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First published online June 15, 2006
Journal of Experimental Biology 209, 2515-2524 (2006)
Published by The Company of Biologists 2006
doi: 10.1242/jeb.02277
The origin of mean arterial and jugular venous blood pressures in giraffes
1 Department of Zoology and Physiology, University of Wyoming, 1000 E
University Avenue, Laramie, WY 82071, USA,
2 Physiology: Biomedical and Chemical Science, University of Western
Australia, Perth, Australia
3 Department of Physiology, University of the Witwatersrand, Johannesburg,
South Africa
* Author for correspondence (e-mail: mitchg{at}uwyo.edu)
Accepted 18 April 2006
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Summary |
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We conclude that mean arterial blood pressure in giraffes is a consequence of the hydrostatic pressure generated by the column of blood in the neck, that tissue pressure around the collapsible jugular vein produces the known jugular pressures, and that a siphon does not assist flow through the cranial circulation.
Key words: giraffe, siphon, cranial circulation
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Introduction |
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TOPSummaryIntroductionMaterials and methodsResultsDiscussionReferences |
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; Goetz and Budtz-Olsen,
1955; Goetz and Keen,
1957; Goetz et al.,
1960), Van Citters (Van
Citters et al., 1966; Van
Citters et al., 1969), and most recently by Hargens
(Hargens et al., 1987). These
studies have shown that the cranial circulation of giraffes is unique and
characterized by high carotid artery pressures (
200 mmHg at the heart
compared to 100 mmHg in humans; 1 mmHg=0.33 kPa), and positive jugular
vein pressures. The origin of these pressures is controversial. The
controversy has been reviewed at least six times
(Badeer, 1986;
Seymour and Johansen, 1987;
Pedley, 1987;
Badeer, 1988;
Badeer and Hicks, 1992;
Seymour et al., 1993) and
evaluated empirically five times using mechanical models
(Holt, 1959;
Hicks and Badeer, 1989;
Pedley et al., 1996;
Badeer, 1997;
Seymour, 2000).
From these reviews and experiments two main mechanisms have been suggested
for the origin of giraffe arterial blood pressure. The conventional,
hydrostatic, mechanism predicts that the principal determinants of blood
pressure at the level of the heart will be the required perfusion pressure
plus the hydrostatic pressure generated by the length of the neck. Mean
arterial pressure at the head, calculated from all pressures that have been
measured at the head in giraffes, is 100.3±20.9 mmHg (systolic
128.3±20.2 mmHg; diastolic 78.3±20.2 mmHg)
(Mitchell and Skinner, 1993).
For a head 2 m above the heart, as it often is in giraffe, the hydrostatic
pressure generated by the column of blood in the carotid artery is 2000
mmx1.055 (density of blood)/13.6 (density of mercury), which is 155
mmHg. Thus the pressure generated by the heart should be 255 mmHg. However, in
the same animals from which average cranial arterial pressure was calculated,
heart pressure was calculated to be on average 185±41.6 mmHg (systolic
211.1±37.6 mmHg; diastolic 151.4±32.6 mmHg)
(Mitchell and Skinner, 1993).
This lower than predicted average pressure may be because some of the animals
were anaesthetized at the time of measurement, or were holding their heads at
an average angle less than vertical, or did not have two meter long necks, but
it is also possible that mechanisms exist that reduce the work of the
heart.
Thus, Badeer (Badeer, 1986;
Badeer, 1988;
Badeer, 1997) and Hicks and
Badeer (Hicks and Badeer,
1989) have suggested that as the giraffe cranial circulation can
be regarded as an inverted U-tube that functions as a siphon, gravitational
effects are neutralized and the high pressure results from high peripheral
resistance. Badeer (Badeer,
1997) further suggested that high peripheral resistance is a
consequence of arteries with small lumens plus high sympathetic nervous
system-mediated vasoconstriction, the latter resulting from the absence of a
functional baroreceptor-mediated depressor mechanism.
There is also a third possibility. Giraffe may be hypertensive and have high blood pressure as a result of the mechanisms causing hypertension in humans. This possibility has not been considered seriously but it has also not been eliminated.
In addition to the controversy about the origin of giraffe arterial
pressures, there is controversy about whether gravitational (hydrostatic)
pressure can be neutralized (for example by a siphon) in the cranial
circulation of any animal that stands upright. Hill and Bernard decided that
`the principle of the siphon is not applicable to the vascular system in
which the arteries on the one hand and the veins on the other are of so very
different in distensibility and elasticity'
(Hill and Bernard, 1897), and
more recently other workers (Dawson et al.,
2004; Gisolf et al.,
2005) concluded that a siphon does not operate in the cranial
circulation of standing humans. Holt wrote: `... freely collapsible veins
running from a part above heart level, such as the head, back to the heart can
exert no siphoning effect on the flow of blood to the part'
(Holt, 1959), the reason being
that if the tubes in a siphon system are collapsible (as in the giraffe
jugular vein) the potential energy is lost as frictional heat
(Seymour and Johansen, 1987;
Seymour et al., 1993).
Moreover, if the jugular vein acted as a siphon, the pressure gradient down
the jugular vein would be negative, but, at least in giraffes, it is the
opposite: pressure at the top of their jugular vein is far higher than it is
at the bottom (Hargens et al.,
1987; Mitchell and Skinner,
1993) (see Fig.
1).
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), it was
suggested (Badeer, 1986;
Badeer, 1988; Hicks and Badeer,
1987; Hicks and Munis, 2005)
that the gravitational pressure of blood in the jugular veins can
counterbalance the gravitational pressure in the carotid arteries as long as
sufficient flow exists to establish a continuous column of fluid. This idea
was confirmed (Badeer, 1997) by
using a collapsible tube as the siphon tube in the descending limb of a model.
Flow through the system was greater than if there was no descending limb
(`free fall' flow). He also concluded that high blood pressure `is simply
to minimize the collapse of the vessels in the head and neck', thus
allowing a siphon effect to exist (Badeer,
1997), and that its functional advantage was to reduce the work of
the heart (Hicks and Badeer, 1987). When a pump was used to drive fluid
through a vertical U-tube system, a siphon reduced `heart' work by
12–15% (Hicks and Badeer,
1989), although Seymour et al. could not repeat this result and
concluded that this finding was an artefact
(Seymour et al., 1993). To contribute to these debates we report here some results we have obtained from another mechanical model of the giraffe cranial circulation. The principle of the model was that gravitational and viscous flow pressures could be added or subtracted by various manipulations including creating or breaking a siphon system. The main purposes of the study were to measure and record pressures in both the ascending and descending limbs of the model simultaneously, and to establish the factors that contribute to the known giraffe arterial and jugular venous pressure profiles, which are summarized in Fig. 2. We show that a siphon does not assist cranial flow, and that the origin of the arterial and venous blood pressures in the giraffe cranial circulation is complex.
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Materials and methods |
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The main elements of the model, shown in Fig. 3, are listed below.
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20°C). (2) A submersible pump (Model 3E.12N, Little Giant Pump Co, Oklahoma City, OK, USA) able to deliver precisely regulated flow (F-400 flow meter, Blue White Industries, Hurlington Beach, CA, USA) of water at least 10 liters min–1 at a height of 2 m, irrespective of changes in resistance. Volume flow was regulated in two ways. First by altering the power input using a rheostat (`Powerstat' L116C; variable autotransformer, input 120 V at 50–60 Hz, output 0–140 V at 10 A; Superior Electric Company, Bristol, CT, USA). The power required to produce a given flow allowed an accurate measurement of the work of the pump, and by analogy, by how much heart work might be reduced by a siphon. Secondly, with the rheostat fixed at a specific power output (1000 W), flow was adjusted by altering the resistance in the pump's inflow pipe. Of the two methods, the second produced more stable flows, and was the method used when pump work was not being assessed.
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2 cm longer than the
`jugular' tube to facilitate removal of air bubbles, see below) made of PVC
tubing with an o.d. of 17.1 mm and an i.d. of 12.0 mm. These dimensions
correspond to those of a carotid artery in a (medium sized) giraffe. The
hydrostatic pressure generated by the column of fluid in a tube of this length
is 122 mmHg (1660/13.6). The resistance to fluid flow (viscous flow
resistance) offered by this tube was 31.8±0.5 mmHg l–1
min–1, which is within the range of 26.6–38.6 mmHg
l–1 min–1 calculated from known pressures
and blood flows in giraffe: pressure gradient=
P=85 mmHg;
=2.2–3.2 liters
min–1 (Mitchell and
Skinner, 1993).
(4) A `jugular' tube of 1638 mm in length that also could be made rigid
(using PVC tubing) or collapsible (using rubber, `flat-style', Gooch tubing
cat. no. 75-1000-82, PGC Scientifics, Frederick, MD, USA). This Gooch tubing
had a flat width of 31 mm and a round diameter of 25 mm, dimensions that are
similar to those of a giraffe jugular vein. The hydrostatic pressure at the
bottom of a stationary column of water in this tube, compared to the top,
would be 120 mmHg. The resistance offered to fluid flow was 0.2–1.2 mmHg
l–1 min–1, whereas in giraffe it is
5–7 mmHg l–1 min–1
[P=16 mmHg;
=2.2–3.2 liters
min–1 (Hargens et al.,
1987; Mitchell and Skinner,
1993)]. A valve was placed at the top of the `jugular' tube so
that the tube could be opened or closed to the atmosphere. With the valve
opened to the atmosphere any siphon effect being produced in the descending
`jugular' limb of the model could be broken.
(5) A `cranial' circulation that could be made rigid (using the same PVC tubing used to make the `carotid' tube) or collapsible by replacing the PVC tube with the `flat-style' Gooch tubing.
(6) Six pressure transducers (PX 143, Omega Engineering, Inc., Stanford, CT, USA) measuring pressures between –258 and +258 mmHg at 0.1 mmHg intervals. Three were placed in the `carotid' limb (P1, P2, P3; Fig. 3) and three in the `jugular' limb (P4, P5, P6; Fig. 3).
The collapsible `brain' tube (between P3 and P4) and each collapsible
section of the `jugular' tube (between P4 and P5, P5 and P6, P6 and the exit)
were enclosed in clear PVC tube with an o.d. of 60 mm, and an i.d. of
50 mm (i.e. much greater than the diameter of the Gooch tubing), such
that it formed an airtight container around each section. Each of these
containers was attached to a mercury sphygmomanometer so that a precise
external pressure (mmHg) could be applied to them to create a transmural
pressure equivalent to the capillary hydrostatic pressure necessary to
maintain filtration pressure, or positive pressures generated by cerebrospinal
fluid, or to increase ascending limb hydrostatic pressure so simulating a
longer neck (`brain' tube), or tissue pressure, or venoconstriction (`jugular'
tube).
Experimental design
We made the assumption that functions of the giraffe cranial circulation
could be addressed as if it consisted of a single afferent tube to the head
and a single efferent tube. We also assumed that a giraffe carotid artery
containing blood at a pressure of between 100 and 200 mmHg is for all
practical purposes rigid even though its mix of elastic and collagen fibers
(Franklin and Haynes, 1927;
Goetz and Keen, 1957;
Kimani and Opole, 1991)
produces a windkessel effect. We also assumed that flow throughout
the length of a carotid artery or a jugular vein is constant. It is not. Flow
in the carotid artery decreases as it loses blood to tissues via
tributaries and flow in the jugular vein increases as it gets nearer to the
heart as it collects blood from tributaries.
Unlike other mechanical models of the giraffe cranial circulation
(Seymour and Johansen, 1987;
Hicks and Badeer, 1989;
Pedley et al., 1996;
Badeer, 1997) but like
Seymour's model (Seymour,
2000), our model contained a `brain' circulation that could be
made rigid to simulate Goetz's `deep, non-collapsible venous channels'
(Goetz et al., 1960) or the
effects of positive or negative cerebrospinal fluid pressure, or collapsible
to represent a physiological microcirculation in which an internal pressure
for achieving filtration exists, but which is subject to collapse if
transmural pressure falls towards zero. Similarly the `jugular' limb could be
rigid to represent a jugular vein supported by extravascular connective tissue
or filled by a high volume flow of blood, or one that was collapsible to
represent its normal, observed, physiological state. The model does not take
into account the possibility of two parallel, simultaneously operating, venous
drainage systems – one rigid (venous plexuses) and one collapsible
(jugular vein) as did Seymour's (Seymour,
2000).
The model allowed for the following. (1) Four different tube configurations: (i) all rigid; (ii) carotid and brain rigid, jugular collapsible; (iii) carotid and jugular rigid, brain collapsible; (iv) carotid rigid, brain and jugular collapsible, the combination presumed to occur in giraffe. (2) Three flow states: (i) `siphon', or (ii) `pump-driven', and (iii) a combination of these. (3) Many combinations of flows, pressures and resistances, all in the physiological range of giraffe.
The purpose of the experiment was threefold. First, we wanted to establish the pressures and flows that could be generated by a siphon. Secondly, we wanted to establish what pump-driven pressures in the ascending carotid and descending jugular limbs of the model were, whether these pressures were affected by a siphon, what effect collapsible tubes representing the head and neck microcirculations and jugular vein had on `carotid' pressures, and what effect different fluid flow rates and external pressures had on `carotid' and `jugular' pressures. Thirdly, we wanted to try and replicate the combination of flows, and resistances to flow, that produce the pressures that are known to exist in the giraffe cranial circulation in order to understand the factors that may contribute to them.
The system was calibrated by using the rigid tube configuration and filling the tubes with water, with no siphon tube attached, and no flow. Gravitational pressures measured by pressure transducers at each height above water level were adjusted to predicted values. Predicted values were P1=–11.8 mmHg, P2=–61.1 mmHg, P3=–122.1 mmHg, P4=–120.4 mmHg, P5=–66.4 mmHg, P6=–32 mmHg.
At least three measurements of pressures were made during steady state flow rate or test procedure over a period of a few minutes. Statistical analyses were done using Students t-test. P values of less than 0.05 were regarded as significant.
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),
could be produced through the model by a passive system such as a siphon
alone, i.e. in the absence of pump driven flow. Preliminary experiments were
done using the `all rigid' configuration, in which the jugular tube was either
the same length as the carotid tube, or lengthened by up to 400 mm below water
level by attaching lengths of rigid PVC tubing to its exit. When the two tubes
were the same length there was no flow. With a rigid extension tube attached
to the jugular tube exit the flow rate increased from 0.32 liters
min–1 (at 5 mm length) to 3.3 liters min–1
(at 400 mm length, which equals a siphon pressure head of 29.4 mmHg). These
data confirm a ubiquitous finding about which there is no controversy, namely
that a siphon can generate large flow. In all subsequent experiments a 400 mm
rigid extension tube attached to the bottom of the jugular tube was used to
establish the siphon effect.
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Collapsible tube configurations
There was no flow when any part of the model contained a collapsible tube,
and `carotid' pressures were not altered by a jugular extension. In the
collapsible jugular tube, pressures were always negative, and became more so
when the extension tube was attached (Fig.
4B–D), but when the valve at P4 was opened all pressures in
it reverted to atmospheric pressure (not shown).
We conclude that a siphon has no effect on `carotid' pressures and cannot
produce flow if any part of the system is collapsible. Zero flow confirms
previous conclusions that resistance in collapsed tubes is high, and that
collapse prevents a siphon effect (Holt,
1959; Seymour et al.,
1993; Seymour,
2000).
Pump flow
Rigid tube configuration
When all the tubes were rigid, pump flow rate at 4 l
min–1, and the valve at P4 closed, it was obvious that a
siphon can assist flow, can significantly reduce pressures throughout the
system by the amount of the siphon pressure head (approximately 30 mmHg), and
can reduce the work of the pump, as suggested by Hicks and Badeer
(Hicks and Badeer, 1989)
(Table 1;
Fig. 4E). For example at the
`heart' level (P1), in the absence of a jugular extension the pressure at P1
was +22.8±0.5 mmHg. When an extension tube was attached, P1 decreased
to the predictable –7.2±0.4 mmHg. The power needed to generate 4
l min–1 flow in the absence of the extension tube was 645 W.
With the extension tube in place the power needed was only 465 W (i.e. about a
30% decrease).
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Fig. 4E also shows that if the siphon effect was broken by opening the valve at the top of the rigid jugular tube (P4) to the atmosphere, then the pressures in the jugular limb became atmospheric, those in the carotid limb became equivalent to the height of the water column, and the power consumption of the pump required to maintain a flow of 4 l min–1 increased to 900 W (Table 1).
In all these experiments viscous resistance
(P/) in the carotid
arm did not change: it was 31.8±0.5 mmHg l–1
min–1 (P=127.3±2.2;
=4 liters min–1).
Thus the decrease in `carotid' pressure and reduction in the work of the pump
when the jugular extension was present and a siphon was operating, can be
attributed to the subtraction of the effect of gravity and not to a change in
viscous resistance.
Collapsible tube configurations
In contrast to the all rigid configuration, if either the cranial or
jugular tube, or both, was a collapsible tube then the jugular extension had
no effect on the `carotid' pressures generated by the pump. With a jugular
extension tube attached, carotid limb pressure at P1 was between 121.7 and
134.7 mmHg. In the absence of a siphon effect `carotid' pressure was between
123.4 and 135.9 mmHg, with the latter values not significantly different from
those recorded when the jugular extension tube was attached
(Fig. 4F–H). In the
collapsible jugular tube, pressures were always close to atmospheric, but the
pressure measured at its top (P4) was usually slightly positive and greater
than it was at the bottom (P6), as in giraffe
(Hargens et al., 1987)
(Fig. 2), whether the extension
tube was attached or not.
We conclude that a collapsible tube establishes an isolated column of fluid in the ascending limb that exerts a gravitational, hydrostatic pressure that determines `carotid' pressures. Confirmation of this conclusion is that the work of the pump was unaltered by the presence of an extension tube: power output to maintain flow was approximately 900 W in all cases (Table 1). Further confirmation of these conclusions is that breaking the siphon had no effect on `carotid' pressures or the work of the pump (Fig. 4F–H; Table 1).
The effect of `jugular' cuff constriction
A muscular cuff is present in the wall of the anterior vena cava of giraffe
at the point just proximal to its entry into the right atrium
(Goetz and Keen, 1957). Its
function is unknown but its morphology suggests that it can constrict. One
consequence of constriction could be generation of the typical giraffe jugular
pressure profile. Fig. 5 shows
changes in pressures when an external, `tissue' pressure of 120 mmHg was
applied to the lowest part of the model's jugular tube (R4,
Fig. 3), to simulate
constriction. A typical jugular pressure profile did not result. All pressures
in the system increased with `carotid' pressures increasing less than did
`jugular' pressures. The `jugular' pressure gradient was reversed: pressures
at the top of the `jugular' tube (P4) were less than those in the middle (P5)
or at the bottom (P6).
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P/ across the `brain'
circulation fell from 6 to 2 mmHg l–1 min–1,
because the pressure gradient between P3 and P4 decreased from 24 mmHg to 7
mmHg while flow remained the same.
The effect of `cranial' circulation resistance on `carotid' limb pressures
Blood needs to be delivered to the head at a pressure that will support
microcirculation hemodynamics. The requirement for a filtration pressure can
be simulated in our model by applying an external pressure to the `brain'
collapsible tube. Adding an external pressure at R1
(Fig. 3) reduces the diameter
of the tube and so is the equivalent of increasing cranial resistance.
When we increased cranial resistance, `carotid' pressures increased in proportion to the increase in external pressure at R1 (Fig. 6A,B); to overcome the resistance an increase in hydrostatic pressure was required.
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Replicating giraffe cranial pressures
We tried to replicate the known giraffe pressure profile, using
combinations of flows and external resistances in the `giraffe' tube
configuration. The external pressure around each segment of the jugular tube
was adjusted so that `jugular' pressures corresponded to the known pressures
(shown in Fig. 1) in the
jugular vein, namely approximately 14 mmHg at P4, 10 mmHg at P5 and 7 mmHg at
P6. At the same time, flow rates of 4–6 liters min–1
were produced, `brain' circulation external pressure was maintained at 40 mmHg
(a value assumed to be physiological), and pressures in both the carotid and
jugular limbs were measured.
The calculated mean giraffe `heart' pressure of 185 mmHg
(Mitchell and Skinner, 1993)
was established when brain resistance was 40 mmHg, and flow rate was 6 liters
min–1 (Table
2; Fig. 2). The
calculated cranial pressure of approximately 100 mmHg at P3
(Mitchell and Skinner, 1993)
was established when the external pressure at R1 was 80–100 mmHg (not
shown). Known jugular pressures (Hargens
et al., 1987) were reproduced by `tissue' pressures equivalent to
2–4 mmHg. These pressures are close to the 1 mmHg found by Hargens et
al. (Hargens et al., 1987),
the general tissue pressure of 1 mmHg estimated by Guyton
(Pedley et al., 1996), and
those obtained by Seymour from his model
(Seymour, 2000).
Overall these data reveal that the giraffe cranial pressure profile depends on a complex interaction between hydrostatic pressure, fluid flow rate, vessel wall (viscous) resistance and tissue pressure, which cannot be replicated by the model with a single common combination of these factors.
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), and has been supported, mainly by Badeer and colleagues, in
several articles (Badeer, 1986;
Badeer, 1988;
Hicks and Badeer, 1989;
Badeer and Hicks, 1992;
Badeer, 1997). Goetz
(Goetz, 1955), who in 1955 was
the first to study giraffe blood pressures, encapsulated the idea by asking
`whether the left ventricle does provide the moving force unaided or
whether it is assisted in its task by other mechanisms such as a peristaltic
wave along the carotid artery or a siphon effect of the venous blood carrying
down the jugular vein helping to `elevate' the blood in the carotid
artery' (Goetz and Budtz-Olsen,
1955). After making measurements of giraffe blood pressure Goetz
and Keen concluded that the giraffe cranial circulation proceeded unassisted
by siphons or peristalsis although it was `doubtless aided by
subatmospheric pressures at the brain level'
(Goetz and Keen, 1957). Goetz
and colleagues (Patterson et al.,
1957; Warren et al.,
1957) later concluded, however, that there was no `necessity
for any important contribution to cerebral perfusion pressure from negative
venous pressure at brain level'
(Patterson et al., 1965).
If a siphon does exist then the origin of arterial blood pressure suggested
by Badeer (e.g. Badeer, 1997)
is high peripheral resistance caused by small vessel lumens, and excess
sympathetic tone, itself the product of an ineffective baroreceptor mechanism.
However, the giraffe has a highly functional baroreceptor system
(Kimani and Mungai, 1983;
Millard et al., 1986;
Mitchell and Skinner, 1993),
so excess sympathetic tone arising from its absence is unlikely. Furthermore
the density of sympathetic innervation of arteries is inversely related to
vessel wall thickness and with height, so peripheral constriction is at best
likely to be poor (Nilsson et al.,
1988). Calculated peripheral resistance in giraffes is 2 mmHg
l–1 min–1, which is one-tenth that in
humans, and this value supports the view that their peripheral resistance is
not the source of high arterial pressure. In addition, the data we report here
were obtained from a model in which there was no peripheral resistance
component other than that in the model itself, and no sympathetic nervous
system, and yet the pressures produced in it are very similar to those found
in giraffe.
There is also little anatomical or physiological evidence that a siphon
mechanism exists in the cranial circulation of giraffe. The arterial and
venous arms of the cranial circulation are not known to be connected by
anastomotic channels and they are not similar to an inverted U-tube. They are
separated by extensive intracranial and extracranial capillary beds consisting
of highly permeable vessels. For these capillary beds to function, capillary
pressure must be greater than colloid osmotic pressure. Colloid osmotic
pressure of giraffe blood is about 25 mmHg
(Hargens et al., 1987;
Mitchell and Hattingh, 1993)
the same as it is in other mammals. Thus capillary hydrostatic pressure must
be greater than 25 mmHg. Textbook values for microcirculation pressures are,
at the arterial-end, 35 mmHg with mean capillary hydrostatic pressure about 20
mmHg, which are not compatible with siphon-assisted flow. Therefore, the heart
must generate a pressure that overcomes hydrostatic pressure generated by the
column of blood in the carotid artery, the peripheral resistance of the
cranial microcirculation, and that delivers blood to the cranial tissues at a
pressure sufficient to ensure filtration.
This conclusion is supported by calculations of expected hydrostatic
pressure. Calculated values fit exactly with the known dimensions of giraffe
cranial vessels and with their measured arterial pressures (e.g. Goetz and
Budtz-Olson, 1955). It is also supported by the data we report here and that
collected by Seymour (Seymour,
2000). We have shown here that adding or subtracting gravity by
various manipulations, or breaking the siphon in the jugular limb by allowing
air to enter the water column, does not alter carotid tube pressures, except
when all the tubes are rigid. When they are rigid, breaking the siphon results
in carotid pressures identical to those measured in it when the tubes are
collapsible. These results show, therefore, that gravity accounts for most of
arterial pressure.
The lack of a siphon effect is in one sense a pity. If a siphon did exist
it would, as our data show (Table
1), and as first proposed by Hicks and Badeer
(Hicks and Badeer, 1989),
produce a significant decrease in heart work. When the pump was producing flow
through rigid tubes in our model, a siphon reduced the work of the pump by
half. When Hicks and Badeer introduced collapsible tubes they found that a
siphon decreased heart work by 12–15%
(Hicks and Badeer, 1989), but
we could not replicate this result (Table
1).
Assessing the contribution of viscous resistance
Giraffe cranial resistance is known to double when they raise their heads
and we suspect this is the consequence of extracranial blood vessel
constriction (Mitchell and Skinner,
1993). Data from our model show that reducing the radius of the
tubes by applying external pressure, increases resistance and increases
`carotid' pressures significantly. Changes in flow rate have a less marked
effect on `carotid' pressures. Reducing the radius of the jugular tube had no
effect on'carotid' pressures.
There was, however, an interesting effect of constriction of the lowermost
resistance in the jugular tube (R4, Fig.
3). This manipulation simulated contraction of the muscular cuff
in the anterior vena cava (Goetz and Keen,
1957). The function of the cuff is unknown, but there are at least
three potential functions. One function is that it might reduce the flow of
blood into the right atrium during head-raising. The amount of extra blood
that collects in the jugular veins when a giraffe is drinking can be
calculated to be about 20 liters. The heart would be unable to accommodate
this volume if it emptied into the right atrium when the animal lifts its
head. If the cuff constricts as part of the head raising reflex then flow into
the atrium would be less impetuous. A second possibility is that it constricts
when a giraffe lowers its head so reducing regurgitation of blood from the
inferior vena cava and right atrium into the jugular vein. A third possibility
is that it provides jugular resistance and thus contributes to the
counter-gravitational pressures in the vein that are unique to giraffe. Our
model showed that simulation of cuff constriction did not result in
counter-gravitational pressures, but it did show that cranial resistance was
lowered when this part of the jugular tube was constricted
(Fig. 5B). It is conceivable
therefore that if the jugular cuff constricted during head-raising, when
extracranial constriction is counterbalanced by diversion of blood to the
brain via the occipitovertebral anastomosis
(Mitchell and Skinner, 1993),
then a lowering of cranial resistance could promote cerebral perfusion and
contribute to the prevention of fainting in a very elegant orthostatic
reflex.
Reconstructing giraffe cranial pressures
The giraffe cranial circulation is continuously exposed to changes in
gravitational pressure and to changes in blood flow. To simulate this variety
of circumstances we changed flow rate and external resistances in the model to
establish what combination of flows and pressures best replicates the known
pressure profile in giraffe. As might be expected no particular combination
recreates the profile. What is difficult to replicate is a pressure at the
head of 100 mmHg, and at the same time typical heart pressures of 185 mmHg.
This difficulty suggests that the factors that contribute to cranial
resistance are too complex to replicate in a model.
Venous pressures
Apart from establishing the origin of arterial pressures, the data
generated by our model also support the conclusion that the origin of giraffe
positive and inverted jugular pressures is tissue pressure. Holt
(Holt, 1959) predicted that
jugular pressures should be zero. For the pressures to be positive viscous
resistance must be greater than the force of gravity. Seymour and colleagues
(Seymour et al., 1993;
Seymour, 2000) concluded that
tissue pressure was responsible and that the linearity of decrease could be
attributed to a similar decline in tissue pressure. Our model showed that the
amount of tissue pressure needed was small, similar to that measured by
Hargens et al. (Hargens et al.,
1987), was fairly constant throughout the length of the `neck',
and decreased at high flow rates when the tube itself offered resistance to
flow.
Pedley et al. concluded that three factors in addition to tissue pressure
were also important (Pedley et al.,
1996). These were the degree of collapse of the vein, wall
compliance and flow rate. They also suggested that the origin of tissue
pressure lay in the thickness of giraffe skin (15 mm). An analysis of this
last possibility found that the average thickness of head and neck skin from
six different sites in a giraffe was uniform, 5.7±0.1 mm, and not
different to its thickness in the legs (4.7±1.2 mm). The thickest skin
was over the trunk (9.2±1.8 mm)
(Mitchell and Skinner, 2004).
However, giraffe skin is completely collagenous
(Mitchell and Skinner, 2004)
and can be assumed to be very inflexible.
We think that in order to account for the lower resistance in our model's jugular tube (1 mmHg l–1 min–1) compared to that in a giraffe's jugular vein (6 mmHg l–1 min–1) another factor is important. This factor is the viscosity of blood. Blood is four times more viscous than water and, therefore, from Poiseuille's equation, will offer higher resistance to flow. Thus tissue pressure, perhaps arising from inflexible skin, in addition to blood viscosity, are the most probable sources of jugular resistance in giraffe and are sufficient to create the inverse positive pressures found in them.
In summary our data combined with those from other studies have established
that giraffe mean arterial (heart) pressure is a consequence of a
baroreceptor-regulated mechanism that results in the generation of sufficient
hydrostatic pressure to overcome gravitational effects, and to supply the head
with blood at a pressure of 100 mmHg. No siphon effect is needed. The
counter-gravitational, positive, jugular venous pressures found in giraffes
are a consequence of viscous resistance resulting from a combination of blood
viscosity and tissue pressure.
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Acknowledgments |
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References |
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TOPSummaryIntroductionMaterials and methodsResultsDiscussionReferences |
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