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Vol. 84, Issue 3, 980-986, March 1998
1 Departments of Anesthesiology
and Physiology and Biophysics, University of Texas Medical Branch and
Shriners Burns Institute, Galveston, Texas 77555-0833;
2 Department of Plastic and
Reconstructive Surgery, We determined the effect of reduced bronchial
blood flow on lung fluid flux through changes in lung lymph flow, lung
wet weight-to-dry weight (wet/dry) ratios, and pulmonary microvascular
reflection coefficient (
lung lymphatic; reflection coefficient; pulmonary edema; bronchial
artery; acute lung injury; burns; pulmonary
THE INHALATION OF SMOKE is an increasingly common
finding in the victims of thermal accidents. The pulmonary injury
associated with it is responsible for a considerable amount of the
mortality and morbidity that occurs in these patients (12, 28). We have previously reported that, after smoke inhalation, lung lymph flow, extravascular lung water, and pulmonary vascular permeability increased, as indicated by a fall in the reflection coefficient ( Because the sheep has a common bronchial branch arising from the
bronchoesophageal artery, which supplies the lung, investigators have
conducted a number of experimental studies of the bronchial circulation
in this animal. Recent investigations, however, have shown that there
are multiple systemic arteries to the lung in sheep, as in other
species (8, 9, 19, 20). Baile et al. (4) have reported that mechanical
obstruction of the bronchial artery may lead to opening of the
collateral circulation, although the source of the collateral blood
flow was not clearly defined. Consequently, they concluded that
sclerosing the airway microvasculature with ethanol is a more effective
procedure for abolishing the bronchial circulation (4). The purpose of
the present study was to test whether ablation of the bronchial
circulation could attenuate the increased pulmonary transvascular fluid
flux after smoke inhalation.
Animal care and use.
Animals were cared for in the Ovine Intensive Care Unit at our
institution, which is approved by the American Association of
Laboratory Animal Care. The experimental procedures were approved by
the Animal Care and Use Committee of The University of Texas Medical
Branch. The National Institutes of Health and American Physiological
Society guidelines for animal care were strictly followed. Animals were
studied in the awake state with free access to food and water.
Surgical preparation.
Twenty-one female range-bred adult Merino sheep (25-40 kg) were
surgically prepared for study. All animals were endotracheally intubated and ventilated during the surgery under halothane anesthesia. Arterial and venous catheters (16 gauge, 24 in., Intracath, Becton Dickinson, Sandy, UT) were placed in the descending aorta and inferior
vena cava via the femoral artery and vein, respectively. A Swan-Ganz
thermal dilution catheter (model 93A-131-7F, Edwards Critical-Care
Division, Irvine, CA) was positioned in the right pulmonary artery via
the right external jugular vein. The chest was opened at the fifth
intercostal space in both sides, and an efferent lymphatic from the
caudal mediastinal lymph node (CMN) was cannulated (Silastic
medical-grade tubing, 0.025 in. ID, 0.047 in. OD, Dow Corning, Midland,
MI) by a modification of the technique of Staub et al. (26). The
systemic contribution was removed by ligating the tail of the CMN and
cauterization of the systemic diaphragmatic lymph vessels. Vascular
occluders (In Vivo Metric System, Healdsburg, CA) were placed around
each of the pulmonary veins as they entered the left atrium, as
described by Isago et al. (16). A Silastic catheter was also positioned
in the left atrium during the procedure to measure left atrial pressure
directly. The sheep were given 5-7 days to recover from the
surgical procedure with free access to food and water.
Ablation of bronchial circulation.
After a 5- to 7-day recovery period, the animals were endotracheally
intubated and ventilated during the surgery, which was performed under
halothane anesthesia. In this operation, the animals were equally and
randomly assigned to one of three groups. In the ablation group
(n = 7), the left thorax was reopened
through the fifth intercostal space, and the lungs were retracted,
exposing the dorsal anatomy. During this procedure, a pleural
adhesiotomy was performed. Then the bronchoesophageal artery was
exposed, and 4 ml of 70% ethanol were injected into this artery
through a lacrimal cannula (27 gauge, 30 mm,
Nakamurasi-Ruikansenjyosin-Kairyougata, Handaya, Tokyo, Japan), after
the ligation of the esophageal branch with 5-0 silk suture. In the
ligation group (n = 7), the
bronchoesophageal artery was isolated and tied off using 5-0 silk
suture without ethanol injection. In the sham group
(n = 7), the bronchoesophageal artery
was exposed but left intact.
ABSTRACT
Top
Abstract
Introduction
Methods
Results
Discussion
References
). In the first of two surgical procedures,
Merino ewes (n = 21) were surgically
prepared for chronic study. Five to seven days later, in a second
operation, the bronchial artery of the injection group
(n = 7) was ligated, and 4 ml of 70%
ethanol were injected into the bronchial artery to cause sclerosis of the airway circulation. In the ligation group
(n = 7), only the bronchial artery was
ligated. In the sham group (n = 7),
the bronchial artery was surgically exposed but left intact without
ligation or ethanol injection. One day after these operations the
animals received a tracheotomy and 48 breaths of cotton smoke. The
value of was determined at two points: 24 h before the second
surgical procedure and 24 h after smoke inhalation. Lung lymph flow,
blood-gas parameters, and hemodynamic data were measured every 4 h
after injury. At the end of investigation, samples of lung were taken for determination of blood-free wet/dry ratio. In the sham group, inhalation injury induced a gradual increase in pulmonary vascular resistance and lung lymph flow, which was associated with deterioration of oxygenation. Reduction of the bronchial blood flow attenuated these
pathophysiological changes, and the degree of this attenuation was
greater in the injection group than in the ligation group. The value of
was significantly higher after smoke inhalation in the injection
group compared with the sham group (0.77 ± 0.04 vs. 0.61 ± 0.03, means ± SE) at 24 h. The mean wet/dry ratio value of the
injection group animals was 30% less than that of the sham group. Our
data show that the bronchial circulation contributes to edema formation
in the lung occurring after acute lung injury with smoke inhalation.
INTRODUCTION
Top
Abstract
Introduction
Methods
Results
Discussion
References
)
and rise in the filtration coefficient in a chronically instrumented ovine model (13, 15, 17, 29). These physiological alterations in
pulmonary microvasculature are delayed in onset, and the peak of
increased microvascular permeability was observed around 24 h after
injury (16). In contrast, there is a marked increase in bronchial blood
flow immediately after inhalation injury (1, 27). Because the increased
bronchial blood flow enters into the pulmonary vasculature through
various bronchopulmonary anastomoses (25), it has been suggested that
the bronchial circulation plays a significant role in the spread of
injury from the airway of the lung to the parenchyma (2, 11).
Mechanical occlusion of the bronchial artery reduced lung edema
formation after smoke inhalation in an anesthetized canine model (11)
and in a conscious sheep model (2). However, this method could not
totally abolish the pathophysiological changes that occurred in the
pulmonary vasculature after smoke inhalation.
METHODS
Top
Abstract
Introduction
Methods
Results
Discussion
References
Cotton smoke inhalation injury Before the injury, all of the animals received a tracheotomy and cuffed tracheotomy tube (10 mm diameter, Shiley, Irvine, CA), which was inserted under ketamine anesthesia (Ketalar, Parke-Davis, Morris Plains, NJ). Then anesthesia was continued with halothane, and inhalation injury was induced with a modified bee smoker (17). The modified bee smoker was filled with 50 g of burning toweling and was connected to the tracheotomy tube via a modified endotracheal tube. The connection contained a thermistor to monitor the temperature of the smoke. During the insufflation procedure, the temperature of the smoke did not exceed 40°C. The sheep were insufflated with 48 breaths (650 ml/breath) of smoke. After this procedure the animals were awakened and studied for 24 h.
Measurement of hemodynamic variables. Cardiac output was measured with a cardiac output computer (model 9520, American Edwards Laboratories, Irvine, CA) by using the thermodilution method with 5% dextrose as the indicator solution. Vascular pressures were measured using fluid pressure transducers (P23ID, Statham Gould, Oxnard, CA) adapted to a continuous flushing device and connected to a physiological recorder (model OM9 patient monitor, Electronics for Medicine, Honeywell, Pleasantville, NY). Zero calibrations were taken at the level of the olecranon joint on the front leg, which is considered to be the level of the right atrium. Hemodynamic and lymph variables were measured every 4 h after injury during the 24-h experimental period. Vascular resistances were calculated using standard formulas. Arterial and mixed-venous blood gases were measured by using a blood gas analyzer (model 1302 IL, Instrumentation Laboratory, Lexington, MA).
Lymph and plasma measurements.
Lung lymph flow (
L) was
measured with a graduated test tube and stopwatch. Lymph and blood
samples were collected in EDTA tubes, and total protein concentration
in plasma (CP) and lymph (CL) was then measured with a
refractometer (National Instrument, Baltimore, MD). Lung lymph protein
clearance (LPC) was calculated by the equation: LPC = L × CL/CP.
Permeability analysis.
Determination of sigma in sheep by pulmonary venous occlusion has
previously been described by Isago et al. (16). Five pulmonary veins
empty into the left atrium of sheep; three major pulmonary veins are
normally associated with the right lung and two with the left lung.
Anatomically, these veins enter the left atrium separately, not as a
common trunk, making it is necessary to occlude each vein separately.
We increased pulmonary arterial pressure (PAP) by ~15-20 mmHg by
inflating the pulmonary venous occluders with normal saline. In our
experience, this volume was ~50% of the capacity of each occluder.
If L
stabilized at this level, the occluders were further inflated in an
attempt to obtain a filtration-independent state for
CL.
L and
CL were measured every 30 min
until CL reached a minimal value
at the highest PAP that the animals would tolerate. The pressure was
kept stable for 120 min. The lymph protein levels became stable within
90 min after the pressures were raised, and the data were collected for
analysis when the protein levels in the lymph had been stable at their
lowest level. The reflection coefficient, , was estimated from the
minimal CL by using the formula:
= 1 
CL/CP.
Experimental protocol.
The sheep were connected to pressure transducers and monitors for
continuous monitoring of left atrial, central venous, right pulmonary
arterial, and aortic pressures. The baseline data were determined 24 h
after the second operation. Only the baseline data of were
determined 24 h before the second operation, since this measurement
affects most hemodynamic and lung lymph data, as previously reported
(16). After all baseline measurements were completed, all animals
received 48 breaths of cotton smoke, as described above. Immediately
after insufflation, anesthesia was discontinued and the animals were
allowed to awaken but were ventilated mechanically with a Servo
Ventilator 900C (Siemens-Elena, Solna, Sweden) throughout the next 24-h
experimental period. Ventilation was performed with a positive
end-expiratory pressure of 5 cmH2O and a tidal volume of 15 ml/kg. The inspiratory
O2 concentration was adjusted to
maintain the arterial O2
saturation above 90%. The respiratory rate was set to maintain
normocapnia. Fluid resuscitation during the experiment was performed
with Ringer lactate solution (3 ml · kg
1 · h1).
Analysis of data. All values are reported as means ± SE. Differences from baseline within the three groups were assessed post hoc by Dunnett's test. Analysis of differences between groups was assessed by Scheffé's test. Statistical significance was accepted at P < 0.05.
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RESULTS |
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Top
Abstract
Introduction
Methods
Results
Discussion
References
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The arterial carboxyhemoglobin levels just after smoke exposure were 74.0 ± 5.0% in the sham group, 80.6 ± 4.2% in the ligation group, and 76.2 ± 4.9% in the injection group. These values were not statistically different from one another, reflecting the consistency of the injury in each group.
The changes in blood flow to intraparenchymal bronchi (2-4 mm) before and after the second operation are shown in Fig. 1. In the sham group, blood flow was not significantly changed. The reduction of airway blood flow in the ligation and injection groups was 32.1 ± 12.0 and 86.3 ± 7.2%, respectively. The intrapulmonary airway blood flow in the injection group was significantly less than those in both the sham and ligation groups.
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The changes in cardiopulmonary hemodynamics are shown in Table 1. Mean arterial pressure and filling pressures were maintained at baseline level, although there was a statistically insignificant trend for cardiac index to fall in all groups. The sham group showed a significant increase in PAP at 24 h after smoke inhalation, whereas in the ligation and injection groups the increase in PAP was mild and was not statistically different from the baseline value. There were no significant differences between groups at any time.
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The calculated vascular resistances are presented in Fig. 2. The sham group showed a significant increase in pulmonary vascular resistance (PVR) index after smoke inhalation, whereas systemic vascular resistance (SVR) index was unchanged during the experimental period. The PVR index did not change significantly in the ligation or injection groups. Notably, the PVR index in the injection group was significantly less than in the sham group at 24 h after smoke insufflation.
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Figure 3 depicts oxygenation after smoke inhalation injury. Mechanical ventilation with adjusted fractional concentration of inspired O2 (FIO2) allowed each group to maintain arterial PO2 (PaO2) above baseline levels. Progressively deteriorated oxygenation was observed in the sham group, represented by the decreased PaO2/FIO2 ratio. This deterioration was significantly attenuated in the injection group during the 24-h period. In the ligation group, the fall of PaO2/FIO2 ratio was delayed, but 24 h after smoke inhalation, this value had significantly dropped from the baseline value.
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L increased to
nearly four times the baseline value by 24 h after insult in the sham
group (Fig. 4). This increase was
significantly reduced in the ligation and injection groups. The
increase in L in
the sham group was associated with a significant increase in the LPC
(Fig. 5). In the ligation group, this
increase was less but not significantly different from the increase
seen in the sham group. In the injection group, however, this increase was further reduced, and the protein clearance at 24 h was
significantly lower than in the sham group.
|
|
The reflection coefficient, , decreased significantly in the sham
group (Fig. 6). In the injection group, the
fall in was small and was not statistically different from the
baseline value. The value of of the injection group was
statistically higher than that of the sham group 24 h after smoke
insufflation. The ligation group showed an intermediate decline in .
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Figure 7 shows blood-free wet/dry ratios of both right and left lungs. The control represents normal value in our laboratory from six healthy animals without any injury. The sham group showed significant increases when these values were compared with corresponding lungs from control animals. In the ligation and injection groups, these increases were less remarkable and statistically insignificant from the control values. The left lung wet/dry ratios in both the ligation and injection groups showed significant differences vs. the corresponding value of the sham group.
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DISCUSSION |
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Top
Abstract
Introduction
Methods
Results
Discussion
References
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The findings of the present study confirm our hypothesis that ablation of the bronchial circulation dramatically attenuates the pathophysiological changes that occur after smoke inhalation. In our previous report (2), we suggested that the bronchial circulation might contribute to the pathogenesis after smoke inhalation, but this suggestion remained unsubstantiated, since the mechanical occlusion of the bronchial artery affected only a few parameters and the magnitude of the attenuation was limited.
The anatomy of the bronchial circulation of the ovine lung has been carefully documented (8, 9, 19, 20). Charan et al. (8) showed that sheep have multiple sources of systemic arterial blood flow to the lung and that these arteries anastomose with each other as well as with the pulmonary circulation. Ashley et al. (3) investigated the effect of transient occlusion of the bronchoesphageal artery and demonstrated 70-90% reduction of the intrapulmonary airway blood flow at 5 min after the occlusion. In the present study, the reduction of the systemic blood flow into the same-size airway at 24 h after ligation of the bronchoesophageal artery was merely 32%. This finding suggested that collateral circulation to the intrapulmonary airway could be easily established within a day.
Baile et al. (4) used radioactive microspheres and reported that ethanol injection into the bronchoesophageal artery reduced systemic arterial blood flow into the sheep lung by ~75%, whereas ligation of the bronchial artery resulted in a ~50% reduction. These values cannot be purely interpreted as a reduction of the intrapulmonary airway blood flow, since the systemic arterial blood supply to the lung is delivered not only to the airway but also to the adventitia of large vessels and structures of the lungs (10). However, ethanol injection is certainly a more reliable method than mechanical occlusion of the bronchoesophageal artery, and in the present study regional blood flow into the intrapulmonary airway substantiated the ablated bronchial circulation in the injection group.
Besides these anatomic considerations about airway blood flow, the
findings in the ligation group strongly suggested that the collateral
airway blood flow might be responsible for the incomplete block of the
pathophysiological changes after smoke inhalation. In the ligation
group, L and LPC
were significantly increased 24 h after injury, and oxygenation was
notably decreased. With a more complete elimination of the bronchial
circulation, the injection group showed a greater ability to attenuate
the pathophysiological effects associated with smoke inhalation injury. There were no significant changes in
L, LPC,
oxygenation, or PVR during the whole experimental period. In addition,
at 24 h after injury was not significantly different from the
baseline value. In contrast, all these variables showed statistical
differences when compared with the sham group at 24 h after injury.
The mechanism by which the bronchial circulation contributes to the
pathogenesis in lung parenchyma has not been clearly defined. The
bronchial circulation itself might be a source of the lung edema. Hales
et al. (11) used an acute canine model with intravenous injection of
dye and histologically demonstrated increased permeability in the
bronchial vascular bed after synthetic smoke insufflation. Because our
methods of analyzing lung fluid flux do not allow us to detect the
proportional contribution of the bronchial circulation, increased
L, LPC, and might originate from the bronchial vasculature. However, it is
noteworthy that no parameters measured after the second operative
procedure showed significant differences between groups. These findings
suggested that the contribution of bronchial circulation to
L or other
parameters is not so significant, at least before smoke inhalation.
We have previously demonstrated a three- to fivefold increase in
bronchial arterial blood flow after smoke inhalation (1, 27); however,
this flow was still <2% of cardiac output. Considering that total
blood flow perfusing pulmonary vasculature is equal to cardiac output,
the contribution of the bronchial circulation to the total vascular bed
in the lung (pulmonary and bronchial circulations) is very small.
Because increased
L is a
manifestation of fluid that traversed the total vascular bed in the
lung, it is hardly expected that a major part of the increased lymph
flow originated from bronchial vascular bed.
In our conscious animal model, the pulmonary permeability changes after smoke inhalation are considerably delayed (2, 15, 17), and the peak of increased pulmonary microvascular permeability is observed around 24 h after injury (16). In contrast, increased permeability in bronchial vessels occurs more rapidly, as demonstrated by Hales et al. (11). Barrow et al. (6) also demonstrated a more rapid permeability change in the extrapulmonary airways than that in the lungs. The time course differences between the pulmonary and the bronchial circulation, and the anatomic observation that most of intrapulmonary airway blood flow drained into the pulmonary circulation (5, 9), led us to consider that increased bronchial blood flow played a significant role in the spread of injury from the airway to the pulmonary vasculature.
In the sham group, there was a gradual increase in PVR associated with
a significant rise in pulmonary vascular pressure and a mild drop in
cardiac output. We have previously reported that pulmonary venous
resistance increased proportionally more than pulmonary arterial
resistance after smoke inhalation (14). In the present study, increased
PVR was significantly attenuated by ablation of the bronchial
circulation. There are several putative mediators responsible for the
increased PVR associated with smoke inhalation injury. Quinn et al.
(24) reported that leukotriene D4
is found in lung lymph and pulmonary edema fluid after synthetic smoke
exposure in sheep and that pretreatment with a leukotriene-receptor antagonist attenuated the PVR increase and decrease in cardiac output.
Furthermore, Noonan et al. (21, 22) showed that leukotriene D4 infusion in sheep caused
increases in PAP and PVR, primarily by inducing thromboxane formation.
Additionally, we reported that PAP, PVR, and
L were
significantly attenuated in chronically prepared sheep that had been
made leukopenic with intra-arterial infusions of nitrogen mustard (7).
These findings suggest that leukotriene, thromboxane, and some
mediators released from leukocytes might be associated with the
increase in PVR after smoke inhalation. The most interesting point,
however, is that these vascular changes occur specifically in the
pulmonary and not in the systemic vasculature, since SVR is essentially
unchanged after smoke inhalation.
The present study showed that the bronchial circulation plays a significant role in lung edema formation after smoke inhalation. On the other hand, there is increasing evidence that the bronchial vasculature is also involved in edema clearance. Recently, Fukue et al. (10), using in situ perfused sheep lung, reported that up to 14% of hydrostatic edema might be reabsorbed by the bronchial circulation. Even though our present data do not support the role of bronchial circulation in the clearance of edema, under certain conditions the bronchial circulation can take on the edema-absorbing function. Furthermore, this circulation might be important for regeneration of airway mucosa during the proliferative or reparative phase after smoke inhalation (18). Further investigations are required to elucidate the longitudinal effect of ablated bronchial circulation.
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ACKNOWLEDGEMENTS |
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This work was supported by National Institute of General Medical Sciences Grant GM-33324 and Shriners of North America Grants 8450 and 8570. D. L. Traber is the Charles Robert Allen Professor of Anesthesiology.
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FOOTNOTES |
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Address for reprint requests: D. L. Traber, Investigational Intensive Care Unit, University of Texas Medical Branch, 610 Texas Ave., Galveston, TX 77555-0833.
Received 4 December 1996; accepted in final form 22 October 1997.
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Top
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Introduction
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References
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Significant difference (P < 0.05) vs. sham group. # Significant difference difference
(P < 0.05) vs. ligation group.
