AHEHICAN
Vol.
JOURNAL
OF
PHYSIOLOGY
1974.
226, No. 3, March
Printed
in U.S.A.
Maximum
oxygen
facilitation
in small
MARIO
Institute
ROSENMANN
of Arctic Biology,
consumption
homeotherms
AND PETER
MORRISON
University of Alaska, Fairbanks,
ROSENMANN, MARIO,
AND PETER MORRISON.
Maximum
oxygen
consumption
and heat loss facilitation
in small homeotherms
by He-02 .
Am. J. Physiol.
226(3) : 490495.
1974.-The
high thermal conductance
of an 80% He-20y0
02 atmosphere
was used to elicit
in moderate cold in species rangmaximum
metabolism
(Mmax)
ing from
7-g pygmy
mice (Baiomys
taylori)
to 250-g white rats,
including
redpolls
(Acanthis J?ammea),
two vesper
mice
(Calomys
d&la,
C. callosus),
tundra
voles (Microtus
oeconomus),
and four
strains
of Mus musculus. Values
slightly
exceeded
those in similar
animals
using
other
methods
to confirm
the low
metabolic
ratio
(Mmax/M,
in) in rodents (4-8
X). Submaximal
values at
higher
temperatures
defined
thermal
conductance
in He-02 and
air. In different
species the ratios of these conductances
ranged
from 1.4 to 2.6, differences
which relate to the extent
and quality
of the respective
insulation.
M,,,
was obtained
at 13-70°C
warmer
in He-02 than required
in air for the same metabolic
effort.
Avoidance
of low-temperature
technology
and freezing
injury,
elimination
of treadmills
and training
in running,
prompt
(3-10
min after He-02
exposure),
and obviattainment
of M,,.,
ation
of shaving
or wetting
procedures
are advantages
of the
present
technique.
maximum
conductance;
metabolism;
Baiomys;
helium;
Acanthis;
and heat loss
cold exposure;
insulation;
white rat; Mus; Calomys;
thermal
Microtus
ALTHOUGH
ANIMALS
TN NATURE
spend
the majority
of their
time resting or at low levels of activity,
some functions
critical for survival such as fighting, escaping, or predation
greatly increase the energy demand.
The maximum
capability to increase metabolism
is the main factor in limiting
the intensity of such physical activity and, as well, sets the
limit for cold tolerance.
Evaluations
of maximum
oxygen
uptake (Mm,,) in mammals have been made by cold exposure in air or water, by exercise on treadmills,
by swimming, or by a combination
of these. These methods may
require
extended
training
sessions for running
(as long as
1 mo), cutting off the tail, and elimination
of inept performers
(32). Another
serious reservation
is that these
procedures
may directly modify the character under study.
Exposures to subfreezing
temperatures
risk peripheral
cold
injury or lethal hypothermia
(23). Removal of the natural
insulation
can increase metabolism
greatly but, again, is
traumatic
and results in irreversible
change.
TO avoid such extreme cold exposure and the injuries
reported
during
exercise (32, 16), we have dewdoped the
use of a helium-oxygen
atmosphere
to raise the heat output
of small homeotherms
to maximum
levels at more modest
by He-O,
Alaska
99701
ambient temperatures
(T&). The effect of He-02 in increasing metabolism
has been known for some time (3, 36), and
although
once in some question its action is now generally
ascribed to the increased thermal
conductance
of the gas
(5, 25, 34). Since the insulative
quality of fur or feathers
depends on the slow transfer of heat through the enclosed
air spaces, the substitution
of a 4 times more conductive
medium
such as 80 % He-20 % 02 (26) should greatly
facilitate
heat transfer.
However,
the actual
metabolic
increases reported
in small mammals
are so much more
modest, e.g., <25 % in rats (34) or <50 % in mice (3, lo),
that the exact nature of the effect is still very much in
question.
METHODS
Tests were conducted
on two laboratory
species, the
white mouse and the white rat, previously assessed for M,,,
by various other procedures.
Three further strains of A4us
musculus, a hairless mutant (HRS/J),
and feral house mice
from 15,000 feet at Morococha,
Peru and from Arkansas
were also compared.
In addition,
measurements
were
made on wild species native to different
habitats:
arctic
(Microtus oeconomus from Fairbanks),
alpine (Calomys ducilla
from 13,000 feet near Puno, Peru), and subtropical
(Calomys
callosus from San Joaquim,
Beni Province,
Bolivia),
and
the pygmy mouse Baiomys taylori. The final species was a
small arctic bird, the redpoll
(Acanthis jlammea), also native
to Fairbanks.
We are indebted
to Dr. Oliver P. Pearson
and Dr. Karl M. Johnson
for the respective
Calomys, to
Dr. Hermann
Pohl for the redpolls, and to Dr. John Sealander for the lowland Mus. These rodents were maintained
in our animal facility at a neutral T, of 20-24°C.
Three to
eight individuals
of each type were tested at 735-750 torr.
02 consumption
was measured in a closed-circuit
manometric respirometer
(28). Since the oxygen consumed
by
the animal
is replaced
by successive aliquots,
the inert
component
maintains
its concentration
as established.
The
metabolic
chambers of stainless steel were submerged
in a
thermoregulated
water-glycol
bath. After a variable length
of time (l-3 h) in which the metabolic
rate in air was
measured,
the chambers were flushed with 5-6 times their
volume of an 80 % He-20 % 02 mixture
from a proportioning gas mixing pump or from a gas tank. Use of the
gas tanks with premixed
He-02 reduced the purging
time
to only 2 min as compared
with 7-9 min with the mixing
pumps. To avoid temperature
changes, the He-02
mixture was admitted
through a submerged
copper coil.
HEAT
LOSS
AND
MAXIMUM
OXYGEN
CONSUMPTION
IN
Food as apple, carrot, and sunflower seed was generally
available
during
the tests. Regardless
of the duration
and
temperature
of the metabolic
measurements,
the animals
were tested about 4 times a week, and generally
2 days
were allowed between consecutive tests at high submaximal
rates.
RESULTS
Immediately
after the substitution
of He-O2 for air,
02 consumption
increased
well above the resting levels
in air, as shown in Fig. 1 for ;;M. oeconomus. Of interest also
is the suppression
in He-O 2 of the metabolic
cycles reflecting changes in activity or posture, an effect also seen
at lower T, in air. These relations are shown in Fig. 2 for a
I
I
I-
AIR 20
I,
!
,
0
A-M oeconomus:
2
He-O 2-
,
,
6
in Hours
FIG. 1. Representative
experiment
showing
gen consumption
at 15°C in M. oeconomus.
effect
. . . . . . . :\;; . . . . . . . . . . . . . . . . . . . . . . . . . . . . .
:\
: \
\
\
\
.
.
-
\
\
\
\
,
4
Time
I2
I5 C
\
\
of He-02
on oxy-
/M. oecoffomus
N=3,
329
491
HE-O2
series of T, between
26 and 7°C again for AL oeconomus.
The respective values in air and in He-02 lie along two
straight
lines which extrapolate
to the Tb at 39OC to fit
the relations :
M
=
C(Tb
-T,)
=
CAT
and M
=
CHeAT
The constant C usually designated
as the (minimum)
conductance
actually
includes
a component
of evaporative/
respiratory
heat loss, but at these T, below thermal
neutrality
this represents
a constant
(small) fraction
of the
thermal
loss through
the surface-a
cost of “chemical”
thermoregulation.
Accordingly,
C is a measure of the overall
facility for heat loss from the body and will reflect changes
in the properties
of the insulative
layers. In this example
the substitution
of He-02 increased conductance
from 0.178
to 0.377 ml02 (g*h*OC)+,
a factor of 2.12 (@e/C).
At temperatures
below the thermoneutral
zone, heat
production
more than doubled in He-02 until at about 6°C
(in this species) a limit was reached, indicating
maximum
metabolic
capability
for temperature
regulation
(M,,,).
In fact, at 1 “C in He-O:! the maximum
heat production
could only be maintained
for approximately
5 min, and
longer
exposure
under
these conditions
resulted
in decreased 02 consumption
and hypothermia.
Exposure
to
lower temperatures
in He-02 did not seem to modify their
maximum
response, but the highest rates were held for a
shorter time. The quotient,
M,,/C,
provides an estimate
of the maximum
temperature
differential
tolerable
by the
animal, in this case -70°C.
This has been shown graphically by extrapolation
of M = CAT to the value M,,,
=
12.5 ml02 (g-h)-’
at -3 1 OC. It may be noted that we have
observed limiting
values of cold tolerance
of this species
(neutral
acclimation)
at -25
to -30°C
(unpublished
observations).
A somewhat
lower ratio was observed
in white rats
(Fig. 3). Maximum
rates in He-02 were attained
within
6-10 min at -3OC. Exposure at - 10°C in He-02 resulted
in reduced
02 consumption
and hypothermia.
The effects of He-02 on highland
house mice and white
mice are shown in Fig. 4. The ratio CHe/C was 2.3 in the
house mice as compared
to 2.1 in white mice and M,,,
was 24 % higher,
13.8 vs. 11.1 ml 02 (g h)-‘. In lowland
l
\
.
AIR
-20
0
20
TA in OC
FIG. 2. Oxygen
consumption
of M. oeconomus
and in He-02
(solid circles) measured
at different
and lower dotted
lines indicate
observed
M,,,
tively. Vertical
dotted
line from intercept
M,,,
extrapolated
air temperature
for M,,,
. Vertical
values.
in air (open circles)
temperatures.
Upper
and Mmin , respecand Mair indicates
bars show range of
-40
-20
0
20
40
TA in “C
FIG.
in He-02
3. Oxygen
consumption
of white rats in air (open
(solid circles) . as a function
of T, .
circles)
and
M.
ROSENMANN
AND
P. MORRISON
16
14
2
IO
6,
&
a
8
O”
.-c
6
0”
4
--C ducih
--C cu//osus
N=3,
169
o-a
N=6,48g
‘\
o-8
2
I
-30
-20
-10
20
0
30
-20
40
TA in Ode
:
I :
-IO
I
0
I
IO
‘a* \
I
20
30
40
TA in OC
FIG. 4. Oxygen
consumption
of feral house mice (circles)
and of
white mice (squares)
in air (open symbols)
and in He-02
(solid symbols) as a function
of T, .
FIG.
6. Oxygen
consumption
C. callosus
(squares)
in air (open
bols) as a function
of T, .
of Calomys
ducilla
(circles)
and of
symbols)
and in He-02
(solid sym-
~-
T
25 -
T
. ... .. .. .. .. .. . ... .. ... . ... . .. ... .. .. . ... .. .. . ... .. .. .. ... . ... .
. . . . . . . ..a......-
Pohl
5-
0:’
-80
i
: .. .
. .. ..
”
-60
. . .. .. . ..
.. . . .
’
-40
ffnd
Wed,
.
1973
.
.
I
..
1
-20
. ..
I
. ,
I
0
.
1
.
I
20
\
\ \
\ ‘1
’
.’ A
1
40
TA in “C
I
-20
-10
0
IO
20
30
40
Tn in “C
FIG. 5. Oxygen
consumption
and in He-02
(solid symbols)
compare
function
for normal
of hairless mice in air (open symbols)
as a function
of T, . Reference
curves
mice.
was intermediate
at 12.3 ml02
house mice the M,,,
(g h)-?
To gain insight into the relation
between
the surface
insulation
and the effects of He-02 , hairless mice were also
tested (Fig. 5). The ratio of the thermal conductance
in air
of hairless versus normal mice was 1.9, close to a previously
reported
ratio of 2.2 for these strains (29). However,
in
He-02,
the conductance
ratio hairless versus normal
was
only 1.3 due to the much smaller response of the hairless
mice to helium (CHe/C = 1.40). MmaX in hairless mice was
13 % higher than in the normal white mice (12.5 vs. 11.1
ml02 (g*h)+
but still 10 % lower than in the feral mice.
Similarly,
the metabolic
expansivity
of the hairless mice
(10.5 ml02 (go h)+)
lay between
those of the two other
ratios were 6.3 in both the white and the
strains. MmJMmin
hairless mice as compared with 7.2-7.3 in both feral groups.
Results of He-02 exposure in Calomys A~‘lla, a highland
species, are shown
species, and Calomys callosus, a tropical
l
FIG. 7. Oxygen
consumption
of redpolls
in air (open circles) and in
He-O2
(solid circles)
as a function
of T, . Continuous
line down to
-30°C
indicates
02 consumption
in summer
(M = 8.24 - 0.18 T)
after West (35). Symbols
at -50°C
indicate
02 consumption
values
in spring
(1) and summer
(2) after Pohl and West (33).
in Fig. 6. M,,,
of 14 ml02 (g-h)+
was found in the 16-g
C. duda
and 6.8 mlOZ (go h)-l in the 3 times larger C.
callosus.
Redpolls
(Acanthis jiammea) were treated
in a similar
way to the rodents with the exception
of a wooden perch
in the cages and an aluminum
cover to maintain
a dark
environment
and so diminish
spontaneous
activity.
02
consumption
values in air and in He-02 are shown in Fig. 7.
The highest ratio, We/C
= 2.6, was observed in the redpoll and a M,,,
of 21.8 ml02
(g-h)-l
was elicited
at
-5OC.
Table 1 summarizes
the thermogenetic
effects of He-02
in the experimental
species, the temperatures
at which
M,,,
was elicited in He-02 , the extrapolated
air temperatures for these rates, and the thermal conductance
values in
relation to the He-02 atmosphere
and to the animal’s
surface area. In general, M mm in the rodent species was obtained in He-02
at 13-30°C
warmer
temperatures
than
expected in air, but in the hairless mice the difference
was
only 7OC. In contrast,
a 70°C warmer
temperature
for
Mm,, elicitation
in He-02 was estimated for the redpolls.
HEAT
LOSS
AND
MAXIMUM
OXYGEN
CONSUMPTION
IN
DISCUSSION
A comparison
of our data on M,,,
of mice, rats, and of
the pygmy mouse with reported
values for the same species
but obtained
with different
methodologies
is shown in
Table 2. Our values for white mice are equal or higher
than reported
figures from mice kept at neutral
or warm
temperatures
but are 8 % lower than from cold-acclimated
mice (12). Similarly
in white rats, M,,,
values in He-02
are the same or higher than reported capabilities
in normal
rats and only 4 % lower than cold-acclimated
ones (32).
In Baiomys, 18 % higher M max was obtained
in He-O:! than
the maximum
values reported with cold exposure (20).
Published
data for the rest of our wild species seem to
be unavailable,
but some values have been reported
in reTABLE
1. Metabolic
He-O 2 and air
ratios and conductance factors in
Ta for Mm,,
ML
M
-- mrrx Mmax
2
Species
n
Mmin
Mstt
Ib@
Rattus norvegicus
(albino)
Calomys callosus
Microtus oeconomus
Mus musculus
(albino)
Hairless
Wild,
highland
Wild,
lowland
Calomys ducilla
Acanthys Jammea
Baiomys tayZori *
253
7
4.9
6.1
-3
48
32
30
6
3
5
4.6
5.2
6.3
5.1
8.4
7.3
7
1
7
21
17
17
16
14
7
8
6
4
3
5
6
6.3
7.3
7.2
8.2
5.6
4.3
7.5
7.8
7.0
7.8
5.9
5.5
14
5
10
10
-5
23
* Old subjects,
WOai24 (ml 02/h,
taken as 8 W2j3.
18-28 mo.
t Mst taken
g) for passerines
(24).
TABLE 2. Comfiarison of maximum
‘”
cms.h.OC
ml 02
-30
.078
1.8
16.2
-8
-31
-14
.132
.178
.216
1.9
2.1
2.1
16.7
14.2
11.9
7
-22
-12
-16
-75
10
.575
.236
.247
.254
.197
,455
1.4
2.3
2.0
2.3
2.6
1.8
5.0
13.1
12.6
12.5
16.8
8.7
9
$r,
C-
musculus
Baiomys
norvegicus
Weight,
g
Acclimt
18.5
26.5
26.7
33.0
34.0
33.4
29.5
21 .o
17.3
17.0
albino
albino
C
C
C
n
n
n
n
W
W
C
W
C
n
C
7.3
6.9
t Acclimation:
cold, warm,
neutral,
lated species. In 18-g Microtus arvalis a ratio Mmax/Mmin
5.5
has been reported
in treadmill
studies (21). Our value for
32-g Microtus oeconomus was 5.2.
In summer birds, exposure of house sparrows to -30 to
- 65°C resulted in Mm,, of 15 ml02 (g h)-l and Mm,,/
M min of 3.3 (14). In the goldfinch,
exposure to 0°C after
removing
the feathers gave Mm,, of 18.9 ml02 (g*h)-l
min of 4.2 (8). By comparison
Mm,, of sumand
Mmax/M
mer redpolls in He-02 was 2 1.8 ml02 (g h)-l with a Mm=/
M min ratio of 5.6.
In previous studies of white mice and rats, considerably
smaller effects of He have been reported
(34, 36). Examination shows that those measurements,
sometimes on groups
of animals rather than individuals,
gave reference values
in air which clearly include
a considerable
activity component which is then suppressed under the cooling influence
of the He (compare
Fig. 1). Nor will measurements
made
within
the thermoneutral
zone show as large an increase
in metabolism
with He-02 .
Free/forced
convection
and radiation
present
major
routes for heat loss from bare skin with little or no involvement of simple conduction.
Convective
heat transfer in
He-02
as compared
with air has been described
by Epperson et al. (5), in relation
to the ratios of their thermal
conductivities,
densities, specific heats, and viscosities, together representing
a ratio of 2.1. A somewhat larger value
has been calculated
for conductive-convective
effects (7).
By contrast to bare skin, conductive
heat transfer should be
of greater importance
through fur (1 l), and a facilitation
of
fourfold
is indicated
(air -+ He-02).
However,
it is not
easy to assess the effective thickness of a fur, which will
depend
on the density, length, erection
angle, and uniformity
of the fibers which modify convective
mixing
in
the outer layers. Neither is it easy to assess the amount of
l
l
ratios obtained with d$‘erent techniques
M max ,
ml On/g-h
10.75
10.10
12.15
10.50
n
n
T,.
$ This
M
M
IIlitX
3.5
5.2
6.5
7.40
11 .lO
12.50
13.80
12.30
4.2
6.3
6.3
7.3
7.2
3.20
2.76
4.85
4.81
3.20
5.05
4.90
5.40
5.20
(-5.53)
2.7
2.7
3.5
3.6
2.7
4.2
3.1
4.9
(-5.0)
10.40
12.30
5.3
4.3
study.
Reference
and Technique
min
9.30
W
380
385
290
115
300*
300”
286
334
253
371
taylori
* Assumed.
7.54
area
metabolism and Mmas/M,i,
Hairless
Wild,
highland
Wild,
lowland
Rattus
2
as 3.8 WO.73 for mammals
and
1 Insulation
per unit of surface
Species
A4us
0
1t
C/A’
c
ml 02
g.h.“C
493
HE-O2
(8)
(13)
(12)
(32)
(32)
(18)
($)
($)
($)
($)
Cold water
wetting
Run 6 m/min
at 2°C
Run 5 m/min
at -10°C
Run 23 m/min
at -10°C
Run 19 m/min
at -3°C
Noradrenaline,
1.7 mg/kg
He-02
at 7°C
He-02
at 14°C
He-02
at Z-5OC
He-02
at 10°C
(19)
(4)
(27)
(8)
(17)
(17)
(32)
(32)
(#I)
(22,
Cold exposure
at -35°C
Cold exposure
down to -33 “C
Swim with 2y0 load
Cold water
wetting
Run at 0°C or rest at -35°C
Run at - 30°C or rest at -45 “C
Run 35 m/min
at 6°C
Run 27-37 m/min
at 6 to -3OC
He-02
at -3°C
23) (Cytochrome
oxidase
activity)
(20) Exposure
at 7-15 “C
($) He-02
at 23°C
M.
ROSENMANN
AND
P. MORRISON
T-329
i_
/ 4l
I.&
/
/
I
’
I
4
Insulation,
/
&
/
/ /
00El.+’
I
8
in cm2-hr.
c.c /
0
R.n
I
“C
’
0
I
12
I
I
16
.9
I
per CC 02
effects of He-02
(CHe/C)
in different
species vs.
insulation
per unit area, calculated
as reciprocal
of conductance
per
unit area: C/A with A = 8 W?
Mus musculus
indicated
in square
symbols:
hairless; albino;
wild, lowland;
wild, highland.
Rest of species indicated
by initials in circles.
J-0
FIG. 8. Metabolic
radiant
loss either from the outer layer of fibers or from
more thinly
covered areas as on the face, feet, or tail.
Other factors not directly
influenced
by He are surface
evaporation
and tissue insulation,
with involvement
of the
latter suggested by lower skin temperatures
in He-O2 (34).
Although
the increase in conductance
in the He-On mixture cannot define all these factors quantitatively,
it should
give us some measure of the relative
importance
of conto convection
(f
= 2)
duction
(f = 4) as compared
radiation,
tissue
i.nsulation,
and
surface
evaporation
(f = 1).
As noted in Table 1, CHe/C ranged from 1.4 in the hairless mouse to 2.6 in the redpoll.
Since a thick layer of fur
or feathers will emphasize
conductive
transfer as compared
to other modes, We/C
ratio should vary directly with the
insulation.
That such is the case may be seen in Fig. 8 for
species from 7 to 32 g. The larger C. callosus and white rat,
however, do not conform to this pattern, perhaps because
of greater reliance on tissue insulation.
Similarly,
induction
of hypothermia
in He-02 has been also reported
to be related to body size in rats of 100 to over 200 g (31). The
relation
between conductance
and He facilitation
was confirmed experimentally
by observations
of cooling rates in
air and He-02 in preserved Microtus oeconomus with different degrees of insulation
(Fig. 9). These results show conductance ratios of 1.83 when the fur was intact, 1.62 when
10
20
30
Time
40
50
in Minutes
9. Cooling
curves for individual
and air (right).
Solid lines, intact
to about 1 mm; dotted lines, fur totally
FIG.
(left)
60
Microtus
fur; dashed
removed.
70
oeconomus
lines,
80
in He-02
fur clipped
the fur was clipped to 1 mm, and 1.52 when the fur was
totally removed.
As heat dissipation
is seen to be much more affected by
insulation
in air than in He-02 (>3 times), a simple way
of describing
the metabolic
effects of helium
in different
species is in terms of the functional
removal of the surface
insulation,
regardless
of its degree or quality,
the metabolic increase then being proportional
to the magnitude
of the insulation
so “removed. ” Thus, well-insulated
animals, sensitive to small changes of skin temperature
(Is>,
would show a larger response.
Among the many applications
of inert gases, He-02 atmospheres have been used for therapeutic
reasons (2, 9),
also for prevention
of nitrogen narcosis in divers (1), and in
recent years for induction
of hypothermia
in small mammals (6, 30, 31). The elicitation
of maximum
02 consumption in small homeotherms
may prove to be another practical application.
The rapidly attained
Mm, values (3-10
min), the simplicity
of operation,
the avoidance of extreme
cold temperatures
and of treadmills
and training
tests are
definite advantages
of the present technique
over the current conventional
methods.
This research
was supported
in part by National
Health
Grant
GM-10402
from the National
Institute
Medical
Sciences and Grant RR-00518
from the Division
Resources.
Received
for publication
9 October
Institutes
of
of General
of Research
1973.
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