Control of tissue blood flow at very low temperatures

.I. rherm. Bid. Vol. 22, No. 6, pp. 403-407, 1997 ~$91998 Elsevier Science Ltd. All rights reserved

Printed in Great Britain 0306-4565/98 $19.00 + 0.00

PII: so306465(97)ooo59-4

CONTROL OF TISSUE BLOOD FLOW AT VERY LOW TEMPERATURES STUART Department

of Physiology.

University

EGGINTON

of Birmingham,

Edgbaston.

B15 2TT, U.K.

Birmingham

Abstract-Maximum levels of sustainable swimming activity rely on aerobic metabolism, and hence are limited by the cardiovascular supply capacity which is impaired at low temperatures. It is unclear to what extent species adapted to a continuous cold environment retain control of regional blood flow. Muscle blood flow (MBF) was therefore measured using the radiolabelled microsphere method in the Antarctic teleost Notofhenia coriiceps and compared with data for trout at their preferred (optimal) temperatures of 0°C and 11°C. respectively. In resting fish, blood flow distribution to skeletal muscle was similar (around 8 ml/min/lOO g), despite a lower cardiac output in Nototheniu (7 vs. 27 ml/min). Following maximal exercise there was a significant increase in specific blood flow to slow, but not fast, muscle in both species. However, the relative hyperaemia was greater in trout (6.6- vs. 9.3-fold, respectively), with a similar relative increase in cardiac output (2.3- vs. 3.4-fold, respectively). The increase in blood flow to slow muscle, and decrease in peripheral resistance, during maximal exercise in trout (and hence regional O2 delivery by convective transport) appears to be determined centrally. In contrast, reduced active redistribution from the viscera in Nototheniu is presumably responsible for the attenuated increase in MBF on exercise. However, regional hyper- and hypoperfusion can occur within a single locomotory muscle. suggesting control of vascular tone is maintained. 6 1998 Elsevier Science Ltd. All rights reserved Kq Word Index: skeletal muscle

Cardiac

output;

cold

adaptation:

INTRODUCTION It

is generally

an impaired

muscle

blood

due to an increased from

higher

blood

viscosity

etic nerve activity. thermal will

effects

also

decreased to

a

output

(TPR),

leading

impaired acerbated muscle

by

perfusion the

of vasoconstrictor

tonus

acclimation

(Brown

cardiovascular

failure

of

this is ex-

vascular

although

following

there

may

terminal

low

means

that

cell temperature

branchial

heat

(Taylor

et

control

temperatures

of regional is also

adapted

to a continuous

(Taylor

rt al., 1997). The waters one of the most

MBF

found

at the optimal 4”C,

with

in

cold environment around

Antarctica

severe aquatic

environA of

temperature

of 11°C and sub-

that

Antarctic

of

the

coriiceps at its optimal

teleost

temperature

of

0°C.

with which to address

as the efficient

cardiovascular

and winter

species

We consider here whether control of vascular resistance may be retained at very low temperatures. question,

the impaired

seasonal

Notothenia

occurs if the cold shock is of

are ideal animals

with impaired

in both summer

(MBF)

at an inter-

failure is inevitable,

optimal

too severe a level or onset is too rapid.

Fishes

flow

has to be before cardiovascular

trout

of cold

et al., 1993). Clearly,

blood

was maximal

in

trout

ments, being at or below 0°C all year round. comparison was therefore made between MBF

efficacy

a period

in rainbow

low the temperature

constitute

smooth

and the reduced

substances,

be some compensation

further,

muscle

exercise

even in

excursions

how

at

Blatteis,

pressure,

For example,

temperature,

and whether

and

in blood

1996). It is unclear

al.,

the

microspheres;

used to seasonal

in siow

aerobic

performance

resistance and

increase

mediate

the

the capacity

hypotension

is lowered

the

radiolabclled

changes

species

temperature.

during

(QIo)

Eventually,

(Fregly

inability

to maintain

functions

peripheral

systemic

1996). As temperature

water

sympath-

declines,

must exceed

total

to

tissue

rate

bradycardia.

increase

show

resulting

or increased

on biological

induce

further

resistance

As core temperature

cardiac

eurythermal

flow on cold exposure,

peripheral

coriiceps;

sate for major

that most endotherms

assumed

Nofothenia

MATERIALS

Animals

exchange

is in dynamic

AND METHODS

this

equili-

Rainbow

brium with environmental temperature. However, cold acclimatisation may be inadequate to compen-

trout,

Oncorhynchus

mykiss,

were held

in outdoor raceways throughout the year, and sampled at the seasonally appropriate temperature 403

S. Egginton

s

25-

2

20-

5

15.

% 2

lo5.

Rest

Exercise

0

N. coriiceps

@

4w

@I

1 l°C

trout

trout

Exercise

Rest

Fig. I. Cardiovascular responses to exercise at different environmental temperatures in Notothenia coriirainbow trout. MABP, mean arterial blood pressure; est. TPR. estimated total peripheral resistance. *P < 0.05 vs. 4°C.

reps and

of 11°C (autumn) week recovery tanks marine

around

station

returned trolled

tanks

following

l-2

transducer,

in flow-through

ditions

Notothenia coriiceps

1996).

the British

Antarctic

at

and held in temperature

0 k OYC

until

stimuli

con-

experimentation

the

radiolabelled

previously Egginton,

microsphere

(Neumann

latex spheres

viously implanted

method,

et al.,

1994). Briefly,

‘13Sn labelled

was measured 1983;

were injected

dorsal aortic cannula,

drawal reference sample taken the caudal artery. Mean arterial heart rate were monitored

Table

1. Cardiovascular

Ventricle wt. (% BW) cardiac output (ml/min) stroke volume (ml) cardiac minute work (mJ/kg/min) stroke work (mJ/kg/beat)

rest

46Sc or

exercise rest exercise rest exercise rest exercise

aerobic

or mechanical 1994;

Egginton,

blood

to counts

withdrawal

muscles

were sampled

rates.

organs, also

Slow

for both

while

from

to absolute a sample

and

species,

the pectoral

sampled

for

to calculate

flow; this was converted

known

were

was used

fast

of

trunk

in addition locomotory

in Notothenia as this

swimming.

Data analysis

and a with-

Group

data were subjected

to factoral

analysis

of

variance (ANOVA), with inter-group comparisons made via the PLSD post-hoc test. All data pre-

pressure

sented as mean + SEM.

to exercise in fishes at optimal

and sub-optimal

environmental

N. coriiceps

0. mykiss

O’C

4°C

0.10 6.5 15.3 0.27 0.5 I 15.2 34.5 0.077 1.53

con-

injection

maximal

Egginton,

crossover,

species uses labriform

from a cannula in blood pressure and

response

and

by reference

muscles

and

via a pre-

with a high-gain

resting

A second

following

and

values

to visceral

described

15 pm diameter

determine

by either rheological

(Wilson

relative

using

Wilson

immediately

background

Experimental regime animals

to

injection.

1997). Specific activity of tissue (dpm), corrected

1997). Body mass was similar to that of

in conscious

used

exercise induced

at 774 f 26 g (n = 6).

MBF

and

for the first

was given

Survey’s

on Signy Island (60” 43’S, 45” 36’W),

to the UK,

(Egginton, trout,

et al.,

(Taylor

were caught

and 4°C (winter)

from transportation

f 0.01 + 1.2 * 2.1t + 0.07 i_ 0.077 f 2.9 + 5.4t + 0.016 f 0.28.f

0.13 5.1 10.7 0.14 0.26 9.7 22.3 0.028 0.54

+ 0.01 + 1.6 * 1.8.f f 0.03 k 0.04t + 2.4 & 2.7.f + 0.006 + o.oost

Mean f SEM ml/min/ 100 g (IV = 6, 6 and 8. respectively). *P < 0.05 vs. 4°C; tP c 0.05 vs. rest

temperatures 0. mykiss II‘C

0.11 * 0.004* 27.0 f 8.3* 92.4 + 29.8*t 0.53 + 0.20* 1.35 + 0.35*t 63.3 + 15.6* 218+6l.O*t 1.28 ? 0.23* 3.64 F O.O8*t

Control

150

of tissue blood

405

flow at very low temperatures

1A

90

60

cofiiceps

0

N.

EJ

4OC trout

Ed

11 OC trout

30

??

P.zO.05 vs. 4%

B 0

N.

@

4OC trout

I?#

Rest

RESULTS

hypertrophy body

mass

1996) which

Although

induced

(ventricle in 11” and

a significant

mass = 0.11 4°C

trout;

was not evident

cardiac

and Taylor

4°C

resting

significant

exercise

(Table

manner,

skin were similar

although

trout and Notothenia maintained

mean arterial ferred

in the predicted

blood

(optimal)

pressure

(MABP)

temperatures.

total inverse induced

peripheral trend

resistance to

that

a significant

of

increase

index

was

with estimated

(TPR) HR

showing

(Fig.

MABP

in cardiac

(Fig. 1). With the exception

vascular

variables

and estimated for

Notothenia

was

muscles

gonad

species

also

A

seen

in

in Nototheniu viscera

and

and temperatures,

BF in Notothenia likely due

output

of relative

temperature of 0°C were significantly those of trout at its optimal temperature

its

of the

the

ven-

TPR, all cardioat

Table 2. Blood flow in pectoral locomotory muscles Antarctic teleost Norotheniu coriiceps at 0°C

1). Exercise

(CO) and stroke work at all temperatures (Table I), while reducing TPR and thereby maintaining tricle weight, MABP

with the higher

in

(Fig. 2) poss-

flow in the ventricle, among

than

flow

and pulse pressure.

hyperaemia

locomotory

2). Blood

higher

blood

at their pre-

Cardiac

similar in Nototheniu and 4°C trout,

a similar

pectoral

exercise.

and TPR

exercise

ibly due to the higher MABP most

temperature

and

et a/.,

with en-

vironmental

aerobic

Nototheniu slow muscle was greater

Nototheniu, which had a typical value for teleosts of inversely

maximal

0.13%

in the cold adapted

rate varied

trout

CO was similar

trout,

0.10 rfr 0.01%.

Heart

ll°C

Exercise

Fig. 2. Blood flow in slow (A) and fast (B) trunk muscles at rest and following

Cold acclimatisation

coriiceps

optimal

less than of 11°C.

abductor superficialis erector ventralis abductor profundis adductor superficialis erector dorsalis adductor profundis

Rest

Exercise

3. I f 0.9 2.6 f 1.2 2.7 + 1.1

18.5 + 5.4* 8.2 _+3.4 12.2 + 3.4*

4.7 f 0.9 2.8 * 0.5 3.1 f. 0.8

20.3 & 6.9; 8.6 + 2.3* 19.2 _+3.9t

Mean f SEM ml/min/100 g (N = 6). *P c 0.05, tP < 0.01vs rest.

406

S. Egginton Table 3. Blood flow in other organs, at rest and during exercisefor Nororhenia coriicrps relative to that of rainbow trout Oncorhynchus mykiss acclimatised to winter and autumn temperatures. *P < 0.05 vs 4’C.

ventricle

rest exercise rest

spleen

I .4 + 0.4 3.1 + 1.2 5.1 I I.8 3.6 k I .5 1.510.3 I .o * 0.4 4.8 + 0.60 4. I f 0.9 3.4 * 1.3* 3.4* 1.1* 0.8 f 0. I 0.4 f 0.9

exercise liver

rest exercise rest exercise rest exercise rest exercise

intestine gonad skin

to seasonal parallel any

reproductive

the increased

substantial

ated.

(Nilsson

to other 1996)

sympathetic

peripheral

vertebrates

tor muscles

which,

distinctive

some

evidence

red

flow

of CO to this is likely

of cardiovascular and

hence

influence

tone. However,

have

blood

or at least greatly attenu-

dominance

et al.,

reduced

given the lack of

visceral

and

for selective

may

involve

m. tibialis zones,

perfusion

a

drive and

in the two pectoral white

I .2 + 0.7 2.6 f 1.9 9.3 5 4.x 6.9 + 34 4.9 i_ 2.8 3.9 f 1.9 6.4 + 4.3 15.4 f 8.4 0.6 + 0.4 0.3 f 0. I 0.5 +0.1 0.6kO.l

2.5 f 2.1 6.8 + 5.2 12.8 + 7.9 I.5 + 0.5 I.5 f 0.7 0.9 f 0.7 10.9 i 5.1 20.4 i 9.7 0.5 f 0.4 0.5 f 0.4 1.7*0.1* 1.3 * 0.3*

DISCUSSION

erec-

anterior

there

was

of the most

region (Fig. 3).

The physiological peratures

are most

sequence

of

for

cellular

documented

control

on central

like rodent

0. myki.ys II c

in MBF

an active redistribution

In contrast

oxidative

in

muscle is absent,

due to vagal

Changes

CO which,

change

(Table 3) suggests working

activity.

0. n1rki.v.s 4’C

pathways

inadequate

local and

adaptive

system blood and

removal

Impaired

been observed

in enzymes

from

for

of metabolites

in temperate

of fuels

The cardiorole. as an delivery from from

performance

Exercise

Fig. 3. Blood flow in m. erector ventralis (A,B) and m. erector showing the differential response to exercise in the oxidative

Rest

of

active remote has

zone species at low tem-

*

Rest

ATP have

metabolism.

cardiovascular

of

studies

is essential

as well as transport

depots.

provision

also has an important flow

at low temto be a con-

many

responses

of intermediary

adequate tissue,

to activity considered

respiration,

vascular oxygen

limits often

Exercise

dorsalis (CD) of No/ofhenia coriicrps, (A.C) and glycolytic (B,D) regions.

407

Control of tissue blood floe i at very low temperatures peratures,

which

swimming

capacity

undoubtedly

contributes

Do cold-adapted

species

show

to poor

et al., 1996).

in the cold (Taylor

any further

ment at O”C, i.e., is there any evidence vascular system Given the sparse

optimised to data available

ation/acclimatisation

studies

impair-

for a cardio-

a new set-point? from cold acclim-

no appropriate

com-

this represents

an active control

awaits data on vascular In conclusion, that cardiac

the limited

output

vascular

control

in extreme

the extent predicted reaching

mal temperatures,

do provide

evidence

for some compensation

in car-

tation of the cardiovascular

diovascular

control

at very low temperatures.

The

most

sation lar

clear

evidence

in Nototheniu

to

acclimatised

trout.

temperature

(increased

Nototheniu being

countered

than

at

4”C,

are

appear

Control central

adap-

avoid

relative lead-

in Nototheniu.

This

increased

vascular

as vessel dimen-

among

these

species

higher

vertebrates,

species

for a diversion muscle

in slow

that found

in

situation

in

the

is little evidence

in either

of CO from

the viscera

by active

vasoconstriction

to

blood flow). Increased from

a passive

steal effect. with a local metabolite-induced

vaso-

dilatation flow

providing

that

may, levels showed

could

than

the MBF

is less than

temperature,

Unlike

(which would reduce visceral perfusion

resting

in Nototheniu higher

there

parallels

While

optimal trout.

skeletal

circulation

status.

hyperaemia

acclimatised

muscle

efficient

Other output,

density,

of the peripheral

it is significantly

working

found

vascular

at its higher

muscle

of

then result

a low resistance

accommodates

however,

only

exercise,

impairment

the

be the as

case

Thorarensen

of maximal

path for blood

increased for

CO.

This

sustainable

et a/. (1993)

swimming

perform-

ance in trout following hyperphagia. That active redistribution of MBF may be retained even at the lowest

temperatures

system is found, whereas fails to maintain

adequate

at low temperatures.

is also suggested

Acknolc~ledgements-This work was supported by the Natural Environment Research Council; the British Antarctic Survey generously provided Nototheniu for this study.

rate

the cardiac

is more

to

in either

cardiovascular

trout

heart

observations).

and exercise

cold

TPR

sus-

volume-even

trout.

to be similar

(unpublished

acclimatisation

tissue perfusion

found at higher opti-

these data suggest that cold adap-

of the more

stroke

however,

of

and

lower

Nototheniu

its origin

tone or reduced sions

to that

acclimatised

ing to the higher

levels of performance

to

studies. While not

cold

in the sluggish

with such a low cardiac

have

the effects

mass is less. Clearly,

required.

hypotension

in

viscosity

the

by greater

of cold

compen-

direct

output

with

of cold adapted that

tations

may

blood

cardiac

ventricular

pump

seen the

at 0°C is similar

trout

though

that

Despite

bradycardia)

active

systemic

However,

is given by the lack of a simi-

hypotension

tained

for

seasonal

active tis-

cold is not impaired

from previous

althou

in terms of ecotype,

data suggests

among

sue is not due to regional vasoconstriction.

species

are yet possible

available

redistribution

gh these first data for MBF in an Antarctic

parisons

of local resistance

supply and physiology.

by the selec-

tive regional hyperaemia of the pectoral muscles in exercising Notothenia. Whether

erector or not

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