Download Systemic to Pulmonary Bronchial Blood Flow in Heart Failure*

Systemic to Pulmonary Bronchial Blood
Flow in Heart Failure*
Pier Giuseppe Agostoni, MD, FCCP; Elisabetta Doria, MD;
Franco Bortone, MD; Carlo Antona, MD; and
Paolo Moruzzi, MD
Study objective: The aim of this study was to measure
systemic to pulmonary blood flow from bronchial circulation (Qbr[s-p]) in patients with heart failure.
Design: In the absence of pulmonary and coronary
flows, Qbr(s-p) is the volume of blood accumulating in
the left side of the heart; Qbr(s-p) was measured during
total cardiopulmonary bypass for coronary artery surgery; bronchial blood was vented through a cannula introduced into the left side of the heart and its volume
was measured.
Patients: Patients were subdivided according to the
presence for more than 6 months (group 1, n=6) or less
than 2 months (group 2, n=7), or the absence of heart
failure (group 2, n=15).
Measurements and results: Qbr(s-p) was 89 ± 18* mL/
min, 27 ± 3, 22±2, in groups 1, 2, and 3, respectively
(*=p<O.Ol group 1 vs groups 2 and 3). During total cardiopulmonary bypass, pulmonary venous pressure approximates atmospheric pressure and no differences
between groups were observed in systemic artery pres-
sure, extracorporeal circulation pump flow, and airway
pressure. Therefore, vascular resistance through the
bronchial vessels draining into the pulmonary circulation is reduced in patients with heart failure for more
than 6 months (group 1).
Conclusions: During total cardiopulmonary bypass,
Qbr(s-p) is increased in patients with chronic heart failure. Since with elevated pulmonary vascular pressure
blood flow through Qbr(s-p) vessels is from the pulmonary to the systemic circulation, the lower resistance
observed in group 1 suggests that bronchial vessels
might contribute to reduced lung fluid overload in
patients with chronic heart failure.
(Chest 1995; 107:1247-52)
n heart failure, fluid content of the lung is increased; its removal is achieved through several
ways, including lung lymphatics, pulmonary circulation, bronchial circulation, airways, pleural spaces,
and mediastinal spaces.1 2 The fractional contribution of each of these pathways is not defined and we
do not know whether the removal of lung fluid excess
is affected by the time course of heart failure. A likely
role of lymph vessels has been stressed repeatedly.
However, albeit a manyfold increase of lung lymph
flow after acute and chronic pulmonary vascular
pressure elevation has been reported,36 lung lymph
flow remains in the order of a few milliliters per
hour.4-7 Therefore, lymph flow does not seem capable of maintaining lung water homeostasis in chronic
heart failure and reverting to normal lung water
content after acute heart failure. A role of bronchial
circulation seems more likely. Indeed, the bronchial
arteries drain into a vascular plexus located around
the airways where most extravascular lung fluid accumulates. These vessels have two drainage pathways: 1) the bronchial veins which, through the azygos and the hemiazygos, drain into the superior vena
cava, and 2) the anastomoses with the small pulmonary vessels.8'9 Hence, the intrapulmonary bronchial
vasculature allows communication between pulmonary and systemic circulations.8-10 Bronchial circulation might participate in the reduction of excessive
lung water in heart failure because pulmonary
hypertension reverses blood flow through the bronchopulmonary anastomoses.11'12 Although several reports suggest an increase of bronchial blood flow in
the presence of chronic lung infections, pulmonary
vascular obstruction, and mitral stenosis,10'13-16 to our
knowledge, no information is available for heart
failure. This study was undertaken to evaluate
whether, in humans, systemic to pulmonary bronchial blood flow is modified in acute and chronic
heart failure.
*From the Istituto di Cardiologia dell' Universita degli Studi di
Milano, Centro Cardiologico-Fondazione "Monzino" IRCCS,
Centro di Studi per le Ricerche Cardiovascolari del Consiglio
Nazionale delle Ricerche, Milan, Italy.
Manuscript received June 22, 1994; revision accepted November
16.
Reprint requests: C. N. R. Centro di Studio per Ricerche
Cardiovascolari, clo Cattedra di Cardiologia dell' Universita di
Milano, Via C. Parea, 4-20138 Milano, Italy
Qbr(s-p)-systemic to pulmonary blood flow from bronchial
circulation.
Key words: edema; extracorporeal circulation; lung water;
lymph flow
MATERIAL AND METHODS
We studied 28 patients who had undergone total cardiopulmonary bypass for coronary artery surgery. Patients with previous cardiac surgery, lung diseases, history of asthma, primitive
valvular heart diseases, pulmonary hypertension, and congenital
cardiac malformations were excluded from the study. PreoperaCHEST / 107/5/ MAY, 1995
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1247
tively, patients were subdivided into three groups according to the
presence and duration of heart failure. To do so, inclusion criteria for each group were observed. Patients not fulfilling all the
group inclusion criteria were excluded. The main inclusion
criteria were the following: Group 1 consisted of patients with
heart failure due to coronary artery disease for at least 6 months
as suggested by long-term history of heart failure (at least 1 episode of acute pulmonary edema more than 6 months before
cardiac surgery), reduced left ventricle ejection fraction (<40%),
and increased pulmonary wedge pressure (>12 mm Hg) at preoperative echocardiogram and catheterization, respectively.
Group 2 consisted of patients with heart failure due to coronary
artery disease for less than 2 months. A first episode of myocardial infarction in the 2 months preceding cardiac surgery and
evidence of heart failure since were among the inclusion criteria.
Heart failure before the acute episode of myocardial infarction
had to be excluded. Just as for group 1, left ventricle ejection
fraction and pulmonary wedge pressure had to be, preoperatively,
less than 40% and more than 12 mm Hg, respectively. Group 3
included patients with coronary artery disease but no evidence of
heart failure, as suggested by the patient's history, absence of
myocardial infarction, and normal left ventricle ejection fraction
(>60%) and pulmonary wedge pressure (<12 mm Hg) at preoperative evaluation. Study enrolling time was between January
1992 and May 1993. All patients fullfilling the group 1 and 2 criteria who underwent coronary artery surgery at the Department
of Cardiology of the University of Milan participated in the study.
All subjects provided written informed consent to both the surgical and experimental procedures. The study had been approved
by the local ethics committee; the investigation conforms with the
principles outlined in the declaration of Helsinki.
Total cardiopulmonary bypass was achieved using a standard
technique. A two-stage venous cannula (William Harvey extracorporeal cannula, 34-46 F Bard) was connected, in series, to an
02-heat exchanger (Monolyth, Sorin Saluggia, Italy), to a cardiopulmonary bypass pump (Stockert-Smiley, Munich, Germany), and finally to an aortic cannula (21 to 24F). The pulmonary
artery and the aorta were clamped so that no blood could leave
the pulmonary circulation through the pulmonary valve or leak
into the left side of the heart from the aorta. To drain the blood
arriving into the left side of the heart, a cannula was inserted in
the right superior pulmonary vein, advanced into the left side of
the heart, and positioned into what the surgeon felt was the lowest portion of the left heart. This cannula was connected to a roller
pump and then to a calibrated cylinder from which blood reached
the extracorporeal circuit reservoir by gravity. The position of the
left heart cannula was adjusted when needed; the aspiration from
the roller pump was the lowest possible to keep the left side of the
heart empty of blood. To avoid sucking of the cannula against the
left ventricle wall and to obtain an adequate venting, a three-way
stopcock with one end open to atmosphere was inserted between
the left heart cannula and the roller pump. During total
cardiopulmonary bypass, lungs were kept inflated by a constant
flow of air (2 to 8 L/min, fully humidified, 24°C); airway pressure was kept unchanged throughout the procedure and was
regulated by a positive end-expiratory pressure (PEEP) valve. We
monitored airway and systemic blood pressures, extracorporeal
circulation pump flow (cardiac output), and esophageal, rectal,
and blood temperatures.
The Qbr(s-p) was measured as the volume of blood returning
to the left side of the heart.'15"7 '9 This blood was collected in the
calibrated cylinder and measured continuously during the extracorporeal circulation. We discarded data obtained in the first 10
min of the procedure, during patients' rewarming (+2°C of
esophageal, rectal, or blood temperature from the lowest
achieved), and in the 10 min following cardioplegia if repeated.
With this exception, Qbr(s-p) is the average of the entire run per
patient. During Qbr(s-p) measurements, pulmonary artery and
venous pressures were approximately 0 mm Hg. Assuming that
the relationship between pulmonary venous pressure and Qbr(s-p)
is linear'2,20 and that the pressure at which flow in the intrapulmonary bronchial vessels starts to be from the pulmonary to the
systemic circulation=20 mm Hg,20 the relationship between
pulmonary wedge pressure/Qbr(s-p) was drawn and Qbr(s-p) at
real pulmonary vascular pressure was estimated.
Statistical Analysis
Data are reported as mean ± standard error of mean (SEM).
Differences were analyzed by Student's unpaired t test applying
the Bonferroni correction for multiple comparisons.
RESULTS
Patient characteristics are reported in Table 1.
Preoperative treatment included the following: (1)
group 1-digitalis, 6/6 patients; angiotensin-converting enzyme inhibitors, 5/6; nitrates, 5/6; diuretics,
Table 1-Patient Characteristics*
Patient/Age, yr/
Sex
Smoke
CI,
Ppaw,
LVEF, Ppa,
%
mm Hg mm Hg
L/min/m2
43
21
64
23
26
22
2.3
2.2
2.4
2.4
2.0
3.1
Group 1
1/55/M
2/68/M
3/61/F
4/56/M
5/71/M
6/72/M
+
+
+
+
+
+
+
+
+
21
15
28
43
37
43
22
16
13
22
17
35
30
20
34+61 30±111 22+81
1/50/M
2/55/M
+
+
3/70/M
4/68/F
5/56/M
6/62/M
7/68/M
8/71/F
-
10/44/M
11/49/M
12/62/M
13/60/M
14/68/M
15/71/M
Mean+SE 60+9
30
42
38
34
39
30
27
+
-
Mean±SE 61±6
Group 3
9/50/M
29
15
49
17
15
20
33+71 33±174 24+131 2.4+0.4f
Mean+SE 64±7
Group 2
1/62/M
2/65/F
3/53/M
4/61/M
5/69/F
6/65/M
7/53/M
30
39
20
32
39
35
+
2.2
2.2
2.4
2.9
2.7
2.3
2.6
2.5±0.3f
10
8
16
18
16
10
9
12
14
16
14
12
12
16
12
7
4
3
10
7
2
6
6
4
10
7
6
2
8
1
3.3
3.6
3.0
2.8
3.8
3.7
4.2
3.0
4.1
3.0
4.1
4.0
3.3
2.9
3.1
63+5 13+3
6+3
3.5+0.5
60
55
70
66
68
56
59
72
60
66
58
56
62
64
68
+
+
+
+
+
+
+
+
+
*LVEF=left
ventricular ejection fraction; Ppa=mean pulmonary
artery pressure; Ppaw=pulmonary artery wedge pressure; Cl=
cardiac index; +=smoker; -=nonsmoker; + =ex-smoker; SE=
standard error. Echocardiographic and hemodynamic data were
obtained preoperatively.
fp<0.01 vs group 3.
Jp<0.03 vs group 3.
1248
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Clinical Investigations
To further strengthen this point, Qbr(s-p) was not
measured in patients with an intermediate duration
of heart failure. Patient grouping was made a priori.
A significant increase of intrapulmonary bronchial
blood flow has been reported previously in several
chronic diseases that affect the lungs.8"13-'6 In models of acute pulmonary embolism, bronchial blood
flow is reduced21-23 but it is increased in lungs of animals with previous pulmonary embolism.'4 Beside
the duration of heart failure, the severity of the pulmonary hemodynamic impairment might contribute
to Qbr(s-p) changes. Patients in groups 1 and 2 had
comparable hemodynamics at preoperative evaluation. However, this is a single measurement obtained
at rest, and is possibly not representative of real pulmonary hemodynamic behavior. Therefore, although
several mechanisms might be postulated,'4 the influence of time course and severity of heart failure on
intrapulmonary bronchial circulation remains unsettled.
The differences in Qbr(s-p) between groups might
have some relevance for lung fluid balance in heart
failure. Indeed, in chronic heart failure, elevated
pulmonary vascular pressures are tolerated better
than in acute heart failure, both at rest and during
exercise, and there is evidence that similar elevations
of left atrial pressure produce a less severe pulmonary
edema when attained chronically.2'24 This means that
one or more of the several pathways that can participate to removal of the excessive lung fluids have
undergone some adaptive changes. Excessive extravascular lung fluids accumulate in cuffs around
peribronchial and perivascular loose connective tissue where a network of bronchial capillaries is
located. Recent evidence supporting the role of
intrapulmonary bronchial circulation as a significant
pathway for removal of excessive lung fluids has been
reported.",25'26 In particular, it has been documented
that, even in the absence of pulmonary blood flow,
bronchial circulation is able to clear interstitial
liquid.27
Blood flow in the intrapulmonary bronchial circulation is from the systemic to the pulmonary vessels but changes to from the pulmonary to the
systemic circulation in case of elevation of pulmonary venous pressure.11'12 In experimental models,
the relationship between pulmonary venous pressure
and blood flow in the intrapulmonary bronchial vessels has been found to be linear,'2'20 but this relationship can be affected by systemic artery and right
heart pressures.12'28 The blood pressure in pulmonary
circulation at which the direction of blood flow
through the intrapulmonary bronchial vessels changes
has been questioned.'2'20 Recently, Wagner20 showed
that this pressure is around 20 mm Hg. Therefore,
considering that Qbr(s-p) was measured in our study
with pulmonary vascular pressure around 0 mm Hg,
assuming the existence of a linear relationship between Qbr(s-p) and pulmonary vascular pressure also
in humans and assuming 20 mm Hg as the pressure
at which blood flow in the bronchial vessels starts to
be from the pulmonary to the systemic circulation, a
diagram of Qbr(s-p) vs pulmonary wedge pressure
can be drawn for each of the groups we studied (Fig
2). Using the same assumptions and considering the
pulmonary wedge pressure measured preoperatively,
we estimated the Qbr(s-p) during normal conditions
and observed that flow in the intrapulmonary bronchial vessels was probably reversed in patients with
heart failure. From Figure 2 it may also be suggested
that in long-term heart failure with pulmonary
hypertension, the magnitude of blood leaving the
lung vasculature is relevant and so bronchial circulation might significantly contribute to lung fluid removal in chronic heart failure. It is recognized that
when drawing the Qbr(s-p)/pulmonary wedge pressure diagram, right atrial pressure changes due to
chronic heart failure were not considered and actually the animal experimental models, from which this
relationship was derived, assume a low right atrial
pressure; on the contrary, it is known that increasing
right atrial pressure reduces bronchial blood flow
through the bronchial veins (to the right heart) and
worsens pulmonary edema.25'29 Therefore, the hemodynamic model we propose is limited because it
applies to the condition of elevated pulmonary
venous pressure and low right heart pressure, because
it is based on several assumptions and because it does
not take into account the other pathways that contribute to lung fluid homeostasis in heart failure." 2 In
conclusion, our data show that with chronic heart
failure, bronchial circulation undergoes changes that
produce a reduction of vascular resistances. We hypothesized that low resistance allows a significant
blood flow out of the lungs when pressures in the
pulmonary vasculature are elevated.
REFERENCES
1 Matthay MA. The bronchial and systemic circulation in lung
and pleural fluid and protein balance. In: Butler J, ed. The
bronchial circulation. New York: Marcel Dekker, 1992; 389-415
2 Matthay MA. Resolution of pulmonary edema: mechanisms of
liquid, protein and cellular clearance from the lung. Clin Chest
Med 1985; 6:521-45
3 Staub NC. Pulmonary edema. Physiol Rev 1974; 54:678-811
4 Erdmann J III, Vaughan TR, Brigham KL, et al. Effect of increased vascular pressure on lung fluid balance in unanesthetized sheep. Circ Res 1975; 37:271-84
5 Gee MH, Spath JA. The dynamics of the lung fluid filtration
system in dogs with edema. Circ Res 1980; 46:796-801
6 Grimbert FA, Martin D, Packer JC, et al. Lymph flow during
increase in pulmonary blood flow and microvascular pressure
in dogs. Am J Physiol 1988; 255:H1149-H1155
CHEST / 107/ 5 / MAY, 1995
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1251
Table 2-Duration, Extracorporeal Circulation Pump Flow, and Body Temperature During Qbr(s-p) Measurements*
Patient
Co,
Time,
min
L/min
P Airways,
mm Hg
T Es,
°C
T Rectum,
°C
T Blood,
°C
25
28
15
22
40
35
27+9
6.0
4.3
3.8
3.4
3.3
4.3
4.2+1.0
0
0
0
0
0
0
0+0
27.9
29.9
28.5
28.0
27.6
31.9
29.0+1.6
32.1
32.0
32.0
29.4
30.0
31.5
31.2+1.2
26.3
28.3
25.9
27.7
27.0
29.0
27.4+1.2
27
20
41
15
23
18
40
26+10
4.0
5.5
3.2
3.8
2.9
4.5
5.2
4.2+1.0
0
0
0
0
4
0
0
0.6+1.5
26.8
29.4
29.0
30.1
27.2
28.5
28.0
28.4+1.2
28.9
30.4
31.9
31.6
30.2
33.6
29.0
30.8+1.7
27.9
27.2
27.0
27.7
25.9
27.0
26.8
27.1+0.7
20
15
30
38
22
26
21
30
26
24
18
16
23
40
31
25+7
4.2
4.8
3.9
3.0
5.1
3.5
3.9
3.3
4.0
4.2
4.4
4.8
5.3
4.1
4.3
4.2+0.6
0
0
0
2
0
0
0
4
0
0
2
0
0
0
0
0.5+1.2
28.0
29.6
30.1
27.6
27.9
28.1
26.9
28.0
27.9
30.1
29.0
29.1
28.0
28.5
29.5
29.2
30.4
31.0
28.0
28.2
29.4
28.5
30.1
29.1
31.2
29.9
30.6
30.1
31.6
30.3
29.8+1.1
27.1
29.0
29.0
27.5
27.0
27.6
26.9
29.2
27.6
28.8
28.0
28.5
26.9
29.0
28.2
28.0+0.9
Group 1
1
2
3
4
5
6
Mean+SE
Group 2
1
2
3
4
5
6
7
Mean+SE
Group 3
1
2
3
4
5
6
7
8
9
10
11
12
13
14
15
Mean+SE
28.6+1.0
*Time=duration of Qbr(s-p) measurements; CO=cardiac output (extracorporeal circulation pump flow); P pressure; T= temperature;
Es=esophagus; SE=standard error.
measured blood flow the lung weight changes.'2,21 It
is not possible to measure lung weight changes in
humans. However, changes of lung fluid' content
during our measurements are unlikely because pulmonary vascular pressure was, by necessity, close to
zero and so was airway pressure; therefore, fluid filtration in the lung interstitium or accumulation in the
pulmonary vasculature is unlikely. Furthermore, we
previously showed that Qbr(s-p) values obtained by
this technique are constant with time18 and there is
experimental evidence that lung weight remains
constant under similar conditions.22 With our technique, the possible blood flow from the pulmonary
circulation to the right side of the heart was impeded
by the pulmonary artery clamp. Our technique does
not interfere with the surgical procedure or prolong
the extracorporeal circulation.
It is recognized that Qbr(s-p) measurements were
done in nonphysiologic conditions. Indeed, the surgical procedure, body temperature, inspired gas humidity, absence of pulmonary flow, and close to zero
mm Hg pulmonary vascular pressure influence the
results.19 However, body temperature, inspired gas
humidity, and pulmonary hemodynamics were kept
constant during Qbr(s-p) measurements and no differences in these parameters were observed between
groups. Therefore, albeit our measurements probably do not apply to physiologic conditions, data between groups are at least comparable. Because during total cardiopulmonary bypass the pressures upstream (systemic artery), downstream (pulmonary
circulation), and around the intrapulmonary bronchial vessels (airway pressure) were similar in the
three groups, the differences in Qbr(s-p) imply
differences in resistance through the intrapulmonary
bronchial vessels. This means the existence in patients
with chronic heart failure (group 1) of more dilated
and/or larger and/or more numerous intrapulmonary bronchial vessels.
Duration of heart failure was more than 6 months
for group 1 and less than 2 months in group 2 and it
is the sole relevant difference between these groups.
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Clinical Investigations
To further strengthen this point, Qbr(s-p) was not
measured in patients with an intermediate duration
of heart failure. Patient grouping was made a priori.
A significant increase of intrapulmonary bronchial
blood flow has been reported previously in several
chronic diseases that affect the lungs.8"13-'6 In models of acute pulmonary embolism, bronchial blood
flow is reduced21-23 but it is increased in lungs of animals with previous pulmonary embolism.'4 Beside
the duration of heart failure, the severity of the pulmonary hemodynamic impairment might contribute
to Qbr(s-p) changes. Patients in groups 1 and 2 had
comparable hemodynamics at preoperative evaluation. However, this is a single measurement obtained
at rest, and is possibly not representative of real pulmonary hemodynamic behavior. Therefore, although
several mechanisms might be postulated,'4 the influence of time course and severity of heart failure on
intrapulmonary bronchial circulation remains unsettled.
The differences in Qbr(s-p) between groups might
have some relevance for lung fluid balance in heart
failure. Indeed, in chronic heart failure, elevated
pulmonary vascular pressures are tolerated better
than in acute heart failure, both at rest and during
exercise, and there is evidence that similar elevations
of left atrial pressure produce a less severe pulmonary
edema when attained chronically.2'24 This means that
one or more of the several pathways that can participate to removal of the excessive lung fluids have
undergone some adaptive changes. Excessive extravascular lung fluids accumulate in cuffs around
peribronchial and perivascular loose connective tissue where a network of bronchial capillaries is
located. Recent evidence supporting the role of
intrapulmonary bronchial circulation as a significant
pathway for removal of excessive lung fluids has been
reported.",25'26 In particular, it has been documented
that, even in the absence of pulmonary blood flow,
bronchial circulation is able to clear interstitial
liquid.27
Blood flow in the intrapulmonary bronchial circulation is from the systemic to the pulmonary vessels but changes to from the pulmonary to the
systemic circulation in case of elevation of pulmonary venous pressure.11'12 In experimental models,
the relationship between pulmonary venous pressure
and blood flow in the intrapulmonary bronchial vessels has been found to be linear,'2'20 but this relationship can be affected by systemic artery and right
heart pressures.12'28 The blood pressure in pulmonary
circulation at which the direction of blood flow
through the intrapulmonary bronchial vessels changes
has been questioned.'2'20 Recently, Wagner20 showed
that this pressure is around 20 mm Hg. Therefore,
considering that Qbr(s-p) was measured in our study
with pulmonary vascular pressure around 0 mm Hg,
assuming the existence of a linear relationship between Qbr(s-p) and pulmonary vascular pressure also
in humans and assuming 20 mm Hg as the pressure
at which blood flow in the bronchial vessels starts to
be from the pulmonary to the systemic circulation, a
diagram of Qbr(s-p) vs pulmonary wedge pressure
can be drawn for each of the groups we studied (Fig
2). Using the same assumptions and considering the
pulmonary wedge pressure measured preoperatively,
we estimated the Qbr(s-p) during normal conditions
and observed that flow in the intrapulmonary bronchial vessels was probably reversed in patients with
heart failure. From Figure 2 it may also be suggested
that in long-term heart failure with pulmonary
hypertension, the magnitude of blood leaving the
lung vasculature is relevant and so bronchial circulation might significantly contribute to lung fluid removal in chronic heart failure. It is recognized that
when drawing the Qbr(s-p)/pulmonary wedge pressure diagram, right atrial pressure changes due to
chronic heart failure were not considered and actually the animal experimental models, from which this
relationship was derived, assume a low right atrial
pressure; on the contrary, it is known that increasing
right atrial pressure reduces bronchial blood flow
through the bronchial veins (to the right heart) and
worsens pulmonary edema.25'29 Therefore, the hemodynamic model we propose is limited because it
applies to the condition of elevated pulmonary
venous pressure and low right heart pressure, because
it is based on several assumptions and because it does
not take into account the other pathways that contribute to lung fluid homeostasis in heart failure." 2 In
conclusion, our data show that with chronic heart
failure, bronchial circulation undergoes changes that
produce a reduction of vascular resistances. We hypothesized that low resistance allows a significant
blood flow out of the lungs when pressures in the
pulmonary vasculature are elevated.
REFERENCES
1 Matthay MA. The bronchial and systemic circulation in lung
and pleural fluid and protein balance. In: Butler J, ed. The
bronchial circulation. New York: Marcel Dekker, 1992; 389-415
2 Matthay MA. Resolution of pulmonary edema: mechanisms of
liquid, protein and cellular clearance from the lung. Clin Chest
Med 1985; 6:521-45
3 Staub NC. Pulmonary edema. Physiol Rev 1974; 54:678-811
4 Erdmann J III, Vaughan TR, Brigham KL, et al. Effect of increased vascular pressure on lung fluid balance in unanesthetized sheep. Circ Res 1975; 37:271-84
5 Gee MH, Spath JA. The dynamics of the lung fluid filtration
system in dogs with edema. Circ Res 1980; 46:796-801
6 Grimbert FA, Martin D, Packer JC, et al. Lymph flow during
increase in pulmonary blood flow and microvascular pressure
in dogs. Am J Physiol 1988; 255:H1149-H1155
CHEST / 107/ 5 / MAY, 1995
Downloaded From: http://publications.chestnet.org/pdfaccess.ashx?url=/data/journals/chest/21713/ on 05/08/2017
1251
7 Matthay MA, Landolt CC, Staub NC. Differential liquid and
protein clearance from the alveoli of anesthetized sheep. J Appl
Physiol 1982; 53:96-104
8 Deffebach ME, Charan NB, Lakshminarayan S, et al. The
bronchial circulation: small, but a vital attribute to the lung. Am
Rev Respir Dis 1987; 135:463-81
9 Murata K, Itoh K, Todo G, et al. Bronchial venous plexus and
its communication with pulmonary circulation. Invest Radiol
1986; 32:24-30
10 Ohimici M, Tagaki S, Tsunematsu K, et al. Endobronchial
changes in pulmonary venous hypertension. Chest 1988; 93:
1127-32
11 Awad J, Ghys R, Lou WU, et al. Hemodynamic aspects of the
pulmonary collateral circulation: an experimental study of an
isolated pulmonary lobar circulation by means of tagged
erythrocytes. J Thorac Cardiovasc Surg 1965; 50:596-600
12 Agostoni PG, Deffebach ME, Kirk W, et al. Upstream pressure
for systemic to pulmonary bronchial blood flow in dogs. J Appl
Physiol 1987; 63:485-91
13 Charan NB, Carvalho PG. The bronchial circulation in chronic
lung infections. In: Butler J, ed. The bronchial circulation. New
York: Marcel Dekker, 1992; 535-50
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Clinical Investigations