as much as 67%, from 46
± 2.6 mm Hg to 77 ± 7 mm Hg. ChBVelm and ChBFm
increased with the duration of squatting. We fitted the
changes in both flow parameters with a function of
the form a X timeB, where a and b are parameters. A
plot of log(ChBVelm-100%) and log(ChBFm-100%)
versus log(time) provided significant linear correla-
130 ^
120C
J&
FIGURE l. Sample time course of the flow parameters,
PQ
ChBVel, ChBVol, and ChBF during baseline (0 to <se>65
seconds), squatting {period between vertical, dotted lines) and
U
recovery from squatting (after <se>160 seconds). Time
constants of the recordings and display were 0.05 seconds
and 1 second, respectively. The IOP and systolic/diastolic
are shown on top of the recordings. Changes in the flow
parameters during the heart cycle (bottom) were obtained
on the basis of approximately 20 seconds of recordings centered at 25 seconds (baseline) and at 140 seconds (end of
squatting). The determination of these changes is explained
43
in Methods. ChBVel, ChBVol, and ChBF = velocity, volume,
U
and flux, respectively,
110 -
1009080
-40
40
80
120
160
200
240
40
80
120
160
200
240
140120-
8060
-40
0
140130 -
Time constant of the recordings was 0.05 seconds.
Time constant of the display was 1 second. In this
subject, heart rate increased during the exercise from
64 to 110 bpm and systolic/mean/diastolic BP from
120/93/80 to 200/160/140 mm Hg. There was a 3mm Hg increase in IOP. PPm increased from 50 to 92
mm Hg (84%). Average ChBFm, in which the subscript
m indicates the mean value of ChBF during the heart
cycle, was determined for the 10-second segment centered at 25 seconds: The 10-second segment centered
at 140 seconds showed an increased from 9.8 to 12
units (22%). This increase is mainly caused by a 25%
increase in ChBVelm from 2.43 to 3.04 units. ChBVolm
decreased by =^3%, from 0.35 to 0.34 units. Most of the
changes in the flow parameters occurred at systolic/
diastolic blood pressures between 185/120 and 200/
140 mm Hg. When squatting was stopped, MAP returned to baseline value within approximately 2 minutes (not shown in Fig. 1). ChBVelm and ChBFm returned to baseline in less than 15 seconds.
Figure 2 demonstrates the normalized (baseline
= 100%) group average of PPm and of the flow parameters, ChBVelm, ChBVolm and ChBFm, as a function of
time for the 22 eyes during the first 90 seconds of
exercise, the period during which all subjects were
able to squat. In each subject, the value of each flow
parameter at a given time was obtained by averaging
120-
trill f
110-
PQ
U
1009080
-40
0
40
80
120
160
200
240
200
240
200180 160140120-
*
100-
80
-40
0
40
80
120
*
160
*
Time (sec)
2. Time course of group average of PPm, ChBVel,,,,
ChBVol,,, and ChBF,,, (the mean of each flow parameter
during the heart cycle) during squatting and recovery from
squatting. They were obtained from 22 eyes in 11 subjects.
Each data point is an average of 16 values. It represents a
mean during 10 seconds of recording. Error bars are the
95% confidence limits of the mean. The initial point is the
average baseline value which was normed to 100% in every
subject. PPm = mean perfusion pressure; ChBVel,,,, ChBVol,,,
and ChBF,,, = mean values for velocity, volume and flux,
respectively, of red blood cells in the choriodal vascular
system of the fovea.
FIGURE
Downloaded From: http://iovs.arvojournals.org/pdfaccess.ashx?url=/data/journals/iovs/933419/ on 05/12/2017
2341
Choroidal Blood Flow
180160w
140120-
u
100-
80
80
X \ {I
100
120
140
160
180
200
P P m(°/n\
^ '
3. Average ChBFm versus PPm during squatting obtained from 22 eyes in 11 subjects. Dotted line: ChBFm versus
PPm with no regulation (constant vascular resistance). Each
data point represents an average of 24 consecutive values.
Error bas are the ±95% confidence limits of the mean. For
some of the points, these limits for the PPm values are within
the filled circle ChBFm = mean flux in choroidal red blood
cells; PPM, = mean perfusion pressure.
FIGURE
tion coefficients (r = 0.94, P < 0.01 for ChBVelm and
r = 0.86, P < 0.05 for ChBF m ). These fits were better
than linear fits. ChBVolm decreased linearly as a function of time ( r = — 0.93, P = 0.01). A significant negative correlation (r = 0.84, P < 0.05) was obtained
between ChBVol,,, and ChBVelm during squatting.
ChBVel,,, increased linearly (P < 0.02) as a function
of PP m , but the change in ChBVolm with PPm was not
significant. When squatting was stopped, ChBVelm returned rapidly to a value not significantly different
from that at baseline. It occurred before PPm reached
baseline.
Figure 3 shows the relationship between average
ChBFm and PPni, both expressed as a percentage of
baseline value, using data obtained during the full
duration of squatting, which in some subjects was up
to 3 minutes. It thus includes higher PPm values than
the graph of Figure 2. Seven or eight pairs of ChBF m PP,n data points were obtained in each eye, for a total
of 168 pairs of points. These were sorted according to
ascending values of PPm and divided into seven groups
of 24 pairs of values. For each group, mean and 95%
confidence interval of the ChBFm and PPm values were
calculated. ChBFm was significantly above baseline
value only at the highest average PPm reached (by
analysis of variance, P < 0.003). At this PP m , IOP was
17 ± 2 mm Hg, significandy above the baseline value
of 13 ± 1 mm Hg. Immediately after the end of the
exercise, it dropped to 11 ± 2 mm Hg.
We investigated the correlation between the
changes in the flow parameters in the right eye (OD)
and those in the left eye (OS). These changes were
evaluated in each subject during squatting at values
of PP m with increases above baseline differing by no
more than 4% between eyes (average difference 0.3%;
linear correlation coefficient between PPM1 (OD) and
PPm (OS) was r = 0.99). Furthermore, to use the same
number of data points in each subject, we considered
only the values of PPin < 60% above baseline. We
found no significant correlation between the changes
in each of the flow parameters in OS and those in
OD.
In Figures 4A and 4B, we plotted the time course
of the mean resistance, Rm = PP in /ChBF m during exercise and after the subjects stopped squatting, respectively. During squatting, Rm increased linearly with
time (r = 0.95, P < 0.01). After cessation of squatting,
Rm decreased rapidly and significandy (P < 0.01) to
baseline. A three-parameter exponential fit of the
form y = c + a-exp(-bt), starting immediately after
subjects stopped squatting, provided a time constant
of the return of ChBFm to baseline of 19 seconds.
During this time, PP m nearly reached baseline value.
Figure 5 shows that PQIBK decreased significantly (linear fit, r= 0.76, P < 0.01) when PPm increased during
squatting. Immediately after the subject stopped
squatting, PuChBK increased significantly above baseline (0.24 versus 0.21, paired Student's Hest, P < 0.05)
to return rapidly to a value not significantly different
from baseline. A plot of PuChBF versus pulsatility of
the systemic blood pressure, PuBP = (1—BP(|iasI/BPs>,s,),
measured during squatting and recovery from squatting, showed no significant correlation.
For the subjects used to obtain the data in Figure
3, the values of Sbi and Ssq for ChBVelm, ChBVol,,, and
ChBFm were 4%, 3%, and 4%, and 4%, 3%, and 6%,
respectively. For this calculation, we conservatively
used n = 11, although the lack of significant correla1.6
1.6
1.4
1.4
1.2
1.0
1.0
20
0.8
40
60
80
100 120
Time (sec)
0
40
80
120
160
Time (sec)
FIGURE 4. Change in average choroidal vascular resistance,
Rm, versus time (a) during squatting (start at t = 0 sec) and
(b) immediately after subjects stopped squatting (t = 0 sec).
The correlation coefficient of the linear fit: of Rm during
squatting is r = 0.95, P < 0.01). The linear correlation coefficient of Rm during recovery from squatting, calculated
from log(Rm — c) = loga — bt, where a, b, c are parameters,
is r = 0.96 (P< 0.01).
Downloaded From: http://iovs.arvojournals.org/pdfaccess.ashx?url=/data/journals/iovs/933419/ on 05/12/2017
Investigative Ophthalmology & Visual Science, October 1997, Vol. 38, No. 11
2342
0.30
0.25 -
0.20 -
U
0.15 -
0.10 -
0.05 -
0.00
40
60
70
80
90
PPm (mmHg)
FIGURE 5. Pulsatility PUCI,BF versus PPm during squatting. Correlation coefficient of linear fit r = 0.76 (P < 0.01). PPm =
mean perfusion pressure.
tion between the changes in ChBVelm, ChBVol and
ChBF,n during squatting in OS and OD would have
warranted using n = 22.
DISCUSSION
Results of previous work have demonstrated that during isometric exercise, the blood pressure in the brachial artery rises in parallel with that in the ophthalmic
artery and that the IOP does not change significandy.11 These findings, together with the results of
the current investigation (Fig. 2), indicate that the
maintenance of constant ChBFm, in spite of increased
perfusion pressure, is achieved through an increase
in choroidal vascular resistance (Fig. 4A).
The decrease in ChBVolm during squatting suggests that some of die increase in resistance takes place
in the volume sampled by the laser, which contains
mainly the choriocapillaris.12 To estimate it, we assumed that the change in ChBVolm was caused by
vasoconstxiction of the capillaries of the choroid and
that blood flows in these capillaries according to Poiseuille's law. In this case, die 6% reduction of ChBVolm
occurring during squatting corresponds to a 3%
change in vessel diameter, which would increase the
resistance by 12%. Although Poiseuille flow is unlikely
in these capillaries, this estimated value is well below
the ~70% increase needed to keep flow constant in
the presence of a 60% increase in PPm. Thus, the
changes in resistance during exercise and during recovery from squatting (Figs. 4A, 4B) must occur predominandy in the branches of the ophthalmic artery
feeding the foveal region of die choroidal circulation.
This interpretation of local action is supported by the
finding of a lack of correlation between PuChBF and
PuBp under these conditions.
Aim and Bill7'8 have revealed the protective role of
ocular sympathetic vasomotor nerves in acute arterial
hypertension in cats and monkeys. The investigation
of the effect of systolic arterial hypertension after ocular sympathectomy by Ernest15 has further emphasized
the role of the sympathetic nervous system in the vasoconstriction of die choroidal circulation in response
to arterial hypertension. Our results suggest a similar
regulatory mechanism in humans.
The highly significant increase in heart rate during squatting is expected, in that it is primarily responsible for die elevation in blood pressure.16 In previous
studies, Robinson etal,11 in three subjects, and Marcus
et al,17 in seven subjects, found no significant changes
in IOP during squatting. In the current study in 22
eyes, a 4-mm Hg increase in IOP was observed. This
significant change can be explained by die larger
number of eyes we studied and also the larger increase
in PPm we reached, compared with that seen in die
study of Marcus et al.17 The small increase in IOP and
the nonsignificant change in end-tidal Pco2 during
exercise1117 rule out the possibility that the blood flow
response to acute hypertension was related to changes
in IOP or Pco2.
The nearly constant ChBF, in spite of increases in
PPm up to «62%, does not represent an auto regulatory response in the classic sense, which consists of a
local change in the vascular resistance when the organ
has been isolated from systemic influence. To study
autoregulation in the choroid in response to raised
arterial pressure, the neural input to the choroidal
vessels would have to be removed.
Our measurements provide only information on
the hemodynamics in the foveal region of die fundus.
Whether die ChBF regulation during isometric exercise is as efficient in the peripheral region of die fundus remains to be investigated. A regional variation of
ChBF versus PPm cannot be excluded, because spatial
variations in the changes in choroidal Po2 and pH in
die subretinal space have been found in cats in response to step increases in IOP.1819
In this investigation, the laser-Doppler flowmetry
technique has been applied in normal volunteers. Because the probing laser beam is also the fixation target, the position of the laser beam at the fovea can be
maintained easily. The main task of the operator of
the equipment is to insure that the input pupil of
die laser-Doppler flowmetry optical system remains
approximately centered in the pupil of the eye measured. The continuous monitoring of the DC level of
die Doppler signal, which is proportional to the
amount of laser light reaching the detector, allows the
operator to insure that this is die case. We believe,
therefore, that measurements of ChBF in the region
of the fovea during isometric exercises can be applied
in studies in cooperative patients.
Downloaded From: http://iovs.arvojournals.org/pdfaccess.ashx?url=/data/journals/iovs/933419/ on 05/12/2017
2343
Choroidal Blood Flow
Key Words
choroidal blood flow, isometrics, laser Doppler flowmetry,
regulation, sympathetic nervous control
10.
Acknowledgments
The authors thank Nicole Michellod for help in preparing
the manuscript.
11.
References
1. Lind AR, Taylor SH, Humphreys PW, Kennelly BM,
Donald KW. The circulatory effects of sustained voluntary muscle contraction. Clin Sci. 1964;27:229-244.
2. Delius W, Hagbarth K-E, Hongell A, Wallin BG. Manoeuvers affecting sympathetic outflow in human
nerves. Acta Physiol Scand. 1972;84:82-94.
3. Mitchell JH, Schmidt RF. Cardiovascular reflex control by afferent fibers from skeletal muscle receptors.
In: Shepherd JT, Abboud FM, eds. Handbook of Physiology. Sec. 2, The Cardiovascular System. Vol 3. Bethesda,
MD: American Physiological Society; 1983:623-658.
4. Wesche J. The time course and magnitude of blood
flow changes in the human quadriceps muscles following isometric contraction. / Physiol (Lond). 1986;
337:445-462.
5. Taylor WF, Johnson JM, Kosiba WA, Kwan CM. Cutaneous vascular response to isometric handgrip exercise. fAppl Physiol. 1989;66:1586-1592.
6. Bystrom SEG, Kilbom A. Physiological response in the
forearm during and after isometric intermittent handgrip. Eur fAppl Physiol. 1990; 60:457-466.
7. Aim A, Bill A. The effect of stimulation of the sympathetic chain on retinal oxygen tension and uveal, retinal and cerebral blood flow in cats. Acta Physiol Scand.
1973;88:84-96.
8. Aim A. The effect of sympathetic stimulation on blood
flow through the uvea, retina, and optic nerve in monkeys. ExpEyeRes. 1977;25:19-25.
9. Bill A, Linder M, LinderJ. The protective role of ocular sympathetic vasomotor nerves in acute arterial hy-
12.
13.
pertension. Proceedings of the Ninth European Conference on Microcirculation. Antwerpen, Belgium,
1976. BiblAnat. 1977; 16:30-37.
Michelson G, Groh M, Griindler A. Regulation of ocular blood flow during increase of arterial blood pressure. Br fOphthalmol. 1994; 78:461-465.
Robinson F, Riva, CE, Grunwald JE, Petrig BL, Sinclair
SH. Retinal blood flow autoregulation in response to
an acute increase in blood pressure. Invest Ophthalmol
Vis Sci. 1986;27:722-726.
Riva CE, Cranstoun SD, Grunwald JE, Petrig BL. Choroidal blood flow in the foveal region of the human
ocular fundus. Invest Ophthalmol Vis Sci. 1994; 35:42734281.
Petrig BL, Riva CE. Optic nerve head laser Doppler
flowmetry: Principles and computer analysis. In: Kaiser HJ, Flammer J, Hendrickson P, eds. Ocular Blood
Flow. New Insights into the Pathogenesis of Occult Diseases,
1995. Basel, Switzerland: Karger; 1996:120-127.
14. Bonner RF, Nossal R. Principles of laser-Doppler
flowmetry. In: Shepherd AP, Oberg PA, eds. Developments in Cardiovascular Medicine: laser-Doppler Blood,
15.
16.
17.
18.
19.
Flowmetry. Boston: Kluwer Academic Publishers;
1990:73-92.
Ernest JT. The effect of systolic hypertension on rhesus monkey eyes after ocular sympathectomy. Am J
Ophthalmol 1977;84:341-344.
Shepherd JT, Blomqvist CG, Lind AR, Mitchell JH,
Saltin B. Static (isometric) exercise. Retrospection
and introspection. Circ Res. 1981;48(suppl):l79-188.
Marcus DP, Edelhauser HF, Maksud MG, Wiley RL.
Effects of sustained muscular contraction on human
intraocular pressure. Clin Sci Mol Med. 1974; 47:249257.
Yancey CM, Linsenmeier RA: Oxygen distribution and
consumption in the cat retina at increased intraocular
pressure. Invest Ophthalmol Vis Sci. 1989;30:600-611.
Yamamoto F, Steinberg RH. Effects of intraocular
pressure on pH outside rod photoreceptors in the cat
retina. ExpEyeRes. 1992;55:279-288.
Downloaded From: http://iovs.arvojournals.org/pdfaccess.ashx?url=/data/journals/iovs/933419/ on 05/12/2017