| HOME | HELP | FEEDBACK | SUBSCRIPTIONS | ARCHIVE | SEARCH | TABLE OF CONTENTS |
|
|
|
|||||||
|
|||||||||
1 John B. Pierce Laboratory and Department of Epidemiology and Public Health, Yale University School of Medicine, New Haven, Connecticut 06519; and 2 National Aeronautics and Space Administration-Ames Research Center, Moffett Field, California 94035
 |
ABSTRACT |
|---|
Top
Abstract
Introduction
Methods
Results
Discussion
References
|
|---|
The impact of posture on the immediate recovery of intravascular fluid and protein after intense exercise was determined in 14 volunteers. Forces which govern fluid and protein movement in muscle interstitial fluid pressure (PISF), interstitial colloid osmotic pressure (COPi), and plasma colloid osmotic pressure (COPp) were measured before and after exercise in the supine or upright position. During exercise, plasma volume (PV) decreased by 5.7 ± 0.7 and 7.0 ± 0.5 ml/kg body weight in the supine and upright posture, respectively. During recovery, PV returned to its baseline value within 30 min regardless of posture. PV fell below this level by 60 and 120 min in the supine and upright posture, respectively (P < 0.05). Maintenance of PV in the upright position was associated with a decrease in systolic blood pressure, an increase in COPp (from 25 ± 1 to 27 ± 1 mmHg; P < 0.05), and an increase in PISF (from 5 ± 1 to 6 ± 2 mmHg), whereas COPi was unchanged. Increased PISF indicates that the hydrostatic pressure gradient favors fluid movement into the vascular space. However, retention of the recaptured fluid in the plasma is promoted only in the upright posture because of increased COPp.
colloid osmotic pressure; capillary exchange; fluid shift
| |
INTRODUCTION |
|---|
|
Top
Abstract
Introduction
Methods
Results
Discussion
References
|
|---|
AN IMPORTANT CIRCULATORY adjustment to exercise
training is the expansion of the intravascular fluid compartment (2).
Although exercise-induced hypervolemia has been a consistent finding in exercise training studies, the mechanism(s) responsible for this expansion remains unclear. We recently reported a 10-15% increase in plasma volume within 24 h after an acute, high-intensity exercise protocol (6). The increase in plasma volume was associated with an
increase in plasma albumin content, promoting increased water retention
in the intravascular compartment through its colloid osmotic properties
(7). In addition, a reduction in the sensitivity of cardiopulmonary
baroreflexes occurred within 2 h after exercise. This latter adaptation
plays a role in plasma volume expansion by allowing intravascular
volume to expand without evoking changes in fluid-regulating hormones
which would act to counter the volume expansion (7). Another important
observation was that plasma albumin content increased within 1 h after
intense exercise and that plasma volume was restored to control levels
despite a significant (
800-1,000 ml) deficit in
total body water. These studies clearly indicate an important role of
rapid translocation of fluid and protein, primarily albumin, in the
rapid recovery and eventual expansion of the intravascular compartment
after exercise.
In a more recent study, we reported that plasma volume expansion 24 h after intense exercise was associated with a reduction in the transcapillary escape rate of albumin which contributed to the increase in plasma albumin content (9). In addition, microcirculatory forces which govern transcapillary albumin flux in skeletal muscle were changed in a direction that supported reduced albumin efflux from the blood. However, we did not collect data during the early phase of plasma volume recovery (the first 2 h), when the rapid translocation of fluid and protein into the vascular compartment is critical to the restoration and maintenance of plasma volume after exercise. This phase of fluid balance after exercise is thought to be caused by the simple reabsorption of isotonic fluid from the interstitium (20), a process that is regulated by changes in the Starling forces across the capillary wall (1) and aided by the presence of an osmotic gradient from the extracellular to intracellular fluid compartment. The Starling forces include the hydrostatic and colloid osmotic pressure (COP) gradients (plasma vs. interstitium) across the capillary wall. One purpose of this study was to extend our earlier work in characterizing the changes in the Starling forces in skeletal muscle tissue that contribute to the rapid recovery of plasma volume after intense exercise.
In earlier experiments, a smaller translocation of protein and fluid into the vascular compartment was noted during recovery from exercise in the supine position (7) compared with the seated position (6). In addition, Ray et al. (17) reported that exercise training in the supine position, compared with training in the upright posture, did not result in a significant hypervolemia. The atrial natriuretic peptide (ANP) response to exercise is influenced by posture (16). Elevated ANP would act to limit water and protein retention within the vascular compartment (19), possibly modulating the impact of exercise on plasma volume expansion. These observations indicate that changes in tissue hydrostatic pressure gradients associated with different postures modulate the magnitude of exercise-stimulated protein and fluid transport after exercise. Based on this premise, we used posture as a tool to manipulate exercise-stimulated protein and fluid transport in an effort to describe the contribution of changes in the various Starling forces to the net transfer of fluid into the vascular space immediately after intense exercise.
| |
METHODS |
|---|
|
Top
Abstract
Introduction
Methods
Results
Discussion
References
|
|---|
Eighteen healthy adults (11 men, 7 women) volunteered to
participate in this study. Their physical characteristics were
as follows: age, 24 + 2 (SE) yr; body weight, 77 ± 4 kg; and
maximal aerobic capacity
(
O2 max)
in the upright posture, 41.2 ± 2.4 ml
O2 · min
1 · kg
body weight1. The basic
experimental protocol involved the measurement of fluid and protein
shifts between the interstitial and intravascular compartments during a
2-h recovery period after intense exercise in the upright or supine
posture. Fourteen subjects (8 men, 6 women) participated in the
exercise portion of these experiments and performed two identical
experiments. Each experiment was separated by at least 1 wk, and female
subjects were studied only during the early follicular phase of the
menstrual cycle (days 2-8). Four subjects (3 men, 1 woman) performed similar time control experiments in the upright and supine posture but did not perform any
exercise. The primary purpose of the time control trials was to
document the stability of the measurements over the time course of the
experiment. In all experiments, we controlled fluid, electrolyte, and
caloric intake 16 h before the start of each protocol and asked
subjects to refrain from vigorous physical activity for 24 h before
coming to the laboratory. Starting 15 h before testing, subjects ate
and drank only the food and beverages we provided (dinner: 5.9 MJ, 35 g
fat, 225 g carbohydrate, 48 g protein, 1,820 mg
Na+; breakfast: 1.6 MJ, 2 g fat,
87 g carbohydrate, 7 g protein, 200 mg
Na+), which included 1 liter of
water to drink the night before each testing day, with additional water
intake at home allowed ad libitum. The experimental
protocol was approved by the Yale University School of Medicine Human
Investigation Committee, and each subject was thoroughly acquainted
with all aspects of the experiment before informed, written consent was
obtained.
In the exercise group, we determined posture-specific
O2 max for each
subject on two separate days by using an incremental cycle-ergometer
protocol on an upright Monark cycle ergometer or an electrically braked
Collins cycle ergometer mounted for supine exercise. O2
consumption was calculated from continuous recordings of the fractions
of O2 and
CO2 in expired air and the expired
ventilatory minute volume and corrected to
STPD. Power requirement during the
subsequent exercise protocol was set to the power required to reach the
posture-specific respiratory compensation threshold. This averaged 85 ± 3% O2 max in
the upright and 86 ± 3%
O2 max in the supine
position. The exercise period consisted of eight bouts of exercise,
each lasting 4 min at the intensity described above. Each 4-min
exercise bout was separated by a 5-min recovery period during which the
subjects pedaled at a reduced workload.
The experimental design consisted of a 60-min posture-specific control
period, an exercise period which lasted 84 min, and 2 h of recovery
from exercise. Rest and recovery periods were performed at 27°C,
whereas the exercise protocol was performed at 20°C (<30%
relative humidity). Exercise was conducted at the lower ambient
temperature to minimize thermal strain. Although changing environmental
temperatures will affect changes in plasma volume, the 2-h recovery
period provided sufficient time for adjustment to the new thermal
environment. Time control experiments were identical, except that,
during the "exercise period," the subjects rested with their feet
on the cycle ergometer in the appropriate posture.
Measurements.
On arriving at the laboratory (7:00 AM) subjects ate a standard
breakfast and drank 10 ml/kg body weight of water within a 30-min
period. The subjects then voided their bladders, and urine was
collected over the next 1.5 h. At the end of this period, the subjects
were weighed; then they entered the test chamber to begin the
posture-specific control period. No fluid was ingested during the
remainder of the experimental protocol. Body weights were obtained and
urine was collected after the control period, after exercise, and after
the recovery period. Total urine volume was measured, and a 5-ml
aliquot was stored for analysis of electrolyte and creatinine
concentrations.
70°C for analysis of ANP and plasma renin activity (PRA).
Commercially available radioimmunoassay systems were used to determine
plasma concentrations of ANP and PRA (Incstar, Stillwater, MN). Intra-
and interassay coefficients of variation for ANP at 70.1 pg/ml were 6.4 and 7.0% and for PRA at 5.36 ng angiotensin
I · ml1 · h1
were 3.2 and 4.3%, respectively.
Interstitial fluid (ISF) pressure and composition were measured from
the vastus lateralis muscle of the quadriceps muscle group, from the
deltoid muscle of the shoulder, and from the subcutaneous tissue
overlying the muscle. These two muscle sites represented active (vastus
lateralis) and inactive (deltoid) muscle groups. Subjects were assigned
to a specific posture-muscle group in a modified Latin-squares design.
This design resulted in the following groupings: upright-leg,
n = 8; upright-arm,
n = 6; supine-leg, n = 8; supine-arm,
n = 6. ISF pressure measurements were
made continuously during control and recovery periods, whereas ISF samples were collected once during the control period and again during
the second hour of recovery from exercise.
ISF pressure in the subcutaneous tissue was measured by using a
fluid-filled wick catheter (15). The wick-catheter assembly was filled
with sterile saline and connected to a Statham P23DB pressure
transducer through a 15-cm-long PE-50 tube. These catheters were
inserted through the skin into the subcutaneous tissue at a 30°
angle with the use of a 16-gauge intravenous placement unit (Jelco
Labs, Raritan, NJ) after local anesthesia with lidocaine (1 ml, 1%
lidocaine). The reference level for zero pressure was set at the
catheter tip, and communication between the catheter and ISF was
verified by the response of the wick-catheter to light touch on the
skin. Noddeland et al. (15) reported duplicate measurements of ISF
pressure in thoracic subcutaneous tissue by using the wick-catheter
technique of 0.2 ± 0.2 and 0.6 ± 0.4 mmHg; these
values agree with measurements made by the wick-in-needle technique.
The ISF pressure in muscle was measured by using a slit catheter (8).
The catheter was placed by using sterile techniques under local
anesthesia (1 ml, 1% lidocaine). A 16-gauge intravenous placement
unit (Jelco Labs) was inserted, at a 45° angle from the plane of
the skin, through the skin and muscle fascia. The steel needle was
withdrawn into the plastic tube, and the plastic tube was then advanced
along the avenue of least resistance. The slit catheter was advanced
into the muscle via the plastic tube, which was then removed.
Verification of communication between catheter and ISF was determined
by light finger pressure over the catheter-placement site. In addition,
contraction of the muscle produced a significant rise in muscle tissue
pressure but no response in the subcutaneous tissue catheter. Time
control studies showed the measurement of ISF pressure
by wick and slit catheter to be stable for up to 3 h, with an average
SD of 0.48 mmHg and a between-subject variation of <9%. The tissue
pressure catheter was left in place during exercise. The failure rate
of tissue pressure measurements was 4% for subcutaneous and 14% for muscle measurements, respectively. Failure constituted either an
unstable baseline or extrusion of the catheter from the tissue space
(usually during exercise).
Samples of muscle ISF for determination of COP were collected by using
an empty wick-catheter technique. The wicks were wetted with a small
amount of sterile saline and placed in the muscle interstitium by a
technique similar to that described for the pressure-catheter
measurements. Periodic gentle massage of the tissue overlying the
catheter sites facilitated sample collection and 3-8 µl of
fluid was collected over the 60-min sampling period. Samples of >5
µl were used to measure COP directly; smaller samples were first
diluted and then used for measurement of interstitial COP
(COPi). COP was
determined for the diluted ISF sample and then converted to an
equivalent [alb] by using a COP-albumin standard curve. The
ISF sample-dilution factor was then applied to the [alb] to
obtain a corrected [alb], which was converted back to a
representative COP by using the same standard curve. [Alb]
was determined on all ISF samples, and interstitial [alb]
([alb]i) was directly corrected for the ISF sample-dilution factor. The failure
rate of this technique was 18%, which was caused by insufficient sample volume (7%) and bloody muscle ISF samples (11%). Samples contaminated with blood appeared red or dark pink and were not used for
analysis.
ISF samples from the subcutaneous tissue were collected by using an
implanted-wick technique (14). The implanted wicks were made of
three-strand nylon thread (Enkalon 3 × 3; Enka, Arnheim, The
Netherlands). The skin area was cleaned and shaved, and the site of
placement was anesthetized (0.3 ml per skin puncture site, 1%
lidocaine). The thread was laid double and sutured through the skin
with a straight needle (without cutting edges). The entire site was
covered with a sterile plastic film and left to absorb ISF for 60 min.
After sampling was completed, the wicks were removed and the wick fluid
was isolated by centrifugation. The failure rate because of
insufficient sample volume (10%) and contamination with red blood
cells (35%) was high and thereby prevented any substantive statistical
analysis of COPi in subcutaneous
tissue.
Measurements of plasma volume were made by using Evan's blue dye
(Ophthalmic Labs) dilution, and the transcapillary escape rate of
albumin (TERalb) was estimated
from the rate of decline in optical density (OD) at 620 nm
(OD620) of post-dye-injection plasma samples. Exact dye mass (~0.2 mg dye/kg body weight) was determined by syringe weight to ±0.0001 g. Time for the measurement started when the dye was injected and the venous catheter tubing and
injection syringe had been completely flushed of dye (3 min from the
start of injection). Immediately before dye injection, a blood sample
of 10 ml was taken. Post-dye-injection blood samples of 5.0 ml were
taken at 10, 20, and 30 min postinjection. The OD620 of plasma samples taken at
10, 20, and 30 min postinjection were plotted against time, and a
linear extrapolation to time 0 was
used to correct for the rate of albumin escape from the vasculature
(TERalb) and to estimate the
plasma volume at the end of the experiment. Changes in plasma volume
were determined from changes in Hct and Hb concentration
([Hb]) for the entire experiment and were used in
conjunction with the absolute plasma volume measurement at 120 min to
calculate plasma volume values at earlier time points. In general, the
rate of decline in OD during the 30-min sample period was linear and
could be extrapolated back to time 0 for determination of both plasma volume and
TERalb. The peak OD was usually
seen at the 10-min (27 of 36 measurements) or 20-min (5 of 36 measurements) sample. In cases (4 of 36) in which the rate of decline
of the OD curve was not stable, we were unable to make accurate
estimates of TERalb.
TERalb was calculated as the
percent decrease in OD620 from the
peak measurement through the 30-min sample. Test-retest reliability for
measurement of TERalb by Evan's
blue dye washout is 85% and for measurement of plasma volume by
Evan's blue dye dilution is 99% (9).
Systolic (SBP) and diastolic blood pressures (DBP) (in mmHg) and heart
rate (HR) were measured once every 5 min during control and recovery
periods by using an automatic blood pressure monitor (Colin STBP, model
685). During the exercise period, HR was also monitored every minute.
Mean arterial pressure (MAP) was calculated as
(2 · DBP + SBP)/3.
Statistics. General linear model procedures (PC-SAS, SAS Institute, Cary, NC) were used for data analysis. Variables differentiated by posture (i.e., blood pressure, blood samples, etc.) were compared using a two-way repeated measures ANOVA design. Data for ISF pressure and composition were analyzed by using a repeated-measures split-plot ANOVA design. The effect of posture at specific time points was determined by using post hoc analysis involving the Tukey method. Pearson's product-moment correlations assessed the relationship between TERalb and ANP levels. In two subjects, blood samples were not collected for hormone analysis; therefore, statistical analysis of the hormone data was limited to 12 exercise and 4 time control subjects. Confidence level for statistical significance was set at P < 0.05. All values are reported as means ± SE for 14 exercise and 4 time control subjects except where otherwise indicated.
| |
RESULTS |
|---|
|
Top
Abstract
Introduction
Methods
Results
Discussion
References
|
|---|
O2 max in the upright
posture averaged 41.2 ± 2.4 ml
O2 · min1 · kg
body weight1, which was
greater than the value in the supine posture (36.7 ± 2.2 ml
O2 · min1 · kg
body weight1;
P < 0.05). The relative exercise
intensity required to reach the respiratory compensation threshold was
similar for upright and supine exercise, averaging 85.1 ± 1.4 and
85.5 ± 0.7% of posture-specific O2 max, respectively.
During the latter portion of the exercise protocol, the exercise
intensity was lowered slightly in 4 of 14 subjects. On average, the
subjects maintained 97 ± 2 and 94 ± 3% of the expected
workload (164 ± 11 and 151 ± 10 W) and reached 97 ± 1 and
97 ± 2% of the predicted HR (168 ± 3 and 161 ± 4 beats/min) during upright and supine exercise, respectively. The
exercise period produced a decrease in total body water of 10.2 ± 1.1 and 10.7 ± 1.2 ml/kg body weight in the supine and upright
posture, respectively. During time control experiments, total body
water decreased by 4.7 ± 0.5 and 1.7 ± 0.3 ml/kg body weight in the supine and upright posture
(P < 0.05), respectively.
The influence of posture on SBP and HR at rest and during recovery from intense exercise is shown in Fig. 1. Under our experimental conditions, resting HR (64 ± 2 vs. 59 ± 2 beats/min), SBP (118 ± 3 vs. 111 ± 2 mmHg), and MAP (84 ± 2 vs. 78 ± 2 mmHg) were all higher in the upright compared with the supine posture (P < 0.05). During 120 min of recovery from intense exercise, there was a persistent elevation in HR regardless of posture (P < 0.05). SBP was reduced at 30 and 60 min of recovery from intense exercise in both postures (P < 0.05). SBP remained below control levels throughout the recovery period in the upright posture but returned to control levels by 90 min of recovery in the supine posture. DBP averaged 63 ± 2 and 67 ± 3 mmHg at rest in the supine and upright posture and remained at these levels during the recovery period.
|
Plasma volume at rest was higher in the supine (44.9 ± 1.9 ml/kg body weight) than upright (42.5 ± 1.7 ml/kg body weight) posture (P < 0.05). In time control experiments, plasma volume was quite stable and varied by <1% (range 0.4-0.9%) over the 3.5-h protocol. Figure 2 illustrates the influence of posture on the changes in plasma volume and COPp during intense exercise and during a 120-min recovery period. During exercise, plasma volume was reduced 5.7 ± 0.7 and 7.0 ± 0.5 ml/kg body weight in the supine and upright posture, respectively. During recovery, plasma volume returned to control levels within 30 min in both postures. In the upright posture, this restoration of plasma volume was maintained until 120 min of recovery, when plasma volume fell below control by 0.9 ± 0.4 ml/kg body weight. During supine recovery, plasma volume fell below control values at 60-120 min of recovery (P < 0.05). COPp was unaffected by posture at rest, averaging 25.2 ± 0.8 and 24.6 ± 0.5 mmHg in the upright and supine posture, respectively (Table 1). COPp remained elevated throughout 120 min of recovery from exercise in the upright posture (P < 0.05) but not after supine exercise (Fig. 2).
|
|
Plasma composition. The influence of posture on the composition of the plasma during recovery from intense exercise is shown in Fig. 3. Posture had no significant influence on the electrolyte or protein composition of plasma under resting conditions. The increase in plasma Na+ concentration ([Na+]) during exercise reflects the shift of hypotonic fluid out of the intravascular compartment. Plasma osmolality and plasma [Na+] were elevated during recovery (P < 0.05) regardless of posture. Plasma protein content increased after exercise in the upright posture and remained elevated throughout most of the 120-min recovery period (30, 60, and 120 min; P < 0.05). The change in plasma protein content during recovery from exercise was greater in the upright than in the supine posture (P < 0.05). Changes in plasma albumin content paralleled the changes in plasma protein content and account for >40% of the change in plasma protein content.
|
|
Microvascular forces.
Tables 1 and 2 show the impact of posture
on the microcirculatory forces which govern fluid movement between the
intravascular and interstitial compartments in previously active
skeletal muscle (vastus lateralis, Table 1), inactive skeletal muscle
(deltoid, Table 2), and the subcutaneous tissue overlying their
respective muscles. Tissue pressure in the vastus lateralis was higher
in the upright than in the supine posture (Table 1,
P < 0.05), whereas in the arm muscle
ISF pressure was unaffected by posture. After intense exercise, ISF
pressure in the previously active skeletal muscle was elevated
throughout the 120-min recovery period
(P < 0.05) regardless of posture. No
significant changes were seen in muscle
COPi after exercise (Table 1),
whereas COPp increased in the
upright posture (P < 0.05). Despite
the increase in COPp, the
calculated transcapillary COP difference
(COPp COPi) in muscle was similar
before (15.4 ± 1.4 and 19.0 ± 0.9 mmHg, upright and supine,
respectively) and after (16.9 ± 1.1 and 18.5 ± 1.4 mmHg,
upright and supine, respectively) exercise regardless of posture. The
[alb]i averaged 1.28 ± 0.29 g/dl in resting vastus lateralis muscle and was unchanged by
intense exercise (1.81 ± 0.25 g/dl). In the inactive arm muscle,
[alb]i
averaged 2.17 ± 0.92 and 2.04 ± 0.40 g/dl before and 120 min
after exercise, respectively. ISF pressure and
COPi measured from subcutaneous
tissue were similar at rest and during recovery from exercise, and the
values were not significantly influenced by posture (Tables 1 and 2).
There was a tendency for the transcapillary COP difference in
subcutaneous tissue to increase from 8.5 ± 2.9 to 13.4 ± 1.4 mmHg after exercise (P = 0.06) in the
supine posture. The
[alb]i in the
subcutaneous tissue was not influenced by posture and averaged 2.42 ± 0.38 and 2.56 ± 0.26 g/dl (pooled data) before and 120 min
after intense exercise, respectively.
|
|
| |
DISCUSSION |
|---|
|
Top
Abstract
Introduction
Methods
Results
Discussion
References
|
|---|
The rapid recapture of fluid into the vascular compartment after exercise is governed primarily by forces that determine transcapillary fluid movement. In the present study, plasma volume was rapidly restored to control levels after intense exercise, despite a total body water deficit of 10.1 ± 0.8 ml/kg body weight. The changes in transcapillary forces that contribute to this fluid recapture vary for individual tissues, muscle, and skin. In previously active skeletal muscle, the transcapillary COP difference is similar before and after exercise and does not contribute to the retention of fluid in the vascular space. However, a reduction in the transcapillary hydrostatic pressure gradient in skeletal muscle after exercise, indicated by a slight but significant increase in ISF pressure, favors the movement of fluid into the vascular space after exercise. The increase in ISF pressure would presumably promote increased lymphatic return of fluid and protein to the vascular space (1). Interstitial dilution or oncotic buffering (1, 18) in response to increased ISF pressure is a likely consequence; however, COPi and [alb]i were not reduced during the initial 120 min of fluid restoration after exercise. A dilution of COPi is observed 24 h after intense exercise (9). Although capillary hydrostatic pressure was not measured in our study, Michel and Phillips (11) demonstrated that, during a steady state, changes in capillary pressure are compensated for by changes in the composition of the transcapillary filtrate, thus preserving capillary pressure. Thus we anticipate that capillary pressure would not increase during recovery from exercise and that the balance of hydrostatic forces that govern fluid distribution in muscle would tend to favor fluid movement into the vascular space. This process is limited to previously active skeletal muscle and was not observed in the deltoid muscle after exercise. In subcutaneous tissue, there were no changes in ISF pressure, whereas the transcapillary COP difference was altered to favor fluid movement back into the vascular space (primarily because of increased COPp).
Plasma volume rapidly returns to control within 30 min regardless of posture and despite the 10 ml/kg body water deficit. This restoration of plasma volume must occur at the expense of the ISF and intracellular fluid volume. The ability to restore plasma volume selectively within the first 30 min is independent of body posture (Fig. 2). The most common observation within this time frame is a decrease in transcapillary hydrostatic pressure gradient (elevated ISF pressure) in previously active skeletal muscle. The retention of this recaptured fluid within the vascular compartment over the next 120 min is influenced by posture and is associated with protein (primarily albumin) retention in the blood. One consistent finding with previous studies (6, 7) is that the ability to maintain plasma albumin content promotes restoration of plasma volume. More recently, we have shown that an increase in plasma albumin content and plasma volume expansion after intense exercise is blunted in the supine posture (12). On the basis of these observations, we presume that even a small increase in COPp aids in restoring vascular volume by retaining water in the vascular space during recovery from upright exercise. At rest, tissue pressure in the vastus lateralis is higher in the upright than in the supine posture. The elevated tissue pressure is most likely the result of a postural-dependent contraction of these muscles. The increase in tissue pressure in previously active muscle presumably reflects an increase in ISF volume. During exercise, an increase in extracellular water (20) should lead to an increase in tissue pressure. We recently reported that capillary filtration of previously active muscle is increased 24 h postexercise. The increase in capillary filtration should contribute to an accumulation of fluid in the ISF compartment and an elevation in tissue pressure.
The role of ANP in modulating fluid movement between the vascular and interstitial spaces is documented in animal (22, 24) and human studies (13, 23). The mechanism of action of ANP on transcapillary movement of fluid may be via increasing capillary permeability (21, 23, 24) and/or by increasing the hydrostatic pressure gradient by changing pre- to postcapillary resistance (22). We recently demonstrated that, after intense exercise, TERalb is associated with plasma volume regulation (9) and that local transcapillary forces in the leg muscle favor retention of albumin in the vascular space. The data in Fig. 5 indicate that, at 2 h after intense exercise, TERalb varies as a function of posture and ANP level. Changes in posture will influence several parameters which mediate the movement of albumin across the capillary wall, including hydrostatic pressure gradients, capillary surface area for exchange, capillary permeability, and blood flow distribution between vascular beds with different permeability to albumin. The measurement of the plasma albumin escape rate reflects the weighted sum of tissue uptake for the entire vasculature. As such, the early portions of the washout curve (first 60 min) will be greatly biased by the perfusion of tissues with high albumin permeability (i.e., liver). The differences in TERalb associated with posture may reflect the impact of posture on blood flow distribution. Specifically, blood flow distribution away from the liver possibly reduces TERalb. The association of TERalb with ANP suggests that changes in albumin vascular permeability are influenced by circulating levels of ANP, as proposed by Renkin and Tucker (19). Alternatively, the association of TERalb and ANP may simply reflect the manner in which plasma ANP levels describe the magnitude of physiological disturbance associated with changes in orthostatic stress. In either case, the data are intriguing, because the higher TERalb in the upright posture occurs at a time when the vascular compartment is defending a slightly elevated protein and albumin content, suggesting that the change in TERalb is not critical for the maintenance of plasma volume during the early phase of fluid recapture.
Based on the available data, the process of exercise-induced hypervolemia can be described on the basis of acute and long-term adjustments. The acute adjustment, within the first 24-48 h, involves the selective expansion of plasma volume primarily due to an increase in intravascular albumin content (6, 7). On the long-term basis, the size of the intravascular compartment does not appear to be disproportionately larger than the increase in extracellular volume (10). Taken together, these data suggest that the overall adjustments in fluid compartment sizes take considerable time and that selective expansion of plasma volume has precedence in this procedure. During the acute phase, the increase in plasma albumin content occurs within 1-2 h of exercise and is subsequently maintained (6, 7, 12). The rapid increase in intravascular albumin content cannot be explained by changes in albumin metabolism (synthesis or degradation) or in albumin vascular permeability but must be ascribed primarily to a redistribution of albumin stores from interstitial to intravascular compartments.
However, the simple act of increasing intravascular albumin content cannot explain the plasma volume expansion at 24-48 h because direct infusion of 12 g of albumin into the vascular compartment of humans is entirely lost within 24 h (unpublished results). Thus other mechanisms must be brought into play that contribute to the retention of the additional intravascular albumin and fluid. One such mechanism is the reduction in TERalb (9). Our recently published data suggest that TERalb contributes to plasma volume regulation and that local transcapillary forces in the previously active skeletal muscle favor albumin retention in the vascular space at 24 h postexercise (9). Another mechanism is the attenuation of volume-regulating reflexes (3, 4, 7). This latter mechanism is characterized by an attenuated cardiopulmonary baroreflex control of peripheral vascular tone 2 h after exercise and the maintenance of fluid-regulating hormones such as renin and aldosterone. In combination, these mechanisms appear to play a role in exercise-induced hypervolemia by allowing the increase in fluid volume and albumin content to remain for extended periods. We have been able to block exercise-induced hypervolemia by having subjects perform exercise in the supine position; this also eliminated an increase in intravascular albumin content (12). In the present experiment, we examined the changes in microvascular forces that contribute to the regulation of both albumin and fluid movement between the intravascular and interstitial compartments during the initial 2 h of exercise-induced hypervolemia. These data provide evidence in support of a better plasma volume restoration after exercise in the upright than in the supine posture and support the view that the rapid recapture of fluid in the vascular compartment after exercise is driven primarily by changes in transcapillary hydrostatic forces. The retention of this rapidly recaptured fluid, however, appears to be the function of protein movement into the vascular compartment and an increase in COPp.
| |
ACKNOWLEDGEMENTS |
|---|
We thank Cheryl Kokoszka, Tamara S. Morocco, John R. Stofan, and Richard Wemple for technical support.
| |
FOOTNOTES |
|---|
This work was supported in part by National Aeronautics and Space Administration Grant NAGW-4056 and National Heart, Lung, and Blood Institute Grants HL-20634 and HL-39818. A. Haskell was a Howard Hughes Medical Institute Medical Student Research Training Fellow.
Address for reprint requests: G. W. Mack, John B. Pierce Laboratory, 290 Congress Ave., New Haven, CT 06519 (E-mail: mack{at}jbpierce.org).
Received 1 October 1997; accepted in final form 13 April 1998.
| |
REFERENCES |
|---|
|
Top
Abstract
Introduction
Methods
Results
Discussion
References
|
|---|
1.
Aukland, K.,
and
R. K. Reed.
Interstitial-lymphatic mechanisms in the control of extracellular fluid volume.
Physiol. Rev.
73:
1-78,
1993
2.
Convertino, V. A.,
P. J. Brock,
L. C. Keil,
E. M. Bernauer,
and
J. E. Greenleaf.
Exercise, training-induced hypervolemia: role of plasma albumin, renin, and vasopressin.
J. Appl. Physiol.
48:
665-669,
1980
3.
Convertino, V. A.,
L. C. Keil,
and
J. E. Greenleaf.
Plasma volume, renin, and vasopressin responses to graded exercise after training.
J. Appl. Physiol.
54:
508-514,
1983
4.
Convertino, V. A.,
G. W. Mack,
and
E. R. Nadel.
Elevated central venous pressure: a consequence of exercise training-induced hypervolemia?
Am. J. Physiol.
260 (Regulatory Integrative Comparative Physiol. 29):
R273-R277,
1991
5.
Dill, D. B.,
and
D. L. Costill.
Calculation of percentage change in volumes of blood, plasma, and red cells in dehydration.
J. Appl. Physiol.
37:
247-248,
1974
6.
Gillen, C. M.,
R. Lee,
G. W. Mack,
C. M. Tomaselli,
T. Nishiyasu,
and
E. R. Nadel.
Plasma volume expansion in humans after a single intense exercise protocol.
J. Appl. Physiol.
71:
1914-1920,
1991
7.
Gillen, C. M.,
T. Nishiyasu,
G. Langhans,
C. Weseman,
G. W. Mack,
and
E. R. Nadel.
Cardiovascular and renal function during exercise-induced blood volume expansion in humans.
J. Appl. Physiol.
76:
2602-2610,
1994
8.
Hargens, A. R.,
J. B. Cologne,
F. J. Menninger,
J. S. Hogan,
B. J. Tucker,
and
R. M. Peters.
Normal transcapillary pressures in human skeletal muscle and subcutaneous tissues.
Microvasc. Res.
22:
177-189,
1981[Medline].
9.
Haskell, A.,
E. R. Nadel,
N. S. Stachenfeld,
K. Nagashima,
and
G. W. Mack.
Transcapillary escape rate of albumin in humans during exercise induced hypervolemia.
J. Appl. Physiol.
83:
407-413,
1997
10.
Maw, G. J.,
I. L. MacKenzie,
D. A. M. Comer,
and
A. S. Taylor.
Whole-body hyperhydration in endurance-trained males determined using radionuclide dilution.
Med. Sci. Sports Exerc.
28:
1038-1044,
1996[Medline].
11.
Michel, C. C.,
and
M. E. Phillips.
Steady-state fluid filtration at different capillary pressures in perfused frog mesenteric capillaries.
J. Physiol. (Lond.)
388:
421-435,
1987
12.
Nagashima, K.,
A. Haskell,
T. Nishiyasu,
G. W. Mack,
G. W. Cline,
and
E. R. Nadel.
The effect of posture on exercise-induced hypervolemia (Abstract).
Physiologist
39:
A52,
1996.
13.
Nagashima, K.,
H. Nose,
T. Yoshida,
T. Kawabata,
Y. Oda,
A. Yorimoto,
O. Uemura,
and
T. Morimoto.
Relationship between atrial natriuretic peptide and plasma volume during graded exercise with water immersion.
J. Appl. Physiol.
78:
217-224,
1995
14.
Noddeland, H.
Colloid osmotic pressure of human subcutaneous interstitial fluid sampled by nylon wicks: evaluation of the method.
Scand. J. Clin. Lab. Invest.
42:
123-130,
1982[Medline].
15.
Noddeland, H.,
A. R. Hargens,
R. K. Reed,
and
K. Aukland.
Interstitial colloid osmotic and hydrostatic pressures in subcutaneous tissue of human thorax.
Microvasc. Res.
24:
104-113,
1982[Medline].
16.
Perrault, H.,
H. Cantlin,
G. Thibault,
G. R. Brisson,
and
M. Beland.
Plasma atrial natriuretic peptide during brief upright and supine exercise in humans.
J. Appl. Physiol.
66:
2159-2167,
1989
17.
Ray, C. A.,
K. J. Cureton,
and
H. G. Ouzts.
Postural specificity of cardiovascular adaptations to exercise training.
J. Appl. Physiol.
69:
2202-2208,
1990
18.
Reed, R. K.,
and
H. Wiig.
Compliance of the interstitial space in rats. I. Studies on hindlimb skeletal muscle.
Acta Physiol. Scand.
113:
297-305,
1981[Medline].
19.
Renkin, E. M.,
and
V. L. Tucker.
Atrial natriuretic peptide as a regulator of transvascular fluid balance.
News Physiol. Sci.
11:
138-143,
1996.
20.
Sejrsted, O. M., N. K. Vøllestad, and
J. I. Medbø. Muscle fluid and electrolyte balance
during and following exercise. Acta Physiol.
Scand. 128, Suppl.
556: 119-128, 1986.
21.
Sugimoto, E.,
K. Shigemi,
T. Okuno,
T. Yawata,
and
T. Morimoto.
Effect of ANP on circulating blood volume.
Am. J. Physiol.
257 (Regulatory Integrative Comp. Physiol. 26):
R127-R131,
1989
22.
Trippodo, N. C.,
F. E. Cole,
E. D. Frohlich,
and
A. A. MacPhee.
Atrial natriuretic peptide decreases circulatory capacitance in areflexic rats.
Circ. Res.
59:
291-296,
1986
23.
Wijeyaratne, C. N.,
and
P. J. A. Moult.
The effect of a human atrial natriuretic peptide on plasma volume and vascular permeability in normotensive subjects.
J. Clin. Endocrinol. Metab.
76:
343-346,
1993[Abstract].
24.
Zimmerman, R. S.,
N. C. Trippodo,
A. A. MacPhee,
A. J. Martinez,
and
R. W. Barbee.
High-dose atrial natriuretic factor enhances albumin escape from the systemic but not the pulmonary circulation.
Circ. Res.
67:
461-468,
1990
This article has been cited by other articles:
|
|
 |
|
  M. Ichinose, M. Saito, N. Fujii, T. Ogawa, K. Hayashi, N. Kondo, and T. Nishiyasu Modulation of the control of muscle sympathetic nerve activity during incremental leg cycling J. Physiol., June 1, 2008; 586(11): 2753 - 2766. [Abstract] [Full Text] [PDF]
|
|
|
|
 |
|
 V. H. Huxley, J. J. Wang, and I. H. Sarelius Adaptation of coronary microvascular exchange in arterioles and venules to exercise training and a role for sex in determining permeability responses Am J Physiol Heart Circ Physiol, August 1, 2007; 293(2): H1196 - H1205. [Abstract] [Full Text] [PDF]
|
|
|
|
 |
|
 T. W. Vogelsang, C. C. Yoshiga, M. Hojgaard, A. Kjaer, J. Warberg, N. H. Secher, and S. Volianitis The plasma atrial natriuretic peptide response to arm and leg exercise in humans: effect of posture Exp Physiol, July 1, 2006; 91(4): 765 - 771. [Abstract] [Full Text] [PDF]
|
|
|
|
 |
|
 J. J. Van Lieshout, W. Wieling, J. M. Karemaker, and N. H. Secher Syncope, cerebral perfusion, and oxygenation J Appl Physiol, March 1, 2003; 94(3): 833 - 848. [Abstract] [Full Text] [PDF]
|
|
|
|
|
|
J. Wu and G. W. Mack Effect of lymphatic outflow pressure on lymphatic albumin transport in humans J Appl Physiol, September 1, 2001; 91(3): 1223 - 1228. [Abstract] [Full Text] [PDF]
|
|
|
|
|
|
K. Nagashima, J. Wu, S. A. Kavouras, and G. W. Mack Increased renal tubular sodium reabsorption during exercise-induced hypervolemia in humans J Appl Physiol, September 1, 2001; 91(3): 1229 - 1236. [Abstract] [Full Text] [PDF]
|
|
| ||||||||||||||||||||||||||||||||||||||||||||||||||||||||||||||||||||
| HOME | HELP | FEEDBACK | SUBSCRIPTIONS | ARCHIVE | SEARCH | TABLE OF CONTENTS |
| Visit Other APS Journals Online |
different from Con,
P < 0.05.
) in plasma volume and plasma
colloid osmotic pressure (COPp)
during and after intense exercise. Values are mean ± SE;
n = 14 subjects. * Different
from zero, P < 0.05;
