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The John B. Pierce Laboratory and Departments of Epidemiology and Public Health and of Cellular and Molecular Physiology, Yale University School of Medicine, New Haven, Connecticut 06519
ABSTRACT
INTRODUCTION
METHODS
RESULTS
DISCUSSION
ACKNOWLEDGEMENTS
FOOTNOTES
REFERENCES
ABSTRACT 
Haskell, Andrew, Ethan R. Nadel, Nina S. Stachenfeld, Kei
Nagashima, and Gary W. Mack. Transcapillary escape rate of albumin
in humans during exercise-induced hypervolemia. J. Appl. Physiol. 83(2): 407-413, 1997.
To test the
hypotheses that plasma volume (PV) expansion 24 h after intense
exercise is associated with reduced transcapillary escape rate of
albumin (TERalb) and that local
changes in transcapillary forces in the previously active tissues favor
retention of protein in the vascular space, we measured PV,
TERalb, plasma colloid osmotic
pressure (COPp), interstitial
fluid hydrostatic pressure (Pi), and colloid osmotic pressure in leg
muscle and skin and capillary filtration coefficient (CFC) in the arm
and leg in seven men and women before and 24 h after intense upright
cycle ergometer exercise. Exercise expanded PV by 6.4% at 24 h (43.9 ± 0.8 to 46.8 ± 1.2 ml/kg, P < 0.05) and decreased total protein concentration (6.5 ± 0.1 to
6.3 ± 0.1 g/dl, P < 0.05) and
COPp (26.1 ± 0.8 to 24.3 ± 0.9 mmHg, P < 0.05), although plasma
albumin concentration was unchanged. TERalb tended to decline (8.4 ± 0.5 to 6.5 ± 0.7%/h, P = 0.11) and was correlated with the increase in PV
(r = 
0.69,
P < 0.05). CFC increased in the leg
(3.2 ± 0.2 to 4.3 ± 0.5 µl · 100 g
1 · min1 · mmHg1,
P < 0.05), and Pi showed a trend to
increase in the leg muscle (2.8 ± 0.7 to 3.8 ± 0.3 mmHg, P = 0.08). These data
demonstrate that TERalb is
associated with PV regulation and that local transcapillary forces
in the leg muscle may favor retention of albumin in the vascular space
after exercise.
capillary filtration coefficient; Evans blue dye; interstitial
fluid colloid osmotic pressure; interstitial fluid hydrostatic
pressure; plasma volume
INTRODUCTION PLASMA VOLUME (PV) expansion is a well-described
consequence of endurance exercise training (5-7). Plasma albumin
content expansion has been hypothesized to facilitate PV expansion
through albumin's colloid osmotic properties (5, 6). Convertino et al.
(5) demonstrated a progressive expansion of plasma albumin content
during 3 days of endurance exercise training, whereas Gillen et al. (6,
7) showed that albumin content expands by 1 h after exercise to the
level it maintains for the next 40 h. An expansion of plasma albumin
content without preceding exercise, however, does not lead to prolonged
PV expansion (31). Therefore, conditions must favor the retention or
restitution of albumin in the vascular space for up to 40 h after
exercise.
Mechanisms that regulate plasma albumin content are the transcapillary
escape rate of albumin (TERalb),
lymphatic albumin return, and the albumin synthesis-to-degradation
ratio. TERalb measures the whole
body rate at which albumin leaves the vascular space. It is controlled
by macrovascular and microvascular factors including plasma albumin
concentration, plasma atrial natriuretic peptide (ANP) concentration,
capillary filtration coefficient (CFC), capillary hydrostatic pressure,
interstitial fluid hydrostatic pressure (Pi), interstitial fluid
colloid osmotic pressure (COPi), and interstitial fluid albumin concentration
([Alb]i) (2, 16, 24,
25, 30, 31, 34). Pi and the transcapillary colloid osmotic pressure
gradient are increased in previously active muscle within 14 min after
intense exercise (16), but these microcirculatory forces remain to be
characterized 24 h after exercise.
The purpose of this study was to investigate the contribution of
reduced TERalb to the general
process of exercise-induced hypervolemia. In addition, we characterized
the local microcirculatory forces, in the previously active muscle and
overlying skin, that govern albumin flux with the purpose of
correlating these forces with changes in
TERalb. We hypothesized that PV
expansion 24 h after exercise would be associated with a decrease in
TERalb. We further hypothesized
that Pi would increase and COPi
would decrease in the previously active muscle.
METHODS
O2 max)
on an upright bicycle ergometer.
O2 max ranged from 33.0 to 56.6 ml · kg1 · min1
with a mean of 42.4 ± 2.3 ml · kg1 · min1.
CFC was measured in the left forearm and leg by using venous occlusion plethysmography by relating the rate of change in limb girth to measured venous pressure on the assumption that increase in limb girth after cessation of venous filling is attributable to capillary fluid extravasation (10, 11, 29). Cuff pressures of 20 mmHg for 7 min, 30 mmHg for 8 min, and 40 mmHg for 9 min were applied, thereby allowing for 4 min of data contributable to fluid extravasation after cessation of vascular filling (29). The sequence was repeated, and the order of cuff pressure application during each sequence was randomized. Mercury in Silastic strain gauges (Parks Medical Electronics) were applied over the left forearm and calf at the estimated point of maximal circumference and tensioned to 20 g. Strain-gauge calibration was performed on a hard plastic cylinder of approximately the same diameter as the subject's limb. Occlusion cuffs were placed around the left arm and thigh and covered with metal restraining bands. Care was taken to avoid influencing circulation to the limbs with the deflated cuffs. Venous pressure was measured by attaching left forearm and leg indwelling venous catheters (18 g; Jelco) to pressure transducers (P23XL, Visso-Spectramed), which were positioned such that zero pressure corresponded to the height of the respective catheter tip. Pressure transducers were calibrated by using a water-filled manometer. The left arm was hung with a foam sling around the hand, and with support at the elbow, so that the forearm was horizontal and at heart level without disturbing the strain gauge. The leg was similarly supported at the knee and ankle. Recordings of venous pressure and strain-gauge length were recorded twice per second by computer. Pi was measured in the right vastus lateralis muscle and overlying subcutaneous tissue by using the slit catheter and wick catheter techniques, respectively (1, 2, 18, 21). These techniques measure hydrostatic pressure in free interstitial fluid at the end of a fluid-filled column connected to a pressure transducer (2, 18). Noddeland et al. (18) demonstrated duplicate measurements in thoracic subcutaneous tissue in eight and seven humans by using the wick catheter technique, resulting in mean Pi of
0.2 ± 0.2 and
0.6 ± 0.4 [not significant (NS)], which agree
well with simultaneous measurements made by the wick-in-needle
technique. Rapid dynamic measurement of Pi has been made by slit
catheter in the human leg muscle and subcutaneous tissue during lower
body negative pressure (1). Time control studies on four human subjects
in our laboratory show the measurement of Pi by wick and slit catheter to be stable for up to 3 h with average standard deviation over time of
0.48 mmHg and between-subject variation of <9%. Under sterile
conditions and local anesthesia (
0.6 ml 1% lidocaine/site), 16-gauge catheter insertion units (Jelco) were inserted into the appropriate tissue spaces and the plastic sheaths were advanced 1-2 cm. The metal needles were removed from the sheaths, and the slit catheter and wick catheter, filled with sterile saline, were advanced into the muscle and subcutaneous tissue, respectively. The
plastic sheaths were removed over the slit and wick catheter tubing,
the catheters were held in place with a clear plastic dressing
(Tegaderm, 3M), and the free ends were connected to pressure transducers (P23XL, Visso-Spectramed) positioned such that zero pressure corresponded to the height of the respective catheter tips.
Proper catheter placement was verified by lightly tapping over the
catheter tip (skin response) and by having the subject contract the
anterior thigh muscles (muscle response). Catheters with poor dynamic
response or that failed to show the appropriate response for their
compartment were replaced. Slit catheters were made by cutting six 2-mm
longitudinal slits into one end of a 30-cm length of PE-50 tubing
(Becton-Dickenson) and attaching a 23-g Luer stub adapter
(Becton-Dickenson). Wick catheters were made by pulling ~5 mm of
doubled 3-0 polyester fiber (Johnson & Johnson) with 6-0
polypropylene monofilament (Johnson & Johnson) into a 30-cm length of
PE-50 tubing and attaching a 23-g Luer stub adapter.
Interstitial fluid samples for measurement of
COPi and
[Alb]i were collected
from the right vastus lateralis muscle and overlying subcutaneous
tissue by using the empty wick catheter technique (2, 8, 18).
COPi measured after direct
collection of interstitial fluid by this technique is comparable to
that measured by interstitial fluid sampling by implanted nylon wicks
and by an implanted colloid osmometer with a mean standard deviation of
1.7 mmHg, although variables such as amount of negative pressure and
sample collection time must be controlled (18). Increasing amounts of
negative pressure applied to the sample collection catheter decrease
measured COPi, although the
decrease is unlikely to be significant at pressures <10 mmHg (18).
Catheter insertion units were placed into the appropriate tissue space
as described above. Empty wick catheters were dipped into sterile
saline and shaken to remove excess saline before insertion. Less than
10 mmHg of negative pressure applied to the skin wick catheter and
periodic gentle massage of the skin overlying the catheter sites
facilitated sample collection (2, 18). Interstitial fluid samples were
grossly bloody in 2 of 18 muscle samples and in 4 of 18 skin samples.
Data from these samples were excluded from the calculation
of mean COPi and
[Alb]i in both control
and postexercise, leaving seven and five complete data sets in the leg
muscle and skin, respectively.
Measurements of TERalb and PV were
made by using Evans blue dye (Ophthalmic Labs) washout and dilution,
respectively. Exact dye mass (~0.05 mg dye/kg) was determined by
syringe weight to ±0.0001 g (Mettler). Time for the
TERalb 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 20-ml blood sample was
taken from the left forearm indwelling venous catheter used for venous
pressure measurement. Post-dye injection blood samples of 2.5 ml were
taken every 5 min for 1 h. This provided 8 min between dye injection
and the first blood sample, allowing single-compartment analysis of
TERalb (3). Test-retest
reliability for measurement of
TERalb by Evans blue dye washout
is 85% and for measurement of PV by Evans blue dye dilution is 99%.
TERalb measured by blue dye is
comparable to that measured by
131I-labeled albumin (22).
Exercise day.
After initial hydration and a 90-min upright seated rest period, the
subjects underwent eight bouts of upright bicycle exercise lasting 4 min at 85% of their
O2 max, with 5-min
rest periods between bouts. After exercise, subjects rested seated
upright for 2 h, after which they drank a volume of water equal to the estimated water loss calculated by change in body weight.
Analyses.
Interstitial fluid samples were diluted with 0.9% NaCl to achieve a
volume of ~13 µl, with exact interstitial fluid sample dilution
factors determined by weighing the samples before and after dilution to
±0.0001 g. Mean interstitial fluid sample sizes at control and 24 h
postexercise were 4.5 ± 1.4 and 3.4 ± 0.6 µl (NS) for muscle
and 1.7 ± 0.4 and 2.5 ± 0.5 µl (NS) for subcutaneous tissue,
respectively. COPi was measured by
using a sample volume of 10 µl with a small volume membrane colloid
osmometer with pore restriction of 30,000 Da (PM30, Amicon).
[Alb]i was measured by bromcresol purple (Sigma Chemical).
A small aliquot of each blood sample was used for immediate
determination in quadruplicate of hematocrit and total protein concentration by microhematocrit and refractometry, respectively. Hemoglobin was measured in the predye sample by cyanomethemoglobin (Boehringer Mannheim). Five milliliters of the predye blood was aliquoted into an EDTA tube with aprotinin, whereas the remaining blood
was aliquoted into potassium-heparin tubes, and all tubes were spun for
15 min at 1,500 g at 4°C. Plasma
was aliquoted for immediate determination of
[Alb]p
colorimetrically with a bromcresol purple reaction (Sigma Chemical),
plasma osmolality by freezing-point depression (Advanced Instruments),
COPp by using a small-volume membrane colloid osmometer with pore restriction of 30,000 Da, and
Evans blue dye concentration by spectrophotometry at 620 nm. Plasma was
frozen at 70°C for later determination of ANP by
radioimmunoassay (INCSTAR; intra-assay coefficient of
variation of 2.6% for midrange standards) by utilizing
one kit for all samples.
Calculations.
CFC was calculated as below
|
|
is the ratio of post- to precapillary resistance, taken to be
constant at 0.16 (10), and 
is change.
COPi was determined for the
diluted interstitial fluid samples and converted to an equivalent
concentration of albumin by using a COP-albumin standard curve. The
interstitial fluid sample dilution factor was applied to this albumin
concentration to obtain a corrected albumin concentration, which was
converted back to COP.
[Alb]i was directly
corrected for the interstitial fluid sample dilution factor.
TERalb was calculated from the
initial slope of the exponential curve fit through the optical density
of post-dye injection plasma samples at 620 nm. PV was calculated from
the known mass of dye injected and an estimate of the initial plasma
concentration of dye taken from the extrapolated exponential curve.
Percent change in PV was also calculated by using hematocrit and
hemoglobin (3). Plasma protein and osmolar content were calculated by multiplying the corresponding concentration by PV. PV, protein, and
osmolar contents are reported as the respective value divided by
control body weight.
Statistics.
Comparisons between control and postexercise data were analyzed by
using a paired t-test. Pearson's
product-moment correlations assessed the relationship between
TERalb and PV.
Confidence level for statistical significance was set at
P < 0.05. All values are reported as
means ± SE.
RESULTS
PV = 0.54 · TERalb + 1.8; r = 0.69,
P < 0.05) (Fig.
3). PV expansion was associated with a
dilution of slowly changing plasma and blood constituents, including a decrease in hematocrit of 4.3%, plasma total protein concentration of
3.1%, and COPp of 6.9%. However,
[Alb]p was unchanged,
so albumin content showed a trend to increase by 5.9% (Fig. 2).
COPp decreased by 1.8 ± 0.7 mmHg (Fig. 4), whereas plasma osmolality
increased by 1.9 ± 0.8 mosmol/kgH2O. Plasma ANP
concentration was unchanged between control and postexercise. Measured
cardiovascular parameters were similar between control and
postexercise. Control and postexercise heart rates were 65 ± 4 and
62 ± 2 beats/min, respectively, systolic blood pressures were 117 ± 3 and 118 ± 3 mmHg, respectively, and diastolic blood
pressures were 67 ± 1 and 68 ± 2 mmHg, respectively.
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, Means; error bars, SE.
) in
TERalb and in both PV
(A) and plasma albumin content
(B). Values are individual
measurements for 9 subjects.
,
Means; error bars, SE.
Microvascular parameters. Measured microvascular data from control and 24 h postexercise are listed in Table 2. CFC increased by 34% in the leg at 24 h postexercise (Fig. 4), whereas CFC in the arm was unchanged. Pi in the leg muscle showed a trend to rise after intense exercise by 1.1 ± 0.5 mmHg (Fig. 4). No change was observed in Pi in the skin, or COPi in either the muscle or skin. [Alb]i showed a small but significant increase in the leg muscle of 0.6 ± 0.2 g/dl, with no change in the skin.
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DISCUSSION
Plasma albumin content expansion during hypervolemia and the role of albumin as the major contributor to COPp have led to the hypothesis that albumin content expansion is a driving force for PV expansion (5, 6). We induced a PV expansion of 6.4% with a trend for albumin content expansion of 5.9%. Convertino et al. (5) demonstrated a serial increase in plasma albumin content with little change in globulin content during 8 days of exercise training. Gillen et al. (6, 7) showed that albumin content expands by 1 h and remains expanded for up to 40 h after exercise.
This study represents the first attempt to simultaneously measure the TERalb and microcirculatory variables during PV expansion in humans. A significant new finding of this study is the association between decreased TERalb and PV expansion. A similar negative correlation between TERalb and PV has been demonstrated during hypervolemia induced by plasmapheresis in rats (36). While these results may suggest that TERalb contributes to PV expansion after exercise, an equally plausible interpretation is that PV regulates TERalb or that a third common factor contributes to both PV expansion and decrease of TERalb. In addition, the association is not strong. Some subjects displayed PV expansion without change in TERalb, suggesting that multiple overlapping mechanisms contribute to postexercise PV and albumin content expansion.
One such mechanism may be increased lymphatic return of albumin, with a subsequent redistribution of interstitial fluid albumin to the vascular space. To estimate protein movement, we converted TERalb to grams albumin per kilogram per hour, which yielded an 18% decrease in whole body transcapillary albumin flux after exercise. If TERalb were decreased to this degree for any length of time, whole body lymphatic return of albumin would also have to decrease to account for the measured change in plasma albumin content. However, lymphatic return of albumin from the leg is likely unchanged or increased because CFC and Pi were increased (2). Prenodal lymphatic albumin return in the leg has been shown to increase immediately after exercise, although not for 24 h (20). This implies that a decrease in whole body lymphatic albumin return would be due to a change in transcapillary forces elsewhere in the body. For example, alterations in blood flow to the splanchnic region may account for this discrepancy, owing to its large capacity for fluid and protein movement (9, 26). However, plasmapheresis in anesthetized rabbits increases extravascular uptake of labeled protein, suggesting that increased lymph flow accounts for restoration of plasma albumin content (35), and increased lymph flow after plasmapheresis in sheep contributes to the maintenance of [Alb]]p despite depleted whole body albumin stores (23). No study we know of has measured both TERalb and lymph flow simultaneously.
Additionally, continued upregulation of protein synthesis or downregulation of protein degradation could affect albumin content expansion after exercise. Factors affecting albumin synthetic rate include hormone balance, nutrition state, and systemic stresses (27). Colloid osmotic pressure also plays an important role in both the synthesis and degradation of plasma albumin (27). Infusion of colloids other than albumin results in decreased albumin synthesis, and infusion of excess albumin results in increased albumin degradation. The mechanisms of colloid osmotic regulation of albumin are unknown (27). An attenuation of volume-regulating mechanisms after exercise (7) could allow the plasma to become hyposmotic, effectively signaling the liver to increase albumin production. However, albumin synthesis has been shown not to increase after moderate aerobic exercise (4). In addition, chronic infusion of albumin resulting in hyperproteinemia in splenectomized dogs did not result in expanded blood volume despite an increase in plasma protein concentration, an increase in total extracellular fluid volume, and an increase in COPp (14). This may be because increased interstitial fluid protein concentration balances the increase in plasma protein concentration and maintains the capillary colloid osmotic pressure gradient, implying that increased synthesis of albumin would not lead to increased blood volume unless the albumin could be preferentially retained in the vascular space. Further studies are needed to assess the role of albumin synthesis after intense exercise.
The increase in CFC in the leg, and the decrease in COPp, both stimulate transcapillary fluid flux (2, 26). Changes in CFC may represent changes in total capillary surface area and/or capillary hydraulic conductivity. Alternatively, changes in measured CFC may reflect artifacts resulting from the large cuff pressures used to measure CFC. These pressures may activate smooth muscle constriction and/or alter capillary exchange (13). However, CFC also increases in maximally dilated rat hindquarters (30) after 6-10 wk of exercise training, a condition that eliminates the effect of vascular smooth muscle constriction, as well as during fluid loading in dogs (11) and in humans exposed to lower body negative pressure (12).
Increased transcapillary fluid filtration resulting from increased CFC and decreased COPp is expected to be offset by changes in Pi and COPi, thereby preventing edema in the legs (2). Indeed, Pi in the leg muscle tended to increase after exercise in seven of nine subjects. Pi has been shown to remain elevated in human leg muscle for at least 15 min after 3 min of intense exercise (16). Our data extend these findings to 24 h after exercise. COPi was expected to decrease after exercise, given an anticipated interstitial fluid albumin wash down (26); however, we measured no change in the leg skin or muscle. Similarly, COPi has been shown to remain unchanged in the neck muscle and subcutaneous tissue during head-down tilt despite facial edema (21).
Our estimates of microcirculatory forces that control muscle transcapillary albumin flux during exercise-induced hypervolemia change in a direction that supports reduced transcapillary albumin flux. The two-pore model of transcapillary solute transport describes convective and diffusive albumin flux through large and small pores. Under resting conditions, large pores account for ~80% of transcapillary albumin clearance, which is entirely convective and controlled by transcapillary hydrostatic pressure gradients (26). The remaining 20% of transcapillary albumin clearance is through small pores and is predominantly diffusive (26). In the present study, Pi tended to increase, which would limit convective albumin flux through large pores. Although capillary hydrostatic pressure was not measured in our study, Michel et al. (15) demonstrated that, during steady state, changes in capillary pressure are compensated for by changes in the composition of the transcapillary filtrate, thus preserving capillary pressure. Additionally, because [Alb]i increased in the leg muscle with constant [Alb]p, the diffusive component of small-pore albumin clearance should decrease. On the other hand, the small but significant increase in [Alb]i in the leg muscle may reflect an increase in small-pore convective albumin flux resulting from increased CFC and decreased COPp because typical small pores allow passage of albumin but not immunoglobulins or fibrinogen (26). However, the small-pore convective component of transcapillary albumin transport represents <5% of total albumin clearance (26).
To summarize, we have measured TERalb and transcapillary forces in the leg muscle and skin before and 24 h after intense exercise in humans. Increased leg CFC and decreased COPp are compensated for by a tendency for increased muscle Pi and increased muscle [Alb]i. Thus the transcapillary clearance of albumin in previously active muscle may be decreased. Additionally, TERalb shows a trend to decrease after exercise and is negatively correlated with PV expansion.
ACKNOWLEDGEMENTS
We thank Cheryl Kokoszka, Tamara S. Morocco, John R. Stofan, and Richard Wemple for technical support.
FOOTNOTES
Address for reprint requests: G. W. Mack, The John B. Pierce Laboratory, Yale University School of Medicine, 290 Congress Ave., New Haven, CT 06519 (E-mail: mack{at}biomed.med.yale.edu).
Received 16 December 1996; accepted in final form 2 April 1997.
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