Clinical Science and Molecular Medicine (1976) 51, 583-588.
Distribution of blood flow in the hypothermic (27°C) dog kidney
W. R. WITHEY, B. J . CHAPMAN
AND
K. A. MUNDAY
Department of Physiology and Biochemistry, Medical and Biological Sciences Building, Southampton, U.K.
(Received 30 April 1916)
SummarV
1. Renal function was measured in seven norm0
thermic (38°C) and seven hypothermic (27°C) dogs.
2. The glomerular filtration rate was 60% lower
in the hypothermic animals, and the renal blood
flow was 51% lower. The intrarenal distribution of
blood flow was measured by the uptake of 06Rb
from the blood into different regions of the kidney.
Hypothermia reduced flow by 34% in the outer
cortex, 72% in the inner cortex, 61% in the outer
medulla and 69% in the inner medulla.
3. Radioautography indicated a high blood flow
to an area of the outer medulla of hypothermic
kidneys, which may indicate medullary blood flow
‘shunting’.
4. The results have been discussed in relation to a
number of clinical and experimental observations.
Key words: hypothermia, intrarenal distribution of
blood flow, renal blood flow.
Introduction
A r e d u d body temperature is often encountered
in paediatric and geriatric medicine, in cases of
exposure and in surgery, where organs may be
Or
under hypothemi‘
conditions.
many Of the PhYsiol0gica1
changes induced by hypothermia and the
changes in normal homeostatic function are not well
understood.
Comspondence: Dr B. J. Chapman, Department of
Physiology and Biochemistry, Medical and Biological
Sciences Building, Bassett Crescent East, Southampton
SO9 3TU, U.K.
One such change is the decrease in renal blood
flow. Many factors may contribute to this reduction,
including an increase in blood viscosity (Bickford &
Winton, 1937), haemoconcentration (Kanter, 1968)
and a decrease in mean arterial blood pressure
(Blatteis & Horvath, 1958). However, the major
factor is a cold-induced vasoconstriction (Levy,
1959; Withey, Chapman & Munday, 1975).
Withey et al. (1975) suggested that the vasoconstriction may occur unequally in different regions
of the kidney. Such a phenomenon could explain
such observations as the ability of the hypothermic
kidney to autoregulate normally (Chapman, Withey
& Munday, 1975b), the diuresis and natriuresis of
hypothermia (Johns & Munday, 1967) and the
increase in medullary hypertonicity which occurs
during cooling (Park, Han, Kim & Hong, 1968). To
study further this possibility of a changed pattern
of blood flow in hypothermia the intrarenal distribution of blood flow was studied in anaesthetized
dogs cooled to 27°C.
Methods
A total of fourteen male and female dogs weighing
6.5-18 kg were prepared by use of the methods
described by Withey et al. (1975). The animals
were anaesthetized with just sufficient intravenous
sodium pentobarbitone to suppress the corneal
reflex and to prevent shivering during hypothemia.
Cannulae were inserted into the right cephalic vein
and superficial branches of the right femoral artery
and vein. This latter cannula was^ manipulated into
the left renal vein through an incision in the
domen. A Biotronex BLlOO electromagnetic blood5 83
584
W. R. Withey, B. J. Chapman and K. A . Munhy
flow transducer and pneumatic blood-vessel occluder
were placed on the left renal artery. After every
renal blood flow reading, the zero-flow flowmeter
deflection was determined by briefly occluding the
renal artery. After every experiment the flowmeter
was calibrated in vitro, at 38°C and at 2 7 T , by
using the renal artery and blood taken from the
experimental animal. Urine was collected separately
from the right and left ureters. Tyrode’s solution,
containing p-aminohippurate and creatinine, was
infused at a rate of 15 ml h-I kg-‘ to measure the
renal clearances of these substances. All wounds
were sutured and covered with adhesive tape. An
equilibration period of 3 h was allowed before
further experimentation. Core temperature was
measured by an electronic thermometer with a
probe placed in the oesophagus at the level of the
heart. The temperature of the seven normothermic
(control) animals was maintained at 38”C, but the
temperature of the seven hypothermic (experimental)
animals was reduced, by surface cooling with crushed
ice, to 27°C. In all other respects the two groups of
animals received identical treatments. Renal function
(urine flow, clearance of creatinine and p-aminohippurate, and renal blood flow) and cardiovascular
function (arterial and renal venous pressures and
heart rate) were then monitored for four consecutive 30 min periods in both groups of animals.
Qualitative and quantitative assessments of the
intrarenal blood flow were obtained by a modification of the method of Harsing & Bartha (1966),
which depends upon the quantitative uptake into
the kidney of intravenously injected 86Rb. This
method is based upon the principle that the amount
of 86Rb taken up by tissues is proportional to the
fraction of the cardiac output perfusing those tissues
in both normothermic and hypothermic animals.
The validity of results obtained by the method in
normothermic kidneys has been clearly demonstrated by a number of workers (Steiner & King,
1970; Deutsch & Dreichlinger, 1963; Girndt &
Ochwadt, 1969). The validation depends on the
measurement of renal arterial-venous differences of
86Rb, the time-course of 06Rb uptake and on
comparison with other methods that depend on
different principles. Similarly there is also considerable evidence that lowering the body temperature
does not impair the accuracy of this method (Willson,
Chapman & Munday, 1976; Bullard & Funkhouser,
1962).
Ten minutes after the final clearance period, 50
pCi of 06RbCI solution in sodium chloride solution
(150 mmol/l; saline) was rapidly injected into the
cephalic vein and flushed in with 1 ml of saline. After
1 min both renal arteries and veins were clamped
and the kidneys removed. These were rapidly
frozen at -30°C and subsequently sectioned by
hand into longitudinal slices about 2 mm thick.
The right and left kidneys were then treated separately.
Radioautographs of the right kidney were prepared by exposing the frozen sections to X-ray
film (Kodak Blue Brand double-coated) for 72-96
h. After development, the density of the images on
the radioautograms indicate the relative magnitude
of blood flow in the different regions of the kidney.
Quantitative measurements of the intrarenal blood
flow were obtained as follows. The frozen slices
from the left kidney were dissected into five discrete
visible morphological regions, namely capsule with
peri- and intra-renal fat, outer cortex, inner cortex,
outer medulla and inner medulla, and were placed
in tared scintillation vials. Several vials were used
for each region so that a number of independent
assessments of the radioactivity in each region
were obtained. Mixtures from the boundaries
between any two regions were placed in a separate
series of tared vials. Furthermore the inner medulla
was divided into three portions: the region nearest
the outer medulla, an intermediate region and the
tip of the papilla. The tissues were dried at 100-1 10°C
for 72-96 h (to constant weight) and then dissolved
in two or three successive 1 ml aliquots of concentrated nitric acid with gentle warming. Successive
small additions of concentrated hydrochloric acid
were made until the solution ceased to turn brown.
This was necessary because the nitrates discoloured
the solution and caused quenching of the photon
output. Radioactivity was counted in a Beckman
scintillation counter at room temperature by the
Cerenkov effect of the 1.99 MeV beta particles from
86Rbcounted on a 32Pisoset (Elrick &Parker, 1968).
The overall efficiency of counting in every vial was
assessed by adding an internal “Rb standard
solution and re-counting the vials. The total radiation
counted was volume-independent, provided that
the sample volume was within the range 5-15 ml.
After the measurement of the 86Rb content per
unit weight of each region, it was possible to
apportion algebraically each mixture into its component regions, as follows. If W , = weight of a
mixture, C, = c.p.m. of 06Rb/g of the mixture,
585
Bloodflow in the hypothermic k i h y
WA = weight of region A in the mixture (unknown),
CA = c.p.m./g of region A, WB = weight of region
B in the mixture (unknown) and CB = c.p.m./g
of region B, then
W M . CU =
and
WA' c A + wB*
CB
WM =
wA+wB.
Hence
It was then possible to find WBand the amount of
radioactivity due to each region making up the
mixture. It was also possible to do this apportioning
on the basis of small, but consistent, differences in
the water contents of the regions.
Thus the total amount of radioactivity and the
total wet and dry weights of each region were
obtained. Regional blood flows were calculated
from the total amounts of isotope in each region of
the kidney and the total renal blood flow was
measured by the electromagnetic blood flowmeter.
The advantages of this method are that it can be
used in conditions in which renal function may be
changing, and furthermore the location of the isotope
within the kidney can be confirmed by radioautography.
Results
Table 1 shows cardiovascular and renal function
in the two groups of animals. The changes are
typical of those found in the hypothermic dog.
The 51% decrease in renal blood flow occurred in
the absence of the haemoconcentrationwhich usually
accompanies hypothermia ; plasma protein concentration was unchanged and packed cell volume
decreased slightly (see Withey ef ul., 1975). pAminohippurate and creatinine clearances decreased
by 61% and 60% respectively. The data in Table 1
also show that the functions of the right and left
kidneys were very similar.
Qualitative assessments of regional blood flows
from the right kidney were obtained by radioautography (Fig. 1). In the kidneys of normothermic animals (Fig. 1A) there was a homogeneous
blood flow throughout the cortex. However, in the
hypothermic animals (Fig. 1B) the flow was no
longer homogeneous but was markedly reduced in
that part of the cortex nearest the medulla. Blood
flow was also reduced in all parts of the medulla
except for a narrow region close to the cortex. These
changes were consistently recorded in the kidneys
of all the hypothermic animals used in these studies.
Quantitative data obtained from the left kidneys
confirm these qualitative results (Table 2). In normo
TABLE
1. Cardiovascular and renal function of normorhermic and hypothermic abgs
Results are expressed as the meanf SEM of the pooled data from the four clearance periods of the seven dogs in each
group. Statistical evaluation was by Student's t-test. NS = not significant; PAH = p-aminohippurate.
Normothermic
BrOUP
Statistical
evaluation of
difference
between groups (P)
Hypothermic
BrOUP
~~
Body temperature ("C)
Mean arterial blood pressure (mmHg)
Left renal venous pressure (mmHg)
Heart rate (beatslmin)
Packed cell volume (%)
Plasma protein concn. (dl00 ml)
Urine flow
Left kidney
Right kidney
(pl min-l kg body wt.-l)
CPAH
Left kidney
Right kidney
(ml min-I kg body wt.-')
Ccrc.ua1oo
Left kidney
Right kidney
(ml min-' kg body wt.-')
Extraction ratio PAH (%)
Lea kidney
Renal blood flow
(ml min-' kg body wt.-')
38.2k0.2
126f8
8+ 1
151+7
47.5f 0.1
4.7f 0.2
57.1f 8.4
57-8fl.8 NS
274f 0-2
96+ 6
8f2
70f 5
45.6f 0.3
4.1+0*1
41*0+7.5
34.2f9.1 NS
2.8f0.3 NS
28f0.2
1
< 0.001
< 0.001
NS
< 0001
< 0.05
NS
< 0.001
~ : ~ ~ ~ : ~< / ~ ~
3.0f 0.2
27+ 0 2
77* 1
17*4+2*1
1.2f0.1
1.3f0.1
68+2
8*5+1.0
0001
< 0.001
NS
<0*001
< 0.01
W . R. Withey,B. J . Chapman and K. A . Munday
586
TAELE
2. Regional bloodflows in kidneys of normothermic and hypothermic dogs
Data are the mean results k SEM from seven animals in each group. Statistical evaluation
was by Student's t-test. The SE of the ratios was calculated with the method described by
Colquhoun (1971).
Blood flow
(ml min-' g-' of tissue)
Outer cortex
Inner cortex
Outer medulla
Inner medulla
Average
Outermost
Intermediate
Tip of papilla
Statistical
evaluation (P)
Ratio
hypotherrnicl
normotherrnic
5.7f 1.3
2.6k0.3
3,0+ 0.6
NS
<0.01
< 0.02
0.66+ 0 17
0.28+ 0.06
1.4fO.2
1.7f0.3
< 0.01
< 0.02
< 0.001
< 0.01
0.3 I f 0.07
0.28+ 0.08
0.33 f 0.08
0.31+0.09
Normothermic
group
Hypothermic
group
8.7k 1.2
9.4f 1.8
7.6k 1.5
4.5k0.8
6.0t 1.4
4.3 k 0.4
3.2f 0.6
thermic animals the blood flows per gram wet
weight of tissue of the inner and outer regions of the
cortex were very similar. In the hypothermic animals,
however, blood flow through the outer region of the
cortex was reduced by 34% and in the inner region
it was reduced by 72%.
The 86Rb content of the inner medulla showed a
gradient, being highest nearer the outer medulla
and lowest at the tip of the papilla. Similar (nearly
twofold) gradients existed in both normothermic
and hypothermic kidneys, and may represent a
gradation of blood flow across the medulla or may
indicate that 86Rbis excluded from the inner regions
of the medulla by transfer of isotope from descending to ascending vasa recta by the countercurrent
flows through these vessels, although there are
reasons for discounting this latter possibility (Deutsch
& Dreichlinger, 1963; Steiner & King, 1970).
The measurements of the 86Rb content of the
outer medulla are consistent with the radioautographic evidence that this region of the renal
vasculature was not influenced by hypothermia to
the same extent as the inner cortex and inner
medulla. Comparison of the radioautographs with
the tissue slices from which they were produced
shows that this effect was restricted to the region
of outer medulla closest to the inner cortex.
Discussion
The 34% reduction in blood flow through the outer
cortical timue is similar to the change that would be
1.4t0.3
1.0k0.2
0.39f0.11
expected if renal blood flow was subject to only the
22% increase in viscosity which occurs when blood
is cooled from 38" to 27°C. Although it is possible
that the outer cortex behaves in this passive way,
other mechanisms are clearly involved in the much
larger blood-flow changes in other parts of the renal
vasculature. Indeed, it is evident from previous
work that the reduction in total renal blood flow
which occurs during hypothermia cannot be accounted for by the temperature-dependent increase
in blood viscosity, by the hypothermic haemoconcentration (Withey et af., 1975), nor by the
reduction in mean arterial blood pressure (Chapman
et a/., 1975a), and it has been inferred (Withey et a/.,
1975) that there is a cold-induced vasoconstrictor
response in the kidney. The present results support
this conclusion by showing that vasoconstriction
occurs selectively in the inner cortex and inner
medulla.
Similar renal blood flow changes have been
obtained in the hypothermic rat (Chapman, Munday,
Willson & Withey, 1975a). Outer cortical blood
flow is reduced by 40%, and inner cortical and
medullary blood flows decrease by 64-67%. However, the region of relatively high blood flow in
the outer medulla was not observed after 30 min
hypothermia in the rat. Its occurrence in the dog
kidney may be related to a species difference, the
saline diuresis induced by the rapid intravenous
infusion, or the much longer duration of hypothermia.
A relatively high blood flow in the outer medulla
Blood flow in the hypothermic kidney
0
1uter
medulla
Outer
medulla
Inner
medulla
Inner
medulla
Out:er and inner
cortex
Inner
cortex
Outer
cortex
FIG. I . Radioautographs showing the distribution of 86Rb in kidney slices. (A) Kidney removed from normothermic dog (38°C); (B) kidney from hypothermic dog (27°C).
(Facing p . 586)
Bloodflow in the hypotherrnic kidney
or juxtamedullary cortex has been reported in a
number of species under many experimental conditions (see review by Fourman & Moffat, 1971).
These authors suggested that capillary vessels can
be widely distensible and can act as rapid transit
pathways from artery to vein. This ‘shunting’ of
blood commonly occurs when there is intense,
prolonged renal vasoconstriction (Trueta, Barclay,
Daniel, Franklin & Richard, 1947; Gomori, Nagy,
Zolnai, Jakab & Meszaros, 1965; Hinshaw, Bradley
& Carlson, 1959) and ‘shunting’ has also been
observed in artificially perfused rat kidneys (Chap
man, 1970). Under other experimental conditions
similar changes have been ascribed to osmotic
dilatation of blood vessels (Elpers & Selkurt, 1963)
and to regional differences in intrarenal pressure
(Selkurt, 1963).
It is interesting to consider how regional alterations in blood flow may influence the function of
the hypothermic kidney. The kidneys of dogs at
27°C are able to autoregulate their blood flow in
spite of the vasoconstrictionin the renal vasculature
(Chapman et al., 1975a). The present results suggest
a basis for this property in that normal autoregulation occurs in the outer cortical region,
although blood-flow changes in the remaining
regions are dominated by the cold-induced vasoconstriction. Autoregulation of renal blood flow
does not occur below 18°C (Harth, Lutz & Kreienberg, 1960; Waugh & Shanks, 1960), presumably
owing to an inability of the vascular smooth muscle
to contract at these low temperatures. This is
consistent with the observation of Smith (1952),
who found that cooling initially causes constriction,
but further cooling leads to dilatation of isolated
blood vessels.
This suggestion, that very low temperatures
cause relaxation of vascular smooth muscle, may
account for the observations of Miller, Alexander
&Nathan (1972) and Small, Bell, Filo & Woodward
(1973), who found no vasoconstriction in the inner
cortex of kidneys cooled to 10”and 15°Crespectively.
However, this difference may be due in part to the
fact that both groups of workers used isolated
kidneys perfused with cell-free serum. Furthermore,
they did not furnish data concerning control,
normothermic tissue which strictly would be necessary in order to provide a better comparison between
these and the present results.
Hypothemia is commonly associated with natriuresis and diuresis (Johns & Munday, 1967), and
E*
587
even when these do not occur the salt and water
excretion rates are much greater than would be
expected to accompany the marked reductions in
glomerular filtration rate and renal blood flow.
Hypothermia inhibits the active processes responsible
for reabsorption of salt (thus tending to increase
the urinary excretion of salt and water) but also
reduces glomerular filtration rate (tending to depress
salt and water excretion). However, the reduction
in renal blood flow (and presumably also glomerular filtration rate) is shown to occur largely at
the inner cortex, while renal blood flow (and
glomerular filtration rate) is maintained at relatively high values in the outer cortex where
nephrons are known to excrete a high proportion
of the filtered Na+ and water (De Rouffignac &
Bonvalet, 1974; Barger & Herd, 1971). Thus the
localization of the cold-induced renal vasoconstriction contributes to the high rates of salt and
water excretion.
These results also confirm a suggestion of Park
et al. (1968). These workers observed an increase
in medullary hypertonicity in hypothermia and
suggested that a reduction in medullary blood flow
could cause this by reducing the rate of solute
removal.
Willson et al. (1976) have commented that the
changes in tissue blood flows which occur in hypothermia are similar to those seen when the circulatory system adapts to stressful conditions. With
most stresses urine flow, glomerular filtration rate
and renal blood flow are reduced (thus tending
to maintain blood volume and allow diversion of
nutrient blood flow to more important tissues).
Such responses are seen in only the inner cortex and
medulla of the hypothermic dog kidney, but they
may be very important in neonates where the outer
renal cortex (which does not respond to hypothermia)
is undeveloped (Kleinman & Reuter, 1973) and
where the thermoregulatory mechanisms are also
undeveloped so that hypothermia is more likely to
occur.
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