Beruflich Dokumente
Kultur Dokumente
functional
analysis
of gas exchange organs in vertebrates
JOHANNES
PIIPER AND PETER SCHEID
Abteilung Physialogie, Max-Plan&Institut
fiir experimentelle
D-3400 Gtittingen, Federal Republic of Germany
PIIPER,JOHANNES,
AND PETER SCHEID.M~~~Z~~OTa comparative functional
analysis of gas exchange organs in vertebrates. J. Appl. Physiol.: Respirat. Environ. Exercise Physiol.
53(6): 1321-1329, 1982.-The
analysis of external gas exchange
in the various respiratory
organs of vertebrates
is based on
models with gas transport properties determined by ventilatory,
diffusive, and perfusive conductances
and by the geometric
arrangement
of medium and blood flows. The following factors
are examined: water vs. air as external medium; gas transport
properties of blood; diffusive gas transfer between medium and
blood; problems in assessing diffusion limitation
in fish gills,
amphibian skin, avian lungs, and mammalian
lungs. Finally the
limitations to the analysis imposed by various physiological
and
anatomical complexities
are discussed.
gills; skin; lungs; water-air
dium-blood
diffusion
breathing;
me-
BRIEF
REVIEW
is to provide an introduction to comparative physiology of gas exchange mechanisms in vertebrates. Emphasis has been placed on the
physical and physicochemical properties of the media
involved (air, water, tissue, and blood), the anatomical
structure of the respiratory organs, and the application
of simplified models to analysis of external gas exchange.
Many aspects of importance in respiration, such as mechanics of breathing, acid-base balance, control of ventilation and blood flow, metabolic rate, and allometric
relationships, have not been considered. The selection of
examples and literature references is not meant to be
complete or even representative and is obviously biased
in favor of work performed in our laboratory.
A general model that serves as a discussion of the basic
variables involved is presented first. Thereafter, the individual models for the different respiratory organ
types-gills, skin, and lungs-are treated. The problems
in applying simple models to the complex real gas exchange organs are pointed out throughout and particularlyin SECTIONS
IV and VI.
The interested reader is referred to recent monographs
and reviews dedicated to comparative physiology of respiration: general (7, 23, 27, 35, 51, 65, 67, 70), vertebrates
(18, 20,45, 76), fish (21, 22, 25, 56)) reptiles (ll), and birds
(10, 60).
MODEL:
CONDUCTANCES
Copyright
Physiological
(2)
v*prn
(3
(0
,B= dC/dP
I. GENERAL
Me&in,
Gdiff
Society
M/(prn
pb)
(5)
1321
1322
J. PIIPER
AND
P. SCHEID
III.
1.
coa.
II.
EXTERNAL
MEDIUM:
WATER
VS.
AIR
< PO&r)
pco,(air)
GAS
TRANSPORT
BY
BLOOD
by Blood
In mammalian blood, physical solubility of 02 is relatively small compared with chemical binding to hemoglobin. However, the relative role of physical solubility (LX)
becomes more important in animals with low 02 capacity
(low hemoglobin concentration) and at low temperatures,
where CYis increased. In the Antarctic icefish (Chaenichthyidae), which contains hemoglobin-free blood, all 02
transport by blood is through physical solubility (17).
For equal Oz-binding properties (see below), Do, for
blood is nearly proportional to hemoglobin concentration. Whereas blood hemoglobin concentration among
lower vertebrates is variable, it is remarkably constant
among mammals and birds, about 11-16 go100 ml-,
corresponding to an 02 capacity of 15-21 ~01%. Since an
increase in hemoglobin concentration by polycythemia
increases the viscosity of blood and leads to disturbances
of microcirculation, the physiological red cell concentration appears to represent a compromise between 02
capacitance of blood, energy requirements for the heart,
and stability of microcirculation.
Aside from the 02 capacity, blood 02 carriage is customarily characterized I) by the half-saturation pressure
of 02 (P&, 2) by Hills coefficient (n), and 3) by the
extent of the Bohr and Root effects.
The PO, value for the same saturation range increases
with decreasing Pm in a nearly proportional manner when
the general shape of the dissociation curve remains unchanged. On the other hand, the physiologically possible
range of arterial and venous PO:! is set by other factors.
Therefore, PIjomay be considered as adjusted to the PO:!
range, being not far from the venous values. This is
understandable, since around and below Psothe slope of
the O2 dissociation curve is at its maximum (if Hills n is
not close to 1.0, see below). The important dependence
of PsOon temperature and the intraerythrocyte
concentration of allosteric modifiers-inorganic
phosphate,
adenosine triphosphate, guanosine phosphate, inositol
pentaphosphate, and 2,3-diphosphoglycerate-has
been
extensively analyzed (2, 3).
For equal P5o, increase of Hills n increases the sigmoidicity of the Oz-dissociation curve. This entails an
increase of p around Psoand a decrease of p at high and
low Po2 values. Since the middle range of 02 saturation
GAS
EXCHANGE
ORGANS
IN
AND
G AS
EXCHANGE
BLOOD:
DIFFU
BETWEEN
R;I = K*(Pl
- Pz) *A/l
(6)
DQX
(7)
5, the
of Diffusion
Limitation
MEDIUM
SION
by Blood
1323
VERTEBRATES
Conductance
Exchange
of CO2 and
02
1324
J. PIIPER
= R~[(D40,/(Ddco,]
(10)
Since for the gas phase ~o,/aco, equals unity and the
ratio Do~/Dco~ is about 1.4, the slope of the diffusion R
lines for R = 0.85 is about 1.2.
For the lungless salamander,
Desmognathus
fuscus,
the cutaneous gas exchange has been shown to be mainly
diffusion limited (42). Since the KcoJKo:!
ratio for tissue
is about 20, the slope of the diffusion R line for R = 0.85
is about 0.043. This value is close to the convection R
line for wat.er breathing (see SECTION
II).
Therefore the
low PCO~ measured in mixed cardiac blood of these
animals (6 Torr) becomes understandable.
Problems in Assessing Diffusion
Real Organs vs. Models
Limitation:
AND
P. SCHEID
MODELS
AMPHIBIAN
AND
MAMMALIAN
FOR
SKIN,
GAS
EXCHANGE
AVIAN
IN
FISH
GILLS,
LUNGS,
LUNGS
GAS
EXCHANGE
Fish
Secondary
QRGANS
gills
IN
1325
VERTEBRATES
Bird
lung
Mammalian
lamellae
4lveolus
lung
Amphibian
A Ventilation
Skin
load
liar ies
Ventilator
y water
flow
Ventilatory
Counter-current
air
PO01 I
Blood
capillaries
FIG. 2. Basic
structural
and functional models for analysis of external
gas
exchange
in vertebrates.
I, inspiratory;
E, expiratory;
a, arterial;
v, venous.
Open
i=e
i
a
-e
a-c
surface
f (ow
Cross-current
skin
The countercurrent
flow of water and blood appears
to result from the anatomy of the gills in both teleost
and elasmobranch
fish (56).
The countercurrent
model offers the highest inherent
efficiency of all gas exchangers,
since the outflowing
blood approaches equilibrium with the inflowing medium
and the outflowing medium approaches equilibrium with
the inflowing blood.
The condition of perfect or near-perfect
equilibration
has never been observed in fish. In most cases even a
crossing-over
of blood and water partial pressures (i.e.,
and Pace,< PECO,) is not observed. This
Pa0,>
-0,
reduced efficiency may be attributed to diffusion limitation and/or to functional inhomogeneities
(unequal distribution of water to blood flow, water shunt, and blood
shunt) e
A more comprehensive
analysis of 02 transfer has been
performed in the rainbow trout (57), in the carp (24), and
in the dogfish, Scyliorhinus
stellaris (40) and S. canicula
(66)
The O2 data measured in S. stellaris could satisfactorily be explained using the estimates of the diffusion
resistances of the blood-water
barrier based on morphometric data and of the interlamellar
water based on
model calculations
(61), thus leaving little space for inhomogeneity
effects and blood shunting (63). The very
variable and frequently very low Pao, observed in some
teleosts, e.g., in the carp (24), suggests occurrence
of
considerable shunting of water or blood.
The COz exchange deserves particular interest, but its
experimental study is difficult because the PCO~ values in
water and blood are very small and close to each other.
The blood-to-water
gradients for Pco~, usually about 2
Torr, are even smaller than anticipated from 0% exchange
on the basis of Kroghs diffusion constants for tissue (40).
This high efficiency of blood-water
CO2 equilibration
may be interpreted to indicate that limitation by reaction
kinetics is of minor importance
or that 02 exchange is
depressed due to inhomogeneity
or reaction kinetics.
B. Open Model for Amphibian
Skin
1326
J. PIIPER
predominantly
in the lung. This behavior is independent
of the outer medium of cutaneous gas exchange (air or
water).
TABLE
diffusing
Model
for Parabronchial
VI.
LIMITATIONS
Variable
OF
THE
Capacitance
ANALYSIS
Coefficient
of Blood
nk
D = C D, = C (p %
n=l
n=l
rn-
)
bn
(11)
For the ventilated pool model of alveolar lungs the alveolar partial pressure (Pm) is constant, and the integration
is performed from mixed venous to arterial values. For
optimization it is recommended
to decrease the pjIn steps
in the flatter part of the dissociation curve.
For the crosscurrent
model of parabronchial
lungs, a
Bohr integration must be made for each cross-sectional
element of the parabronchus,
with Pm constant, at a
value determined by the combined &?I in upstream elements. The mixed arterial partial pressure results from
(PI
PE)
(Pa - Pv)
Crosscurrent
Ventilated
Open
pool
system
D, diffusing
capacity;
M, transfer
rate; PI, PE, Pa, and Pv, inspiratory, expiratory,
arterial,
and venpus partial
pressures,
respectively.
* When PI - PE = Pa - Pv, D = M/(PI
- Pa) = M/(PE
- Pv).
mixing of end-capillary
blood from each cross-sectional
element. Starting from PI and Pv, the experimental
&!I,
Pa, and PE are approximated
by trial and error.
For the countercurrent
model of fish gills the Bohr
integration is much simpler, consisting of a single integration starting at the one end with PI and Pa and ending
at the other end with PE and Pv.
All the procedures are also applicable to COZ. Usually
the blood CO2 dissociation curve between the venous and
the arterial values can be considered as linear, and the
equations of Table 1 may be used.
Metabolism
Equation
Countercurrent
The appropriateness
of the crosscurrent,
or serial-multicapillary,
model for analysis of gas transfer in avian
lungs is supported by the experimental
finding that reversal of gas flow in parabronchi
does not alter the
efficacy of air-blood gas transfer (62) as well as by anatomical evidence (9).
As for maximum inherent efficacy, the crosscurrent
model is inferior to the countercurrent
model. However,
for COa exchange the crosscurrent
model can achieve an
unexpectedly
high efficiency when combined with the
Haldane effect, which enables end-expired Pcoz to exceed
P&o, (33)
Comparison
of the performance
of the crosscurrent
model of avian lungs with the ventilated pool model of
mammalian lungs clearly shows the higher efficacy of the
crosscurrent
system. However, the Pao, is usually found
to be lower than end-expired PO, also in birds, although
the model predicts the reverse for the ideal crosscurrent
model. Apparently
diffusion limitation
and functional
inhomogeneities
reduce the overall gas exchange efficiency, more for O2 than for COS.
P. SCHEID
1. Equations
for calculating
capacity for the various models
Model
C. Crosscurrent
Lungs of Birds
AND
of the Exchange
Organ
The analysis of gas exchange is based on the assumption that the O2 consumed and the CO2 produced by the
gas exchange organ are of no influence, either because
their metabolism
is small in relation to the body or
because the 02 requirement
of the gas exchange organ is
covered from other sources (arterial blood).
The 02 consumption
of mammalian lungs appears to
be small when related to the total 02 uptake. Fish gills,
however, are the site of energy-consuming
active electrolyte transport and therefore are expected to have a higher
02 consumption
(and CO2 production).
Based on measurements in isolated teleost gills, about 7% of the total
02 consumption
was estimated to take place in gills (26).
Gas Exchange
at Accessory
Sites
State
GAS
EXCHANGE
ORGANS
IN
1327
VERTEBRATES
Medium:
According to the general arrangement of the circulatory system and to its connection with the respiratory
organ it can only be expected in fish, birds, and mammals
that 1) systemic arterial blood is essentially identical
with the blood leaving the respiratory organ and 2)
respiratory organ perfusion is close to the body perfusion
(cardiac output). In amphibians and reptiles central (intracardiac and extracardiac) blood mixing may lead to
considerable deviations from these conditions.
However, in fish there is also anatomical or functional
evidence for the following kinds of accessory vascular
pathways (30, 68, 72): 1) channels leading from afferent
to efferent branchial arteries bypassing secondary lamellae; 2) vessels leading from parabranchial arteries via the
central vein of the filament to the venous system; and 3)
anatomically more numerous connections between postbranchial arteries and the venous system of the filaments
(this is probably the nutritive circulation of the gills,
analogous to bronchial circulation in mammals).
From the viewpoint of gas exchange, vessels of type 1
would lead to a true shunt or venous admixture to
postbranchial blood, whereas the vessels of types 2 and
3 would decrease the extent of extrabranchial body perfusion relative to gill perfusion, but they would not produce venous admixture. These alternative pathways
should also be considered if effective gill perfusion or
cardiac output is calculated from branchial 02 uptake
and systemic arterial-to-mixed venous 02 concentration
difference (Fick principle).
In reptiles, with the exception of the crocodiles, the
ventricular septum is incomplete, and in crocodiles there
is an opening (foramen Panizzae) between the roots of
the arterial trunks originating in the left and right ventricles. Thus in all reptiles blood mixing between the
right and left heart or their outflow channels is possible
and has been observed (75). In lizards simultaneous rightto-left and left-to-right shunt has been observed (4).
Since in amphibians the ventricular septum is totally
lacking, the finding of rather restricted arteriovenous
mixing in the bullfrog is remarkable (69). Further complications arise from the fact that part of the skin is
supplied by systemic arterial branches (with arterialized
blood), part by venous blood via the pulmocutaneous
artery (34). The outflow of blood from the skin is to the
venous system. The external gills, when persisting in the
adult, are functionally similar to skin, but their blood
outflow is into the arterial system (like in fishes). In the
lungless plethodontids, in which skin (and buccal mucosa) is the only site of gas exchange, the circulatory
system is secondarily simplified into a system where the
gas exchange organ is in parallel to the systemic capillaries (in contrast to fish, birds, and mammals) and where
all organs, including skin, receive blood of the same
composition (mixed cardiac blood) (12).
VII.
CONCLUSION
1328
further investigation
animal groups.
J. PIIPER
of the respiratory
function
in these
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