Cutaneous blood flow in the pigeon Columba livia: its possible relevance to cutaneous water evaporation
1 Department of Cell and Animal Biology, Institute of Life Sciences,
Hadassah School of Dental Medicine, The Hebrew University of Jerusalem,
Jerusalem, Israel
2 Division of Physiology, Hadassah School of Dental Medicine, The Hebrew
University of Jerusalem, Jerusalem, Israel
Deceased (8 March, 2000).
* Author for correspondence at present address: Israel Naval Medical Institute, POB 8040, Haifa 31080, Israel (e-mail: yehuda-a{at}maoz.org.il)
Accepted 20 May 2002
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Summary |
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Key words: Adrenergic receptor, clonidine, heat acclimation, propranolol, thermoregulation, pigeon, Columba livia
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Introduction |
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Inhibition of ß-adrenergic receptors (ß-ARs) (e.g. by
propranolol) or stimulation of 2-adrenergic receptors
(
2-ARs) (by clonidine) causes CWE to be `switched on' in HAc
pigeons, even at normothermic Ta, to levels similar to
those measured in heat-exposed HAc birds
(Marder and Raber, 1989
;
Ophir et al., 2000
;
Ophir et al., 1995
). Moreover,
these studies showed that both selective ß2-AR and
non-selective ß-AR agonists totally blocked pharmacologically induced as
well as heat-induced CWE. The effect on heat-exposed HAc pigeons was
concomitantly accompanied by intensive panting. This suggests that CWE is an
adaptive trait that is subject to neural control, although humoral control
cannot be excluded.
Dermal/epidermal tissue and peripheral microvasculature have both been
considered as CWE effectors. (1) Dermal or epidermal tissue. Peltonen et al.
(1998) showed that the skin of
the HAc pigeon differs significantly from that of NAc and CAc birds. Marked
differences include the presence of highly vascularized areas, a thicker
epidermis (partly as a result of tissue hydration), and the unique patterns of
intracellular structures such as mammalian-like keratohyalin. Furthermore,
heat exposure of HAc pigeons induces structural modifications in the
epidermis, reflected by the distension of extracellular spaces. (2) Peripheral
microvasculature. Arieli et al.
(1999
) demonstrated that
microstructural adjustments in the capillary wall such as interendothelial
cell gaps and fenestral openings, occurring in response to heat exposure and
adrenergic manipulation at normothermic Ta, are strongly
associated with CWE. The observation of Marder and Raber
(1989
) that both heat- and
propranolol-induced CWE are accompanied by cutaneous vasodilatation suggests
that this mechanism involves vasodynamic changes. Their finding that
propranolol induces a vasoactive effect only in HAc pigeons suggests a
possible link to CWE. Apart from this correlative association, however, there
is no solid quantitative evidence for vasodynamic changes. The candidate
effectors could be complementary, producing a combined synergistic effect, and
adjustments in skin permeability to water might serve as a gating mechanism,
with vasodynamic changes modulating the driving force of this process.
The purpose of the present study was twofold: (1) to investigate whether effective CWE requires augmented cutaneous blood flow, and (2) to determine whether the specific nature of the adrenergic control of vasomotor responses provides the means for CWE.
Our data show that although CWE is normally coupled with augmentation of skin blood flow, this relationship is merely circumstantial, and CWE is probably influenced by vasomotor adjustments designed to regulate microvascular pressure.
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Materials and methods |
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Skin blood flow, CWE, skin temperature (Ts) and body temperature (Tb) were measured in birds from both groups at room temperature, upon acute heat exposure, and following pharmacological manipulations under normothermic conditions (room temperature). These parameters were not measured simultaneously, but in separate experiments, so as to prevent undue stress caused by lengthy handling of the birds and to reduce variability in the duration of exposure to the specific conditions, particularly to heat exposure in conscious pigeons. Blood flow in major cutaneous vessels was measured under anesthesia in tandem with CWE.
Acute experimental treatments
Acute heat exposure
(i) To measure the effect of progressive temperature elevation on CWE,
Ts and Tb, the birds were placed in
the environmental chamber and exposed to stepwise heating (30-60°C
Ta, in 5°C increments; RH varied from 30-10 % with the
elevation of Ta). Because NAc birds did not tolerate
Ta=60°C and were highly stressed at
Ta=55°C, the upper temperature limit for CWE
measurements was set at 50°C, and for Tb and
Ts at 55°C. Measurements were made 90 min after each
temperature increment.
(ii) To determine the effect of high Ta on skin capillary blood flow, the birds were placed in an environmental chamber and exposed to two different Ta settings (25°C, RH=50 % and 50°C, RH=30 %). Measurements were taken inside the chamber, prior to and 90 min after the onset of heat exposure.
Pharmacological treatment
To examine the involvement of adrenergic receptors in CWE and skin blood
flow, propranolol (a ß-AR antagonist; Aldrich, WI, USA), or clonidine (an
2-AR agonist; Sigma, MO, USA) was injected into the pectoral
muscle with a 25-gauge hypodermic syringe at a dose of 1.3 mg kg-1
and 80 µg kg-1, respectively. These were the minimal doses
required to produce maximum CWE, determined from their respective
doseresponse curves (data not shown). All pharmacological manipulations
were carried out under normothermic conditions. Following treatment, blood
flow was measured as described below.
Measurements
Temperature
Tb and Ts were measured using a
needle thermistor (Hypodermic probe no. 524, YSI, Yellow Springs, OH, USA)
attached to a Tele-Thermometer (46 TUC, YSI). For Ts, the
thermistor probe was lightly attached to the skin surface until a stable
reading was obtained. Preliminary measurements showed that this gentle
procedure affects neither local blood flow nor CWE in the measured area. The
mean abdominal Ts for each bird was calculated from stable
readings at two locations on the abdominal skin. For Tb,
the probe was inserted 2-3 cm deep, parallel to the vent through the lower
intestinal tissues. This procedure is preferred in birds because of their
short rectum; use of the standard procedure for measuring rectal temperatures
in mammals may cause intestinal fissure. Tb was read after
approximately 3 s. The same probe was used for measuring both
Ts and Tb to reduce any possible
errors.
Cutaneous water evaporation
CWE was measured using a porometer (AP-4, Delta-T Devices, Cambridge, UK).
This device was calibrated daily with its original calibration plate, supplied
by the producer. Stable readings were automatically taken from two locations
on the abdominal areas and the mean value was calculated. Resistance values
were converted to CWE according to Monteith
(1990), Cena and Monteith
(1975
) and Campbell
(1977
). Each value presented is
the mean of the entire group of birds used in the experiment (for more
detailed description, see Ophir et al.,
2000
).
Blood flow
Cutaneous blood flow Q was measured by laser Doppler flowmetry and
ultrasonic flowmetry. Laser Doppler flowmetry measures net tissue blood
perfusion in a selected area of 1 cm2 at a depth of 1 mm. This
method is based on the blood cell flow in the tissue (measuring blood cell
velocity and blood cell mass to extract the flow volume) and provides flow
values (ml min-1 g-1) from which the relative change in
tissue perfusion was calculated. Ultrasonic flowmetry measures fluid flow in
individual exposed vessels and provides absolute flow values (ml
min-1) in the examined vessel. By integrating the data from these
two distinct methods, we attempted to gain more insight into the events taking
place in the cutaneous microvasculature.
Tissue perfusion was measured using an ALF21D laser Doppler flowmeter equipped with a 780 nm infrared laser diode and a 0.5 mm fiber spacing prism type probe (Advance Company, Tokyo, Japan). Measurements were made prior to and 60 min after the onset of heat exposure or after drug administration, in two areas on the dorsum of conscious pigeons, sedated by darkness. Readings were taken after at least 1 min from placing the probe on the skin, allowing the probe temperature to reach that of the skin. Only stable readings (<10% variation over 1 min) were recorded. The blood perfusion values are the mean of the values measured every 10 s during a 2 min period. To minimize disturbances, only two measurements per animal were made: prior to and following each treatment. Consequently, no sequential dynamics of blood perfusion could be plotted.
Blood flow in single vessels was measured using the ultrasonic flowmetry method. Experiments were conducted on fully anesthetized pigeons (ketamine, 1 mg kg-1, i.m.), using a T-106 blood flowmeter (TSI, Ithaca, NY, USA). The pigeon to be examined was placed on a homeothermic blanket with a control unit (Harvard Apparatus Inc., Holliston, MA, USA) set at 40°C to maintain Tb in the normothermic range. The main arterial and venous vessels supplying the pectoral skin (a. cutanea abdominalis and v. cutanea abdominalis, respectively) were surgically exposed and detached from the skin. A U-shaped S1 probe was gently attached to each vessel and carefully fixed in the appropriate position, using a stereotactic apparatus. The entire space between the probe and the vessel was filled with Aquarius 101 ultrasound gel (Meditab, Israel). Blood flow signals were transmitted from the device to a BS-273 recorder (Gould Instrument Systems, OH, USA) and the blood flow from each vessel was measured. Readings were taken after at least 80 min from onset of anesthesia and lasted 42 min. At high ambient temperatures (>45°C), the readings were unstable, probably because of a temperature effect on probe sensitivity or transfer of heat from the metal probe to the blood vessel, so only pharmacological manipulations under normothermic conditions are reported. Representative recordings from individual HAc and NAc pigeons are shown in Fig. 1. To calculate arterial or venous blood flow, we divided the entire period of measurement (42 min for each experiment) into 4 min units. The mean flow (ml min-1) of each time unit was calculated from the area under the curve. CWE, Ts and Tb were measured separately in anesthetized pigeons. Collectively, despite its limitations (the need to anesthetize the animal), this method provided us with discrete values of blood flow in the afferent and efferent blood vessels of the measured skin area.
|
Statistics
The significance of the differences within and between groups was assessed
using two-way ANOVA for repeated measures. For post hoc analysis,
Dunnett's control comparison analysis was used. For pairs of mean values, we
used Student's two-tailed t-test. P<0.05 was considered
significant; P<0.005 was considered highly significant. The
results are presented as means ± S.E.M. All statistical analyses were
performed using JMP (SAS Institute Inc., Cary, NC, USA).
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Results |
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Drug effects on Tb and cutaneous water evaporation
The effects of clonidine and propranolol on Tb and CWE
are presented in Fig. 3. In
general, administration of clonidine or propranolol resulted in a significant
drop in Tb (Fig.
3A) and an increase in CWE
(Fig. 3B)
(P<0.005). Clonidine induced a significant, hypothermic effect in
the NAc birds (Tb=2.8°C, P<0.005).
The same treatment produced a greater effect in the HAc pigeons
(
Tb=4.5°C, P<0.005). The
hypothermic effect of propranolol in both the NAc and HAc pigeons was less
pronounced (
Tb=1.1°C and 2.6°C,
respectively, P<0.005). Both treatments induced a significantly
greater hypothermia in the HAc group, compared with the NAc group
(P<0.005). No significant differences were found between the drugs
in their effect on CWE in the HAc and NAc groups, but HAc pigeons showed
significantly higher CWE following administration of either drug
(P<0.005), and this effect was also observed in anesthetized birds
(Fig. 4).
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Measurement of subcutaneous microvascular blood perfusion
To elucidate whether CWE intensity depends on skin blood flow, both
parameters were measured concomitantly, using three different stimuli: heat
exposure (a=50°C),
propranolol and clonidine. The skin blood flow of the dorsum was measured
using laser Doppler flowmetry.
As shown in Fig. 5A,D, heat exposure caused an increase in both skin blood flow and CWE in the HAc and NAc pigeons. However, the elevation of skin blood flow in the HAc group was greater (2.4-fold, P<0.005) than in the NAc group (1.8-fold, P<0.005), and the two groups were significantly different (P<0.005). Concomitantly, CWE values in the HAc pigeons increased dramatically (6.2-fold, P<0.005) compared with those of the NAc birds (2.1-fold, P<0.05), and were significantly different (P<0.005).
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Propranolol administration resulted in a significant 1.3-fold increase (P<0.005) in skin blood flow in the HAc pigeons (Fig. 5B). In contrast, the skin blood flow of the NAc pigeons declined by 0.7-fold (P<0.005) following drug administration. The increase in skin blood flow in the HAc pigeons was accompanied by a marked rise in CWE (5.3-fold, P<0.005), whereas the NAc birds showed no change (P>0.05, Fig. 5E). Clonidine administration resulted in a significant decrease in skin blood flow in both the HAc and the NAc pigeons (Fig. 5C). Following clonidine administration, the skin blood flow for the HAc and NAc pigeons was 42% and 46%, respectively, of that obtained for the matched controls (P<0.005 and P<0.005), with no significant difference between the two groups. Fig. 5F shows a 2.7-fold elevation in CWE in the HAc birds (P<0.005), but no increase (P>0.05) was observed in the NAc group.
Arterial and venous blood flow
Arterial (Qa) and venous (Qv) blood
flows were measured simultaneously, using ultrasonic flowmetry. Both
propranolol and clonidine induced a significant increase in the skin
Qa of the HAc pigeons, while decreasing
Qv (Fig.
6A,C). The differences between Qa and
Qv were highly significant for both treatments in the HAc
pigeons (P<0.005), but not in the NAc birds
(P>0.05).
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The effect of propranolol on the HAc pigeons was greater and of much longer duration than that of clonidine. Qa gradually increased following the injection of propranolol, reaching stable values after 16-20 min. The stable blood flow was maintained to the end of the experiment (t=42 min). The effect of propranolol on Qv was faster, the obtained values stabilizing after 4 min and remaining constant until termination of the experiment.
The effect of clonidine on Qa in the HAc pigeons was faster than
that of propranolol: steady readings were obtained 4 min after drug injection.
Qv showed a similarly quick response. The mean difference
between the arterial and the venous blood flow
(Qa-v) prior to propranolol administration was not
significant, whereas the mean
Qa-v at
t=20-42 min was 0.4 ml min-1 (P<0.005). The
mean ratio of Qa to Qv
(Qa:v) was 0.75 prior to propranolol administration and
2.5 at t=20-42 min. No significant changes in Qa
or Qv were found in the NAc pigeons following similar
treatments (Fig. 6B,D).
Under our experimental conditions, both propranolol and clonidine individually induced a significant increase in CWE and a decrease in Ts and Tb in the HAc pigeons (Fig. 4). A weak, although significant, increase in CWE was induced by these agents in the NAc pigeons.
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Discussion |
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During acute heat exposure in the HAc pigeons, both CWE and skin blood flow
increased, whereas Ts and Tb remained
relatively stable. In the NAc pigeons, the heat-induced increase in both CWE
and skin blood flow was weaker, and Ts and
Tb were augmented. In the NAc pigeons,
TbTs dropped with the
elevation in Ta, whereas the HAc pigeons maintained a
relatively constant
TbTs. These findings
point to the strong cooling effect of CWE in the HAc pigeons.
The correlation between the dynamics of CWE and skin blood flow could imply
that these two phenomena are interdependent. However, as discussed below, the
finding that, following clonidine administration, blood flow was independent
of CWE dynamics, rules out this possibility. Both
2-adrenergic stimulation and ß-adrenergic inhibition
resulted in increased CWE, together with decreased Tb and
Ts. Moreover, these effects were stronger in the HAc
birds, further confirming the enhanced cooling capacity of CWE in the HAc
pigeon. Another conspicuous finding in our study is the different, and to some
extent antagonistic, dynamics of arterial versus venous blood flow
(
Qav) to the skin
(Fig. 6) that occurred in tight
association with the pharmacologically induced CWE in the HAc pigeons
(Fig. 4). The above findings
suggest a difference in a:v resistance ratio, leading to elevated cutaneous
capillary pressure and, in turn, an augmented driving force for water efflux
and CWE. Interplay between
2- and ß-adrenergic
signaling appears to control differences in a:v resistance.
Effect of heat exposure
The diversion of blood to the skin in homeotherms following heat exposure
is well documented and acts to maintain normal Tb by
enhancing heat dissipation via the skin
(Johnson and Proppe, 1996;
Jones and Johansen, 1972
;
Nolan et al., 1978
;
Wolfenson, 1983
). Our finding
that heat exposure increased skin blood flow supports this notion. Since water
evaporation can lower surface temperature to values below the ambient
temperature, CWE amplifies this ability when
Ta>Tb. However, during heat
challenge, HAc pigeons showed only a mild elevation in Ts,
despite having a markedly higher skin blood flow. In contrast, NAc pigeons
exhibited a considerable increase in Ts, with a smaller
rise in skin blood flow. This difference between HAc and NAc pigeons is
attributed to the former's ability to resort to CWE.
Pharmacological manipulations imply that skin blood flow is not
indispensable in inducing cutaneous water evaporation
The difference between the effects of propranolol and clonidine was evident
in the laser Doppler flowmetry measurements of net blood perfusion in the skin
(Fig. 5). In HAc pigeons,
propranolol, like heat exposure, induced an increase in skin blood flow. In
contrast, clonidine, although evoking CWE, triggered a decrease in skin blood
flow. The ability to dissociate CWE from skin blood flow implies that
processes other than increased skin blood perfusion play a role in CWE. Not
only the opposing effects of clonidine, but also the different elevation in
skin blood perfusion (2.4-fold) and CWE (6.2-fold) following heat exposure or
propranolol administration (1.3-fold and 5.3-fold for skin blood flow and CWE,
respectively) of HAc pigeons, supports the notion that skin blood flow is not
the sole direct factor involved in the induction of CWE. Apparently, it acts
in concert with other regulatory mechanisms, such as those responsible for the
adaptability of skin and capillary permeability to water. Moreover, its
association with CWE is conceivably derived from other, hemodynamic skin blood
flow-associated changes, most likely hydrostatic capillary pressure. The
effect of skin blood flow is probably instantaneous, and it may be regulated
by various adrenergic-controlled factors, such as pre- and post-capillary
resistance, measured in this investigation.
Control of capillary hydrostatic pressure
Greater arterial blood flow in the face of reduced venous drainage may
reflect an augmented difference in a:v resistance ratio leading to greater
capillary hydrostatic pressure. In turn, this may enhance water efflux from
the lumen of the capillary to the epidermal tissue where it can serve as a
water source for prolonged CWE. Our finding of concomitantly enhanced CWE
under these conditions is in agreement with this interpretation. Our results
complement previous observations of increased extravasation, manifested by the
efflux of Evans Blue-labeled albumin
(Arieli et al., 1999), and
hydrated epidermal tissue (Peltonen et
al., 1998
) following exposure of HAc pigeons to acute heat. It is
not clear how this augmented difference in a:v resistance is achieved.
However, it is evident from our data that the hemodynamic influence of both
- and ß-AR agents used in the HAc pigeons does not correspond to
the effect that would be expected from our knowledge of mammalian pharmacology
(Crandall et al., 1997
;
Koss, 1990
; van Brommelen et
al., 1986). On the contrary, both drugs induced augmented arterial blood flow.
Interestingly, this is not the only exception to the mammalian pattern.
Propranolol induces cardioacceleration in summer-acclimatized pigeons, in
contrast to its suppressive effect in mammals, and in winter-acclimatized
pigeons (Ophir et al., 2002
).
However, based on the results obtained in this investigation and our previous
studies (Ophir et al., 1995
;
Ophir et al., 2000
), we
hypothesize that differences in
/ß-adrenergic receptor density and
affinity are involved, as illustrated in
Fig. 7. The role of other
vasoactive signaling pathways cannot be excluded, although this was beyond the
scope of the present investigation. Light and electron microscopic findings
from our laboratory (Y. Arieli, unpublished results) revealed the existence of
flattened venules (comprising approx. 5% of the total microvessels in the
skin), detected exclusively in the skin of HAc heat-exposed pigeons. This
observation may imply that a glomerulus-like mechanism, such as post-capillary
constriction, occurring during the CWE period, contributes to the greater
difference in a:v resistance ratio.
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Intra/extravascular fluid passage in the skin
When calculating the amount of water evaporating from the abdominal skin
(up to 0.5 µl cm-2 min-1), we found it much lower
than the mean value of Qav, normalized to
the supplied skin area (approximately 10 µl cm-2
min-1). A mechanism based on intensive extravasation,
counterbalanced by drainage via the lymphatics, could account for
this apparent discrepancy.
Indeed, a considerable extravasation takes place in the skin
microvasculature of the HAc pigeon. Arieli et al.
(1999) found that intensive
cutaneous extravasation of Evans Blue-labeled albumin occurs following heat
exposure or propranolol administration in the HAc pigeon, thus providing a
driving force for water efflux. Therefore, the resultant outflow should be
partly negated by intensive lymphatic drainage, rather than by post-capillary
reabsorption (Fig. 8). As shown
previously (Arad et al., 1989
),
the protein content of avian plasma, especially the albumin concentration, is
substantially lower than that measured in mammals. This results in low basal
colloid-osmotic pressure in the capillary, thus reducing its ability to retain
water. This situation would require an alternative pathway to restore large
volumes of water outflow in certain tissues, namely the lymphatic system.
Although we have no direct evidence for a highly developed lymphatic vessel
network in pigeon skin, there is evidence for such functional, rich lymphatic
networks in other tissues in the pigeon and in other birds
(Berens von Rautenfeld and Budras,
1981
; DeStefano and Mugnaini,
1997
). However, it was argued that the fluid balance in the skin
relies on lymph flow (Levick,
1995
). This scenario predicts the development of a difference in
a:v hematocrit. The exceptionally low whole body:venous hematocrit ratio
(0.71) documented in the pigeon
(Kalomenopoulou and Koliakos,
1989
) supports this hypothesis. A possible consequence of the
findings of Arieli et al.
(1999
) would be a drop in the
colloid-osmotic pressure in the venous side of the capillary, concomitant with
a rise in the perivascular interstitial colloid-osmotic pressure. In
conclusion, low basal values of capillary colloid-osmotic pressure in birds
might reduce the inward driving force, particularly during CWE. Alternatively,
enhanced lymphatic return could remove excess water from the tissue. Augmented
protein extravasation during CWE would further reinforce this route of fluid
return to the circulatory system.
|
Conclusions
Taken together, our present findings provide a conceptual basis for the
existence of a powerful driving force in the evaporative cooling mechanism of
the HAc pigeon. We envisage the CWE process as orchestrated complementary
changes, both in the cutaneous microvasculature and in the dermal/epidermal
tissue architecture, possibly controlled by adrenergic signaling. Greater skin
capillary hydrostatic pressure and increased plasma protein extravasation
provide the driving force for water efflux to the epidermis. Concomitantly, in
the skin, swelling of the cells in the hydrated epidermis, together with
intra- and extracellular ultrastructural adjustments, result in greater water
permeability, thus allowing water movement towards the skin surface
(Arieli et al., 2002;
Peltonen et al., 1998
). In
other words, structural and ultrastructural changes in the skin and
endothelial openings serve as the gating component of the process, while
hemodynamic events provide the driving force. These events are conceivably
accompanied by a reduction in water reabsorption by postcapillaries and
venules due to colloid leakage into the interstitial space. In turn, the
lymphatic vascular network may be responsible for drainage of the excess water
into the circulation.
Perspectives
The results of the present study, together with accumulating knowledge on
ultrastructural and physiological changes in the skin and its microvasculature
in heat-acclimated pigeons, allow a better and more integrated insight into
one of the most highly efficient cooling mechanisms known. Yet, this
investigation raises fundamental questions, such as the uniqueness or
generality of this mechanism and its various components. Comparative studies
on CWE in other avian species may illuminate the pattern of its phylogenetic
distribution, evolutionary origin and significance.
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Acknowledgments |
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