Capillary Filtration
in the Small Intestine of the Dog
By Paul C. Johnson, Ph.D., and Kenneth M. Hanson, Ph.D.
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ABSTRACT
The purpose of these studies was to determine the capillary filtration coefficient of the small intestine of anesthetized dogs by the gravimetric technique.
Capillary filtration was produced by elevating venous pressure. Filtration rate
increased as venous pressure was increased but the relation between the two
was not proportional. At venous pressures greater than 10 mm Hg, filtration
rate tended to reach a limit. As a consequence, the filtration coefficient decreased at higher pressures. Mean capillary pressure was estimated by the isogravimetric technique. When capillary pressure was 10 mm Hg, the filtration
coefficient averaged 0.37 ml/min per 100 g and decreased to 0.11 when capillary pressure was elevated to 20 mm Hg. The reduction in filtration coefficient
at high capillary pressures was apparently due to closure of precapillary sphincters.
ADDITIONAL KEY WORDS
capillary filtration coefficient
isogravimetric technique
intestinal capillary pressure
precapillary sphincters
peripheral circulation
capillary function
• The permeability of intestinal capillaries
appears to be greater than that of certain other
capillary beds. The protein concentration of
lymph flowing from the intestine is higher
than that from skeletal muscle and cervical
areas (1) and large molecules such as dextran and albumin cross the capillaries of the
intestine more readily than those of skeletal
muscle and brain (2). The filtration constant in individual capillaries of the frog mesentery (3) is about 20 times greater than that
calculated for mammalian skeletal muscle
(4). The present studies were undertaken to
obtain information on the intestinal capillaries
of a mammalian species by the gravimetric
technique previously employed by Pappen-
From the Department of Physiology, Indiana University School of Medicine, Indianapolis, Indiana.
This work was supported in part by a grant-in-aid
from the American Heart Association and by grants
(HE 05200-05 and AM 06221-03) from the U. S.
Public Health Service. Facilities provided in part by a
grant (H-6308) from the National Heart Institute,
U. S. Public Health Service.
A preliminary report of the work was given at the
XXII International Congress, International Union of
Physiological Sciences (Vol. II, 1962, p. 410 and Physiologist 7: 169, 1964).
Accepted for publication July 7, 1966.
766
heimer and Soto-Rivera (4) for capillary filtration studies in the hind limb.
Methods
Twenty dogs, anesthetized with 30 mg/kg sodium pentobarbital given intravenously, were used
in this study. The abdominal wall was opened
in the midline and a loop of small intestine was
exteriorized. The bowel was completely covered
with gauze, moistened widi physiological saline
solution and kept at 37°C with a heat lamp. A
segment of intestine having a single artery and
vein was selected, and the vessels were dissected
free from surrounding tissue for a length of 1 to 2
cm. Adjacent mesenteric tissue was doubly ligated and cut. Special care was taken to tie all
lymphatic vessels. No evidence was seen in any
experiment of lymphatic drainage from the vascular pedicle. The remainder of the mesentery
was cut with a cautery, small vessels being doubly
ligated before cutting. An incision was made in
each end of the intestinal segment, and a 4- to
5-cm length of Tygon tubing was inserted into
the lumen and tied in place. All tissue connections between the experimental preparation and
the remainder of the intestine were then severed.
The mesenteric artery and vein were both cannulated. Prior to cannulation the animal was given
a priming dose of 2.5 mg/kg heparin, intravenously, followed by a sustaining dose of 1 mg/
kg every 30 min. The arterial perfusion circuit
consisted of a length of polyethylene tubing with
a T-connector of Pleriglas interposed near the
Circulation Rtsircb, Vol. XIX, Oclottr 1966
767
INTESTINAL FILTRATION
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mesenteric artery. The side branch of the T was
connected to a Statham strain gauge and pressure
recorded on an Offner type R oscillograph. The
other end of the arterial circuit was inserted into
a femoral artery. Vascular reactivity of the intestine is best maintained if new polyethylene tubing
is used in each experiment (5), a precaution
which was followed here.
The venous circuit consisted of a polyethylene
cannula which was connected to JS-inch silicone
tubing. Polyethylene T-connectors were used in
the venous circuit for recording venous pressure
and for a venous pressure reservoir. The outflow
orifice of the venous circuit was placed above a
100-ml collecting reservoir connected to the jugular
vein. Adjustment of the orifice level enabled us
to set intestinal venous pressure at any desired
value. During the zero flow-isogravimetric procedure (6), venous pressure was adjusted with
the venous pressure reservoir mentioned above.
The intestinal loop was suspended from a
beam balance to record weight changes. To prevent dehydration, the intestinal segment was surrounded with a thin layer of moist gauze, covered
with a plastic wrap, and mounted in a plastic
box. The intestine was mounted in the box in an
inverted U fashion, supported by a polyethylenecovered wire inserted through the lumen. This
position assured free drainage of intestinal secretions or blood from the intestine. Several strips
of moistened gauze were attached to the ends of
the intestinal segment to facilitate fluid drainage.
The bottom of the box was open to permit free
drainage of secretions. In addition, the animal was
given 1 mg/kg propantheline bromide (Probanthine, Searle) to minimize intestinal secretion
and spontaneous peristaltic activity.
The beam balance from which the intestinal
loop was suspended was connected to a linear
variable differential transformer which sensed
changes in beam position as weight was altered (5). The sensitivity of the system was adjusted so that a weight change of 1 g corresponded to a deflection of 20 mm to 30 mm on the
oscillograph.
Blood flow was measured periodically at the
outflow orifice of the venous system with a graduated cylinder and stop watch. In some experiments flow was also measured with an orifice
flowmeter.
Measurement of Capillary Filtration. When
venous pressure is elevated, intestinal weight increases rapidly at first, but the rate of gain gradually diminishes as the weight reaches a new level
as shown in Figure 1. A typical example showing
the exponential gain of weight is shown in Figure
2. Two distinct logarithmic components are apparent, a rapid initial phase and a slow secondary phase. (See also ref. 7.) It has been shown
CircuUtkm Rti—rtb, Vol. XIX, Oaobir 1966
ARTERIAL
PRESSURE
(nun Hi)
"T
i
VEMOCS
PRESSURE
(nun H j ) f
_f\—3
INCREASE
T
SENsrnvmr
WEIGHT CHANGE
(Gran*)
l i
:T
BLOOD FLOW
(ml/mln/100 t )
FLOWMETER
TURNED OFF
40
10-
:
FIGURE 1
Record of intestinal weight change with sustained
elevation of venous pressure. Note that the rate of
weight increase gradually decreases until the weight
reaches a new equilibrium level. At the right side of
the figure is the record obtained during the isogravimetric procedure. Arterial and venous circuits are
occluded and the venous system is opened to a
reservoir. Venous pressure is adjusted by manipulation of the reservoir level until a constant weight is
obtained. Weight of intestinal loop = 56 g.
previously by measurement of arteriovenous protein differences (5) that the slow phase is due to
capillary filtration. The rapid phase appears to
represent increase of blood volume. It is probable
that reduction of filtration rate with time is due
to dilution of extravascular protein and reduction
of colloid osmotic pressure outside the capillaries (6).
We were most interested in determining the
filtration rate shortly after venous pressure elevation, when the rate is maximal. The magnitude of
the secondary weight change during the first 30
sec of venous pressure elevation was used for this
purpose. This value could be determined with
precision from a semilog plot of the weight
change (Fig. 2). Capillary filtration coefficient is
calculated as
filtration rate
change in capillary pressure
Measurement of Mean Capillary Pressure. We
have noted in previous studies (6) that the intestine will eventually attain a constant weight
at any venous pressure between 0 and 18 mm
Hg. Because of this feature, mean capillary pressure could be determined at a variety of venous
pressures by the zero flow-isogravimetric technique. This is a modification of the original isogravimetric technique described by Pappenheimer and Soto-Rivera (4). The original technique
JOHNSON, HANSON
768
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o.i
T I M E
I N
M I N U T E S
FIGURE
Semi-log plot of the.change in intestinal weight shown in Figure 1. Note the rapid and slow
phases of weight change. The initial 30-sec period of the slow phase is taken as the initial
filtration rate.
cannot be applied to the intestine directly because reduction of arterial pressure activates an
arteriovenous reflex in this vascular bed (5, 8).
To determine capillary pressure by the zero flowisogravimetric technique, arterial inflow and venous outflow of the isogravimetric intestine are
occluded simultaneously. Capillary pressure is
assumed to be equal to venous pressure at this
time, since flow is zero. Venous pressure is adjusted by a reservoir until a level is found at
which the weight stabilizes—which is taken to
be isogravimetric capillary pressure. A record
which illustrates the procedure is shown at the
right side of Figure 1. Details of the technique
have been described previously (6). For the
hind limb we have compared the zero flow technique and the original method described by Pappenheimer and Soto-Rivera and found that they
yield the same value for mean capillary pressure (9).
Experimental Procedure. Arterial and venous
pressure and weight were recorded continuously.
The zero reference level for arterial and venous
pressure was the center of mass of the intestinal
loop. The mean capillary pressure was measured
several times at 0 mm Hg venous pressure with
the zero flow-isogravimetric technique. Venous
pressure was elevated by an increment of 3 to
15 mm Hg and maintained until the weight became stable. This required 2 to 3 min at low
venous pressures and as much as 30 min at high
venous pressures. Blood flow was measured frequently during elevated venous pressure. When
weight was stable, capillary pressure was again
determined by the method described above. Venous pressure was returned to the zero level after
capillary pressure was determined.
Results
The relation between venous pressure and
initial filtration rate for 20 preparations is
shown in Figure 3. It is evident that the filtration rate of the intestinal capillaries depends on the magnitude of the increase in
pressure. However, it is also obvious that in
the intestine there is not a simple proportionality between these two factors. In most
intestinal loops the filtration rate approached
CinmUtio* Ru-rcb, Vol. XIX, Octcitr 1966
INTESTINAL FILTRATION
769
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10.0
5.0
15.0
P T (mm Hg)
FIGURE 3
Initial filtration rate as a function of venous pressure (Pv). Data are means of pooled results
from 20 preparations. Vertical lines represent ± ISD.
a maximum at higher venous pressures. (Figure 4, for example, shows a single preparation
in which this phenomenon was pronounced.)
In only 3 of the 20 preparations did we find
an apparent linear relation between filtration
rate and venous pressure, and in those preparations the filtration rate was below normal for the group, at all but the highest pressures.
Figure 5 illustrates the relation between
capillary pressure and calculated capillary filtration coefficient for all preparations. The
dependence of filtration coefficient upon capillary pressure as implied in Figure 3 is evident in a striking manner—decreasing from
an average of 0.37 at a capillary pressure of
10 mm Hg to 0.11 at 20 mm Hg. Measurements
were not made above 23 mm Hg capillary
pressure because the intestine did not become
isogravimetric in a reasonable period of time
(30 to 40 min) above this pressure.
Intestinal filtration rate tends to approach
a limit at higher venous pressure. Since the
filtration rate in the intestine is quite high,
the blood flow could be a limiting factor. It
is possible that because of the ease of water
movement across the capillary wall, plasma
CircuUtioo Rnmrcb, Vol. XIX, Oaoktr 1966
protein concentration and colloid osmotic pressure may increase in the capillaries. The importance of this factor may be appreciated
from Table 1, where plasma flow and initial filtration rate were used to calculate the increase in colloid osmotic pressure between
the arterial and venous ends of the capillary.
It is apparent that the magnitude of this increase is a substantial fraction (50 to 80%) of
the increase in capillary hydrostatic pressure.
However, it should also be noted that the
change in colloid osmotic pressure in the capillaries was proportionately greater with small
increases in hydrostatic pressure, ruling out
this factor as being responsible for the reduction in filtration coefficient at higher capillary
pressures. Nonetheless, the magnitude of this
factor is such that its effect on intestinal filtration cannot be ignored.
In calculating filtration coefficients for
Figure 4, it was assumed that the colloid osmotic pressure of the plasma remained constant. Since this is not so, it is obvious that
the apparent filtration coefficient which we
have calculated deviates considerably from
the true value. To correct the filtration coefficient for this effect, the mean increase in
770
JOHNSON, HANSON
"2 0.40 • -
8
SE
C
0.30 - -
E 0.20 • •
0.10
u
• •
1.501.25 •
P8
1.000.75/
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0.50"
0.250-
-
/
r
/
M
10
-
\
1
12
Pc
1
1
14
16
(mm Hg)
18
1
20
FIGURE 4
Initial filtration rate and filtration coefficient as a function of capillary presure (Pc). Note the
nonlinear relationship between capillary pressure and initial filtration rate. In most experiments,
initial filtration rate tended to reach a maximal value at higher capillary pressures. Data from
1 preparation.
colloid osmotic pressure must be determined.
If all capillaries were structurally similar,
with comparable hydrostatic pressures along
their length and comparable flow rates, it
would be possible to make some estimate
of the mean colloidal osmotic pressure in the
plasma from knowledge of the rate of filtration and arterial plasma protein concentration.
However, in recent studies of flow, in single
capillaries of the mesentery we have found
that flow velocities vary widely both temporally and spatially (Johnson and Wayland, unpublished results). Since it is possible that
such variations may occur in other portions
of the intestinal capillary bed as well, the
necessary assumption of uniformity is probably not satisfied.
Discussion
These studies show that the capillary filtration coefficient of the mammalian intestine
is considerably higher than that of skeletal
muscle (4). This finding is not surprising in
light of the relatively high permeability to
large molecules that these capillaries possess
(2). The true filtration coefficient must be
considerably higher than the apparent value
obtained in these studies, since we calculate
that the colloidal osmotic pressure increases
by as much as 85% of the increment in capillary pressure (Table 1).
Mayerson et al. (2) have studied permeability of capillaries in the intestine and the
cervical area to large lipid-insoluble molecules.
While quantitative comparison of permeabilities is difficult, the data indicate that labelled
serum albumin reaches its maximum concentration about seven times faster in the intestinal lymph than it does in the cervical
lymph. A parallelism between movement of
water and large molecules is evident, but the
mechanisms may be different. It has been
suggested (2, 10) that large lipid-insoluble
molecules may move across some capillary
membranes by a process of cytopempsis.
The capillaries of the intestine are known
to be structurally and functionally different
from those of certain other organs. Bennett
and co-workers (11) have found that intestinal capillary endothelial cells contain nuCircmUtiom Rilurcb,
Vol. XIX, Oclobtr
1966
INTESTINAL FILTRATION
771
0.60
0. 4 0 - -
0.35- •
0. 3 0 - •
0. J5- "
o.ao- -
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0.15" •
0.10--
0. 05 - •
0
8
10
12
14
16
18
CAPILLART PRESSURE (mm Hg)
20
FIGURE 5
Relation between capillary pressure and capillary filtration coefficient in 20 preparations. Open
circles represent average values.
TABLE 1
Effect of Increase in Mean Capillary Pressure (AP on Plasma Colloid Osmotic Pressure
at Venous End of Capillary
Group
i
u
IU
IV
V
(mm Hg)
FUtrltion
Rite
(ml/min per 100 g)
FUtrition
PUirru Flow
2.7
3.5
4.9
6.1
8.2
0.82
0.64
0.90
0.77
1.06
0.086
0.076
0.114
0.124
0.170
Eitimited
Rate
(mm Hg)
2.3
2.0
3.2
3.5
5.0
Data from 20 preparations divided into 5 groups according to magnitude of increase in
capillary pressure. The increase in plasma colloid osmotic pressure at the venous end of the
capillary is calculated from the ratio of filtration rate to plasma flow, assuming the capillary
filtrate is virtually protein free and that the relation between colloid osmotic pressure and
protein concentration is as given by Landis and Pappenheimer (18).
merous large fenestrations which they estimate
to be 300 A to 600 A in diameter. These
passages would permit movement of considerable quantities of whole plasma by bulk flow.
If this is the case, what structure constitutes
the filtration barrier? One possibility is the conCircuUtion Risetrcb, Vol. XIX, Octoitr 1966
tinuous basement membrane which surrounds
the capillary endothelium. The basement
membrane consists of a fine network of fibers
which could act as a sieve and restrict the
movements of protein across it.
The reduction in apparent filtration coeffi-
772
JOHNSON, HANSON
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cient at higher venous pressures must be a
consequence of the increased intravascular
pressure or of the filtration rate itself.
With respect to the latter possibility, there
are two mechanisms by which filtration rate
could be self-limiting. First, if sieving of
plasma protein occurs in the intestine during
filtration, the protein will exert a counter
pressure which opposesfiltration.This phenomenon has been investigated by Pappenheimer and asosciates (12) and by Renkin (13).
Renkin found, both theoretically and experimentally, that a hyperbolic relationship exists
between filtration rate and the degree of
sieving. From those studies it is apparent that
sieving would cause the curve relating filtration rate and venous pressure to be convex
to the pressure axis at low venous pressures.
At high venous pressures this curve would
approach a straight line which has a positive
intercept on the pressure axis. This is obviously
not the form of the curve which fits the data
(see Fig. 3).
Second, if the rate of filtration exceeded
the diffusion rate of protein in the interstitial
fluid, local changes in protein concentration
outside the capillary wall could occur. This
relationship may be expressed as:
C2 =
where, C2 is the interstitial protein concentration adjacent to the capillary wall,
C3 is the protein concentration in the
interstitial fluid pool,
v is filtration rate,
L is the diffusion distance,
and
D is free diffusion coefficient of protein in interstitial fluid.
If this effect influences filtration, it will also
take the form described above for the sieving
effect. Thus it appears that these two factors
are probably not the cause of the filtration
plateau.
The most likely remaining possibility is that
effective capillary surface area decreases. We
have previously shown (14) that resistance in
the precapillary segment of the vasculature
increases when venous pressure is elevated.
In recent studies (Johnson and Wayland, unpublished results), we have found that the
precapillary sphincters in the mesentery constrict when venous pressure is elevated. In
some capillaries this effect is so profound that
it causes complete stoppage of flow. Such an
effect could, in effect, reduce available capillary surface and limit filtration rate.
Mellander et al. observed a large reduction
in filtration coefficient in the foot when their
subjects were upright as compared with the
recumbent attitude (15). They attribute this
behavior to closure of precapillary sphincters.
This behavior of the capillary bed and its control elements represents a type of autoregulation, in this instance, of capillary filtration.
It is apparent from these studies that the
plasma colloid osmotic pressure in the intestinal capillaries may be greatly altered during
periods of filtration. The magnitude of this
effect obviously depends upon blood flow rate.
In our studies control blood flow was 20 to
30 ml/min per 100 g. In other studies it has
been reported to be 20 to 50 ml/min per 100
g (16). The effect of plasma protein changes
on filtration rate has been recognized as important in glomerular filtration, but it has generally not been considered in other vascular
beds. Correction for this effect would be
small in the case of skeletal muscle capillaries,
where the filtration rate appears to be, at most,
2 to 3* of the plasma flow (10).
Folkow et al. (17) have studied the effect of
isopropylarterenol on capillary filtration in the
cat intestine. They found that the capillary
filtration coefficient increased, reaching a
maximal value of 0.44 ml/min per mm Hg
per 100 g tissue (range 0.56 to 0.28) at the
highest flows (250 ml/min per 100 g per 100
mm Hg). Since their flow rates were very high,
one would expect that the vasculature, including the precapillary sphincters, would be
maximally dilated and all capillaries would be
perfused. Moreover, the change in colloid osmotic pressure with filtration at these flow
rates would be expected to be minimal.
However, there are several differences in
technique which would produce quantitative
differences in measured filtration rate. First,
CtrcuUtum Runrcb. Vol. XIX, Octottr 1966
773
INTESTINAL FILTRATION
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Folkow's preparation contained 25 to 35$ (by
volume) of lymph glands; these were excluded
from our preparation. Folkow found that the
filtration coeflBcient of these glands was only
0.02 to 0.04. Second, Folkow assumed that 85*
of the venous pressure change was transmitted
to the capillaries, whereas by experimentation
we have found that, on the average, only 62%
is transmitted (6). It should also be mentioned that Folkow used the slope of the slow
change (filtration) in the first minute, while
we have used the first 30 sec of this process.
Since the rate decreases exponentially, Folkow's values should be slightly less than our
own on this basis also. If Folkow's data are
computed on the same basis as our studies,
his average maximal value becomes 0.81
(range 1.03 to 0.52).
The control blood flow in Folkow's study
was 40 to 60 ml/min per 100 g, whereas
ours was approximately 20 to 30 ml/min per
100 g. Since in determining filtration coefficient
they elevated venous pressure by 7 to 10 mm
Hg, it may be safely assumed that at this high
blood flow the capillary pressure was 15 to
20 mm Hg. Computing their data on filtration
coefficient in the manner indicated above, we
obtain a value of about 0.22, which corresponds with our value of 0.10 to 0.18 in the
same capillary pressure range. This does not
take into account possible changes in plasma
protein concentration in the capillary in their
study. In view of the higher blood flow in the
denervated cat intestine, this effect would be
expected to be smaller than in our preparation.
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PAPPENHEIMER, J. R., AND SOTO-RIVERA, A.: Ef-
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Capillary Filtration in the Small Intestine of the Dog
PAUL C. JOHNSON and KENNETH M. HANSON
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Circ Res. 1966;19:766-773
doi: 10.1161/01.RES.19.4.766
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