Professional Documents
Culture Documents
To inflating unit
Fig. 1. Diagram of apparatus. The foot is inside a thin rubber sock (broken line). C, occlusion
cuff; V, volume recorder; S, syringe for calibrating; P, centrifugal pump; H.C]., heating or
cooling unit with heater connected to thermostat, T.
The subject lay supine on a couch with the foot and ankle as far as the upper part of the malleoli
inside the plethysmograph. A sock of thin ( h in.) rubber loosely ensheathed the foot, and a water-
tight seal was obtained by stretehing the top of the sock over a dam at the ankle. There was no
pressure by the sock on the foot, and it was assumed that blood flow was not altered by this
process. The plethysmograph was of Perspex, with internal dimensions of 29 x 15 x 14 cm, and
a capacity of 61. It was filled with water at the required temperature kept constant by an
external heating/cooling system. A centrifugal pump circulated the water at 9 L/min, thus
ensuring adequate stirring. The back of the heel was supported by a sponge rubber pad, so that
the weight of the leg was not borne by the dam. An occlusionl cuff of 4 cm diameter was used,
placed with its lower edge about 2* cm from the dam to lessen the cuff artifact. Volume changes in
the plethysmograph were transmitted to a float recorder with a frontal writing point recording on
a kymograph (Fig. 1). At the end of an experiment the apparatus was calibrated by injecting
measured volumes of water into the plethysmograph, with the arterial flow to the foot occluded.
The calibration was non-linear, as was shown by Landowne &G Katz (1942), being a rectilinear
projection from a curvilinear system. The maxrimum error was 3% each side of the mean calibra-
tion value for the arc of traverse of the recording lever used.
FOOT BLOOD FLOW AND TEMPERATURE 347
A collecting pressure of 60-70 mm Hg was employed. Preliminary experiments had shown
a plateau of maximum flow when blood flow was plotted against cuff pressure. The limits of this
plateau varied with the plethysmograph temperature, but a pressure of 60-70 mm Hg fell within
the plateau at all temperatures in the series, and was in good agreement with the pressure recom-
mended by Abramson (1944), viz. 50-70 mm Hg.
A much higher frequency of recording was employed than was used by earlier workers. The
maximum frequency permitted by the technique, allowing three full pulse beats after the artifact
for drawing a tangent and an equal time for the return of the vessels to resting state, is about ten
a minute. An automatic cuff-inflating unit (Kerslake, 1949) was used. Records were taken at
the rate of six flows a minute in experiments at higher temperatures. At moderate temperatures
a rate of three flows a minute (i.e. 10 sec cuff on, 10 sec off) was usual. At lower temperatures,
with a diminished blood flow, a rate of two or one per minute was employed.
Two normal adult feet were dissected, and the proportions by volume of different tissues were
obtained by water displacement. The feet were fresh specimens from leg amputations and showed
no evidence of vascular pathology or wasting.
RESULTS
The proportions of tissues in the two feet dissected are given in Table 1.
These figures are presented first to show that values for blood flow which
follow, largely represent flow through skin and subcutaneous tissue.
TABLE 1. The proportions of tissues in two feet dissected
Foot A, volume 1040 ml.; foot B, volume 862 ml.
Percentage by volume
Foot A Foot B Mean
Skin 21.5* 12-0* 17
Subcutaneous tissue 21-0* 27.5* 24
Deep fat 1.0 3*7 2
Muscle 15-0 12-5 14
Bone, tendon and ligament 415 44-5 43
* Accurate separation of skin and subcutaneous tissue is difficult in this type of dissection. In
dissection of foot A much of the subcutaneous tissue and its embedded fat was left attached to
the skin. The skin proportion can therefore be considered a maximum. In dissection of foot B
the greatest possible amount of subcutaneous tissue was removed from the skin and without
doubt this included deeper dermal regions. The skin proportion for foot B therefore is certainly
too small and can be considered a minimum.
TABLE 2. Number and duration of experiments, timed from filling the plethysmograph
with water at the appropriate temperature
Length of experiment No. of
(min) experiments
120-150 10
90-120 44
60-90 21
Below 60 9
E15 -
-E0 A 0'^u s
0 ~~~~~~~~~~~~~~~~I I
20 40 60 80 100 120
Time (min)
Fig. 2. Subject M.J.A. Foot blood flow plotted against time during experiments at seven different
temperatures. Each point represents the average blood flow over 5 mi.
The major variation followed one of four patterns, depending on the tem-
perature of the water in the plethysmograph.
(1) At temperatures of 290 C and below, the blood flow fell steadily for
a period. The lower the temperature, the steeper was the rate of fall in flow, so
that at 150 C a minimum level was reached 40 min after the foot was in water,
and at 260 C the lowest flows were not reached until after 90 min. After this
fall the flow either returned towards the original value, or remained at the
low level.
(2) At temperatures around 320 C there was no consistent trend, the blood
flow either remaining constant, increasing, or decreasing slightly.
(3) At temperatures from 35 to 41.00 C the flow increased-the rate of
increase being steeper the higher the temperature-until a peak was reached,
after which there was a die-away. At 350 C the peak occurred at about
75 min, whereas at 410 C it was reached after about an hour. Usually the
die-away was not completed when recording finished, so the blood flow was
approaching, but had not reached, the initial level.
(4) Experiments at 440 C showed the sharpest increase in blood flow so that
a peak was reached after 40-50 min, but the existence of a die-away was
doubtful. The same was found in two experiments at 42.50 C.
FOOT BLOOD FLOW AND TEMPERATURE 349
One typical experiment from each pattern is shown in Fig. 3.
These trends were generally similar in all subjects, but there was some
overlap in time of occurrence of the peak. Two experiments showed discordant
patterns; in one at 36.50 C on subject H. S. B. the blood flow was 11 ml. 30 min
after the foot was in water, and progressively diminished, so that 1 hr later it
was 6 ml. An experiment at 310 C on the same subject showed a steep rise in
flow from 4 ml. at 30 min to a peak of 12 ml. 45 min later. We are unable to
explain these two anomalies.
20 40 60 80 30 50 70 90
25 -25
£S20 20
E
E
8 15
VI
44c 410 1
804 4
2 320 coo3
20 40 60 80 30 50 70 90
Time (min)
Fig. 3. Subject H.S.B. Foot blood flow plotted against time at four temperatures, showing
different flow patterns. Each point represents the average blood flow over 5 mi.
The other changes in flow occurring in these experiments were the so-called
'spontaneous' variations described by Hewlett & van Zwaluwenberg (1909)
and studied in the finger by Burton (1939) and by Burch, Cohn & Neumann
(1942). They were seen as differences in the slope of single inflow curves.
Fig. 4 shows a section of a tracing in which spontaneous variations in flow are
occurring. Their frequency and amplitude were varying continuously. No
analysis of the frequency was made. The amplitude of the most rapid variations
increased with temperature. This is shown in Fig. 5 where the standard devia-
tion of flows from their mean is plotted against temperature for two subjects.
Spontaneous variations of the order of minutes in duration were studied by
averaging all flows in a minute, and plotting the flow level each minute during
an experiment. Inspection of these graphs showed that spontaneous variations
of 1-10 min in duration also increased in amplitude as the temperature rose,
reaching a maximum at 38-41° C. At 44° C the amplitude was less than at
41° C in two subjects, but appeared unchanged in two other subjects.
350 M. J. ALLWOOD AND H. S. BURRY
M I I I 1 *
MIs I J
*
q uI I
S I a 'a 1 . u
i~~~.-.Wr,.qm-r-K
M -.
a
.-maq-a-l-r.
!l* a a a M *4 -M -'6 .'0
.* . ' . -'.-F...-lr
' ' ' ' ' -'
10.
Fig. 4. Subject H.S.B. Plethysmograph temperature 320 C, room temperature 23.10 C. Upper
tracing shows spontaneous variations in volume occurring in the foot; lower tracing shows
variation in rate of inflow of blood during a spontaneous volume variation. Time marker:
5 sec.
4 M.J.A. H.S.B.
4
C
* 0 C
._
3 3 .0
0
0@ a AV
*
I
**
,, -o
2
_~~~~~00@ 0
-0 0 2 M
v
Lfl
-
_
3..~~~*
~~to *.
I0
C
0
* 00 VI
n S 0
0
0
nt
v , -
I I I I li ,
0. I* I
. . . .
0
15 25 35 45 15 25 35 45
Water temp. (OC)
Fig. 5. The effect of variation in local temperature on the standard deviation of the mean for
blood flow in experiments on two subjects.
FOOT BLOOD FLOW AND TEMPERATURE 351
The variability of blood flow in experiments at different temperatures was
compared using the coefficient of variation as an index (Fig. 6). Other
things being equal, a higher coefficient of variation would be expected for
experiments at higher temperatures where the flow rises to a peak and dies
away than at intermediate temperatures where there is a level flow. What
actually occurred was the opposite of this. The coefficient was least at 440 C,
and increased as the temperature decreased, so that it was greatest at 29-32° C.
Below 290 C it was less reliable, for the apparatus recorded with accuracy to
the nearest 0.1 ml., and at 26° C and below the flows were approaching this
order. There was greater scatter but the coefficient tended to diminish.
0~~~~~~6
0
60 0g
4.'40 (4
40V
4~~~~~~~~~~~~~t 0k
de0to 0 0 3~~~~~~0 20
*~~ ~ae tep (°C)0
0 I~ ~ ~ ~ * 20
i5 25 35 45 15 25 35 45
Water temp. (OC)
Fig. 6. The effect of variation in local temperature on the coefficient of variation (= (standard
deviation÷ mean) x 100) for blood flow in experiments on two subjects.
15/ , o
S~~~~~~~~~~~~~~~~~
E X
E 10 _ 0/ /
0~~~~~~~~~~~~~~~
0~~~~~~~~~~~~~~~
o .IP
0~~~~~~~ a/
O 15
-_ 25 35 45
Temp. (IC)
Fig. 7. The effect of temperature on blood flow in the foot. Solid line represents blood flow over
the period 30-90 min after the foot enters water. Broken line represents flow over maximum
or minimum 15 min.
A further comparison was made by taking the average tlood flow over the
15 min period of the peak or trough of the flow curve depending on whether
the major variation was a rise or fall. If inspection of a graph of the flow
during an experiment did not obviously reveal the required period, planimetry
was used, and the 15 min period on the graph with the greatest or least area
below was found. All flows in 1 min were averaged, and the average of the
15 min was taken. The majority of experiments at 320 C were analysed by
planimetry, as inspection alone failed when there was relatively level flow.
The results are given in Table 3, column (b); averaged for the four subjects
they are also plotted in Fig. 7. The form of the curve is not significantly
altered.
PH. CXXIV. 23
354 M. J. ALLWOOD AND H. S. BURRY
DISCUSSION
These experiments confirm previous observations that there is an increase in
blood flow to the foot with increasing local temperature, while giving some
indication of the range, variability, and trend of flow in experiments at
a particular temperature.
There is good agreement between our curve for flow against temperature
and values obtained by other workers. In supine subjects Scheinberg et al.
(1948) obtained average flows of 2-3-7-8 c.c. at 320 C, ambient temperature
24-26.5° C. Abramson, Zazeela & Marrus (1939) give 1-3-6-6 c.c. under similar
conditions, but with the foot dependent. Also at 320 C, room temperature
210 C, Hoobler et at. (1949) obtained an average flow of approximately 2 c.c.,
as did Lynn & Barcroft (1950), using an air-filled plethysmograph, on subjects
for sympathectomy with normal arteries. The same agreement is found at
higher local temperatures; Kunkel & Stead (1938) obtained an average flow of
17-1 c.c. at 430 C; Killian & Oclassen (1938) give 14-8 c.c. for controls at 450 C.
Likewise also at lower temperatures; 0-9 c.c. at 250 C (Killian & Oclassen);
0 5 c.c. at 200 C (Love, 1948, using an air-filled plethysmograph).
Hand blood flow is considerably greater than foot blood flow when the limb
is immersed in water at 320 C and below. Some representative hand figures
are:
32-33° C 2-5-15-0 ml. (Cooper, Cross, Greenfield, Hamilton &
Scarborough, 1949)
32-330 C 9-1 ml. S.D. + 2-1 (Abramson, Zazeela & Marrus, 1939)
250 C 2-7 c.c. (Spealman, 1945)
150 C 1-2 c.c. (Spealman, 1945)
At higher temperatures there is some variation in published results for hand
flow, but there appears to be little doubt that it is greater than in the foot,
e.g. 18-7-54-4 ml. at 430 C (Kunkel & Stead, 1938). Likewise after sympath-
ectomy blood flow in the hand is about double that in the foot (Walker,
Lynn & Barcroft, 1950). It has been suggested (Barcroft & Swan, 1953) that
this is probably because the circulation in these parts is mainly through the
skin, and the hand contains a relatively much larger proportion of skin. Our
figures for the two feet dissected do not appear to support this. We found
17 % skin in the foot compared with 19 % in one hand (Edholm, personal
communication) and 41 % skin and subcutaneous tissue compared with 29 %
(Abramson & Ferris, 1940).
Kunkel & Stead (1938) showed that when related to surface area the blood
flow to the hand is still greater. Part of this difference may be related to the
number of arteriovenous anastomoses present, but this is unlikely as Grant &
Bland (1931) have shown that the density of distribution is greater in the
sole than in the palm. This is supported by Pickering & Hess (1933) who
FOOT BLOOD FLOW AND TEMPERATURE 355
concluded that the difference in response to indirect vasodilatation between
hand and foot could not be accounted for by a difference in vascularity. They
suggested that there is greater vasoconstrictor tone in the lower extremity.
This has been confirmed by measurement of blood flow after sympathetic
ganglion blockage (e.g. Slaughter, Brown & Wakim, 1948; Hoobler et al.
1949), and would appear to be the most reasonable explanation for the dif-
ference in volume blood flow to the parts.
The shape of the graph for blood flow plotted against temperature is
remarkably similar in hand, forearm and foot (Fig. 8). There is a gradual
increase in blood flow with increasing temperature up to 290 C; cold vaso-
dilatation did not occur as our local temperatures were not low enough. The
20 -
Hand Foot Forearm 20
lo 2 15
15 is 25 35 25 45 35
Temp. (OC)
Fig. 8. The effect of temperature on blood flow in the hand, foot and forearm. Graph for hand
after Cooper et al. (1949); for forearm from data by Barcroft &; Edholm (1943).
rate of increase is accelerated arounad 29-33° C, and the flow then rises steeply
with increasing temperature to 44° C. The inflexion for the foot is centred
about a slightly lower temperature than that for the hand, which in turn is
approximately 1-2° C lower than that for the forearm.
The pattern of flow during an experiment is generally similar to that at the
same temperature described in the forearm (Barcroft & Edholm, 1943). The
time of onset for the die-away appears to be later in the foot exrperiments at
41 and 38° C; in both parts at 35° C a peak was very often not reached when
recording ceased. Barcroft & Edholm, however, had the hand as well as the
forearm immersed in a water-bath, although they measured only forearm
flow. The effect of this might exrplain the similarity in long-term variation.
It cannot explain the similarity in flow levels which is rather unexpected in
view of the widely different proportions of skin and muscle in forearm and
foot.
23-2
356 M. J. ALLWOOD AND H. S. BURRY
It would have been of interest to prolong experiments to see what followed
the die-away, but recording was stopped when a subject first showed signs of
restlessness as he was considered to be no longer in a 'physiological' state.
Spealman (1945) showed that the hand is approaching a state of equilibrium
with the surrounding water during the third hour, as judged from blood flow
and skin temperature records. Of six experiments in the foot which con-
tinued for 24 hr, two (30.5 and 320 C) showed a fairly constant flow level,
two (35 and 380 C) showed a second rise following the die-away and in two
('37.5 and 39.50 C) the die-away was still in progress, although at 37.50 C the
flows were well above the initial level while at 39.50 C they had fallen below.
Neither brachial arterial pressure measurements nor the small number of skin
temperature determinations appeared to help explain the occurrence of the
die-away.
The absence of a definite pattern of rise or fall and return in blood flow at
320 C makes this the most suitable local temperature for studying the effect of
drugs on the circulation in the human foot. At the same time the relatively
large variation in flow during an experiment, and the variation encountered
between experiments, should be kept in mind.
SUMMARY
1. The rate of volume blood flow in the foot was measured in four subjects
at local temperatures from 15 to 440 C, using the venous occlusion plethysmo-
graphy technique.
2. The average resting blood flow in the young adult male foot ranged from
0-2 ml./100 ml. tissue/min at 15° C to 16-5 ml./100 ml./min at 440 C.
3. The blood flow was not constant during an experiment. The major
variation was an increase with time at temperatures above 320 C, and a decrease
below 320 C, returning after an interval towards the initial value.
4. The absolute amplitude of 'spontaneous' variations was greatest at the
higher temperatures. The relative amplitude, proportional to the mean flow,
was greatest at 29-32° C.
5. The results presented are compared with previous values obtained in the
hand and foot. Flow patterns are compared with those in the forearm and
their importance noted.
The authors wish to express their appreciation to Dr 0. G. Edholm for advice and encourage.
ment. Our thanks are also due to Mr Landau, of the London Rubber Co., for providing socks.
REFERENCES
ABRAMSON, D. I. (1944). Va8,cular Responses in the Extremities in Man in Health and Di8ea8e,
1st ed. p. 65. Chicago: University of Chicago Press.
ABRAMSON, D. I. & FERRIS, E. B. Jr. (1940). Responses of blood vessels in the resting hand and
forearm to various stimuli. Amer. Heart J. 19, 541-553.
ABRAMSON, D. I., ZAZEELA, H. & MARRUS, J. (1939). Plethysmographic studies of peripheral
blood flow in man; physiological factors affecting resting blood flow in the extremities.
Amer. Heart J. 17, 206-217.
FOOT BLOOD FLOW AND TEMPERATURE 357
ABRAMSON, D. I., ZAZEELA, H. & OPPENHEIMER, B. S. (1939). Plethysmographic studies of
peripheral blood flow in man; effect of smoking upon vascular beds in hand, forearm and
foot. Amer. Heart J. 18, 290-302.
BARcRoFT, H. & EDHOLM, 0. G. (1943). The effect of temperature on blood flow and deep
temperature in the human forearm. J. Physiol. 102, 5-20.
BARcROrT, H. & EDHOLM, 0. G. (1946). Temperature and blood flow in the human forearm.
J. Physiol. 104, 366-376.
BARCROFr, H., KONZETT, H. & SWAN, H. J. C. (1951). Observations on the action of the hydro-
genated alkaloids of the ergotoxine group on the circulation in man. J. Phy8iol. 112, 273-290.
BARcRoFr, H. & SWAN, H. J. C. (1953). Sympathetic Control of Human Blood Vessels, 1st ed.
p. 62. London: Edward Arnold and Co.
BURCH, G. E., CoEi, A. E. & NEuMANN, C. (1942). A study by quantitative methods of the
spontaneous variations in volume of the finger tip, toe tip and postero-superior portion of
the pinna of resting normal white adults. Amer. J. Phy8iol. 186, 433-447.
BURTON, A. C. (1939). The range and variability of the blood flow in the human fingers and the
vasomotor regulation of body temperature. Amer. J. Phy8iol. 127, 437-453.
COOPER, K. E., CRoss, K. W., GREENFIELD, A. D. M., HAMLTON, D. McK. & SCARBOROUGH, H.
(1949). A comparison of methods of gauging the blood flow through the hand. Clin. Sci. 8,
217-234.
FREEMAN, N. E. (1935). The effect of temperature on the rate of blood flow in the normal and in
the sympathectomised hand. Amer. J. Phy8iol. 113, 384-398.
GRANT, R. T. & BLAND, E. F. (1931). Observations on arteriovenous anastomoses in human skin
and in the bird's foot, with special reference to the reaction to cold. Heart, 15, 385-407.
HEWLETT, A. W. & VAN ZWALUWENBURG, J. G. (1909). The rate of blood flow in the arm.
Heart, 1, 87-97.
HOOBLER, S. W., MALTON, S. D., BALLANTIEE, H. T. Jr., COHEN, S., NELIGH, R. B., PEET, M. M.
& LYONS, R. B. (1949). Studies on vasomotor tone. I. The effect of the tetraethylammonium
ion on the peripheral blood flow of normal subjects. J. clin. Inve8t. 28, 638-647.
KERSLAKE, D. McK. (1949). Method of the frequent estimation of forearm blood flow under
conditions of decreased atmospheric pressure. J. Phy8iol. 108, 398-404.
KiLaN, J. A. & OCLASsEN, C. A. (1938). Comparative effects of water baths and mustard baths
at varying temperatures on the rate of peripheral blood flow in man. Amer. Heart J. 15,
425-433.
KUNKEL, P. & STEAD, E. A. Jr. (1938). Blood flow and vasomotor reactions in the foot in health,
in arteriosclerosis and in thromboangiitis obliterans. J. clin. Inve8t. 17, 715-723.
KUNKEL, P., STEAD, E. A. Jr. & WEISS, S. (1939). Blood flow and vasomotor reactions in the
hand, forearm, foot and calf in response to physical and chemical stimuli. J. clin. Inve8t.
18, 225-238.
LANDOWNE, M. & KATZ, L. N. (1942). A critique of the plethysmographic method of measuring
blood flow in the extremities in man. Amer. Heart J. 23, 644-675.
LEWIS, T. (1929). Experiments relating to the peripheral mechanism involved in spasmodic
arrest of the circulation in the fingers, a variety of Raynaud's disease. Heart, 15, 7-101.
LOVE, L. H. (1948). Heat loss and blood flow of the feet under hot and cold conditions. J. appl.
Phy8iol. 1, 20-34.
LYNN, R. B. & BARcRoFor, H. (1950). Circulatory changes in the foot after lumbar sympathectomy.
Lancet, 158, 1105-1108.
PICKERING, G. W. & HEss, W. (1933). Vasodilatation in the hands and feet in response to warming
the body. Clin. Sci. 1, 213-223.
SCHEINBERG, P., DENNIS, E. W., ROBERTSON, R. L. & STEAD, E. A. Jr. (1948). The relation
between arterial pressure and blood flow in the foot. Amer. Heart J. 35, 409-420.
SCHNAPER, H. W., JOHNSON, R. L., TuOHY, E. B. & FREIS, E. D. (1951). The effect of hexa-
methonium as compared to procaine or metycaine lumbar block on the blood flow to the
foot of normal subjects. J. clin. Invest. 30, 786-791.
SLAUGHTER, 0. L., BROWN, H. S. & WARmM, K. G. (1948). Effects of tetraethylammonium chloride
on blood flow in the extremities of man. J. Lab. clin. Med. 33, 743-746.
SPEALMAN, C. R. (1945). The effect of ambient air temperature and of hand temperature on
blood flow in hands. Amer. J. Phy8iol. 145, 218-222.
WALKER, A. J., LYNN, R. B. & BARCROFT, H. (1950). On the circulatory changes in the hand
and foot after sympathectomy. St Thom. Hosp. Rep. (2nd series), 6, 18-30.