(Circulation. 1999;100:1808-1815.)
© 1999 American Heart Association, Inc.
Clinical Investigation and Reports |
Central Pulmonary Artery Lesions in Chronic Obstructive Pulmonary Disease
A Transesophageal Echocardiography Study
From the Departments of Cardiology (A.R., C.V., V.D., M.P., R.F.) and Radiology (M.A.), Ospedale Casa Sollievo della Sofferenza, IRCCS, San Giovanni Rotondo, and the Institute of Cardiology, Catholic University Sacro Cuore (M.D., A.L., F.L.), Rome, Italy.
Correspondence to Prof Francesco Loperfido, Istituto di Cardiologia, Università Cattolica del Sacro Cuore, Complesso Integrato Columbus, Via G. Moscati, 31/33, 00168 Roma, Italy. E-mail columbus.cardio{at}linet.it
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Abstract |
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Background—In patients with acute pulmonary embolism, transesophageal echocardiography (TEE) often reveals presumably thrombotic lesions within the central pulmonary arteries (CPAs). These CPA lesions, when found in patients with primary pulmonary hypertension, have been attributed to in situ thrombosis or atherosclerosis. We hypothesized that similar CPA lesions may also develop in patients with chronic obstructive pulmonary disease (COPD) in the absence of pulmonary embolism.
Methods and Results—We examined by TEE 25 patients with COPD and 27 control patients with left heart disease. None of the patients had previous pulmonary embolism or ileofemoral and popliteal vein thrombosis. By use of TEE, CPA lesions were found in 12 COPD patients (48%) and 2 control patients (7.4%) (P<0.01). When CPA lesions were subdivided into types 1 (protruding and mobile) and 2 (wall-adherent), type 1 lesions proved to be uncommon, being found within the pulmonary trunk in 12% and 3.7% of COPD and control patients, respectively (P=NS). Conversely, type 2 lesions, which were always localized in the right pulmonary artery, were frequent in COPD patients (36%) and rare in control patients (3.7%) (P<0.01). When available, helical CT and MR angiography confirmed TEE findings, supporting an atherosclerotic origin of type 2 lesions, which were different from typical thrombotic lesions. FEV1/FVC ratio, RV/TLC ratio, PaO2, hematocrit value, and pulmonary artery systolic pressure were not significantly different in COPD patients with and without CPA lesions. At TEE, however, COPD patients with CPA lesions showed a larger size of the main and right pulmonary arteries.
Conclusions—TEE often reveals CPA lesions in stable patients with COPD even in the absence of significant pulmonary hypertension and not in close relation with the severity of pulmonary dysfunction.
Key Words: echocardiography • thrombus • pulmonary heart disease
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Introduction |
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In patients with acute pulmonary embolism, transesophageal echocardiography (TEE) frequently shows extensive (presumably thrombotic) lesions within the central pulmonary arteries.1 2 3 4 5 6 7 8 9 10 11 12 In most patients, the source of these central pulmonary artery (CPA) lesions is probably embolization from peripheral veins.13 14 However, CPA lesions with similar morphology were also found in some patients with pulmonary hypertension but no previous pulmonary thromboembolism.15 In these patients, CPA lesions were attributed to development of in situ thrombosis, although an atherosclerotic origin could not be excluded.15 CPA lesions found at TEE may be unsuspected clinically, as demonstrated in critically ill patients.16 The prevalence of these CPA lesions in other clinical settings, and in particular in patients in stable condition, remains unknown.
In an old autopsy study, 28% of patients with chronic pulmonary disease and no previous pulmonary thromboembolism had CPA lesions.17 This high rate is not surprising, because chronic pulmonary diseases are associated with pulmonary hypertension18 19 and hypercoagulability,20 which may promote either in situ thrombosis or atherosclerosis within the great pulmonary arteries. No data exist, however, on the prevalence in vivo of CPA lesions in patients with chronic pulmonary disease. Accordingly, we used TEE to determine whether vascular lesions compatible with in situ thrombosis or atherosclerosis are present at the level of the great pulmonary arteries in patients with chronic obstructive pulmonary disease (COPD) and no previous or recent pulmonary embolism. As a control, we examined a group of patients with left heart disease of various origins.
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Methods |
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Patients
Between January 1995 and January 1997, we examined by TEE 27 consecutive outpatients with chronic pulmonary disease (obstructive pattern) and, as a control group, 27 consecutive patients with left heart disease of various origins. All patients were in stable clinical condition. In particular, patients did not have a history of pulmonary embolism or recent symptoms suggesting a diagnosis of pulmonary embolic events, such as sudden onset of dyspnea or pleuritic chest pain.14 Moreover, all patients were <75 years old, and none of them had acquired conditions often associated with pulmonary embolism, such as recent surgery, trauma, immobilization, cancer, obesity, or localized or unilateral swelling of an extremity.14 All patients in both the study and the control groups underwent color Doppler ultrasonography of the lower extremities, and neither ileofemoral nor popliteal vein thrombosis was detected in any of them.
COPD was diagnosed on the basis of clinical history, physical examination, chest radiograph, arterial blood gas analysis, and pulmonary-function tests (FEV1/FVC <70% of the predicted value). As an index of lung hyperinflation, the residual volume/total lung capacity ratio (RV/TLC) was calculated. Two patients with COPD were excluded from analysis because of incomplete echocardiographic examination owing to severe discomfort during the procedure. Thus, the study group consisted of 25 patients (22 men and 3 women, mean age±SD 65±6 years, ranging from 53 to 74 years). In the control group, there were 15 men and 12 women (mean age±SD 61±14 years, ranging from 39 to 72 years). Ten patients had ischemic heart disease, 11 had mitral valve disease (6 with pure mitral valve stenosis), and 6 had primary dilated cardiomyopathy.
Echocardiography
Transthoracic echocardiography
(TTE) and TEE were performed with an Aloka SSD-870 or an Acuson 128
XP/5 system using 2.25- or 3.5-MHz transducers for TTE and 5.0-MHz
multiplane transducers for TEE. All studies were stored on a
1/2-inch video recorder for subsequent review. Two observers
unaware of the clinical findings reviewed each study.
TTE was performed with the patient lying in the left recumbent position. Craniocaudal and lateral dimensions of the right atrium and ventricle were measured in the 4-chamber apical view at end systole and end diastole, respectively. Fixed or mobile lesions within the right atrium or ventricle were noted. Tricuspid regurgitation was determined by color Doppler. Pulmonary artery systolic pressure (PASP) was estimated by continuous-wave Doppler analysis of tricuspid regurgitation jet.
TEE was performed in the fasting state and after the patients' histories had been assessed for esophageal disorders. We did not administer sedatives or analgesics intravenously to any of the patients. The transducer was introduced with the patient lying in the left recumbent position. The base of the heart was first imaged in the short-axis view. Then the transducer was tilted and withdrawn superiorly to visualize the main and proximal right and left pulmonary arteries.1 The left pulmonary artery could be imaged on the transverse plane only in its proximal segment because of interposition of the left main bronchus. The right pulmonary artery was imaged on the transverse plane along its entire course up to the division into its major lobar branches. For longitudinal plane imaging, the transducer was rotated slightly to the right to visualize the pulmonary valve and the main pulmonary artery up to its bifurcation. With further rightward rotation, the right pulmonary artery could be imaged in the short-axis view. Similarly, the left pulmonary artery was imaged by rotating the transducer laterally after imaging of the main pulmonary artery. The diameter of the main, right, and left pulmonary arteries was measured at the origin of the vessels whenever possible.
We noted any echolucent lesions present in both transverse and longitudinal scanning in any segment of the great pulmonary arteries. On the basis of their pattern and mobility,1 CPA lesions were classified as type 1 when they were in part protruding and mobile, suggesting thromboembolism, and as type 2 when they were totally wall-adherent (either laminated or only in part protruding). No attempt was made to subdivide type 2 lesions into thrombotic and atherosclerotic on the basis of their TEE morphology. Artifact images within the pulmonary arteries were excluded through fine adjustments of the transducer rotation in each plane, by modifying the gain regulation settings, and with the aid of color Doppler flow imaging. Location and mobility patterns of structures adjacent to the transducer were also considered to exclude a reverberation phenomenon. In particular, fine linear echoes within the right pulmonary artery were considered to be probable reverberation from the right pulmonary posterior wall.21 A spontaneous contrastographic effect inside the pulmonary artery was also noted.
Other Imaging Techniques
Helical CT, MR angiography after Gd-DTPA injection, and
conventional pulmonary angiography were available in 6, 4, and
1 COPD patients, respectively.
Statistical Analysis
Comparisons of continuous and discrete variables were made
by the t test for unpaired data and either
2 or Fisher's exact test as appropriate. A
value of P<0.05 was considered to be significant.
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Results |
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Patients With COPD Versus Control Patients
Atrial fibrillation was present in 4 COPD patients (16%) and 11 control patients (40.7%) (P=0.09) (Tables 1
and 2).
On TTE, no COPD or control patient had right atrial or
ventricular thrombus. There was no difference in the size
of the right atrium and ventricle or prevalence of tricuspid
regurgitation between COPD and control patients. PASP
tended to be greater in COPD patients than in control patients,
considering only individuals in whom PASP could be assessed (n=14 and
17, respectively), but the difference was not significant. At TEE, the
main and right pulmonary arteries were visualized along their
entire course in transverse and longitudinal planes in all COPD and
control patients. In contrast, the left pulmonary artery was
visualized exclusively in its proximal portion (transverse plane) and
in only 19 of 25 COPD patients (76%) and 19 of 27 control patients
(70%) (P=NS). The diameter of the CPA was not different
between COPD and control patients.
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CPA lesions were found in 12 COPD patients (48%) and 2 control
patients (7.4%) (P<0.01) (Table 3). Examples of type 1 and type 2 CPA
lesions are shown in Figures 1 and 2, respectively. The 2 control patients
with CPA lesions (1 of type 1 and 1 of type 2) had mitral valve
stenosis with mild pulmonary hypertension. Type 1 and
type 2 CPA lesions were found in 3 (12%) and 9 (36%) COPD patients,
respectively (P=NS and P=<0.01, respectively,
versus control group [both: 3.7%]). One patient with COPD had 2 type
2 CPA lesions in the right pulmonary artery.
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All type 1 CPA lesions were found at the level of the pulmonary trunk, in contrast with those of type 2, which were found exclusively at the level of the proximal right pulmonary artery. No patient had lesions in the left pulmonary artery. No CPA lesion was occluding or obstructive, as assessed by color and pulsed-wave Doppler. All type 1 CPA lesions were attached to the vessel wall. Their size ranged from 2 to 5 cm in length and from 1x3 to 2x5 cm in cross section. Type 2 CPA lesions measured 3 to 7 cm in length and 2x2 to 3x5 cm in cross section. In no patient was a spontaneous echo-contrast phenomenon noted.
Helical CT was available in 4 COPD patients with CPA lesions (1 of type
1 and 3 of type 2) and in 2 without. In all these patients, CT scanning
confirmed TEE findings. However, CPA lesions appeared to be smaller by
helical CT scanning than by TEE. An example of a type 2 CPA lesion at
helical CT scanning is shown in Figure 3.
MR angiography after Gd-DTPA injection was available in 4 COPD patients
with CPA lesions (2 of type 1 and 2 of type 2). In 3 of them (2 with
type 1 and 1 with type 2 lesions), MR angiography confirmed the
presence of some abnormality within the CPA. Also with MR angiography,
type 1 lesions were similar to those often visible in pulmonary
thromboembolism. The type 2 lesion was stratified on the right
pulmonary artery wall and was well evident in either the
coronal or sagittal plane (Figure 4). In
the other patient with a type 2 lesion by TEE, no CPA abnormality was
found by MR angiography. Another patient with a type 2 lesion underwent
conventional pulmonary angiography, which confirmed the
presence of a lesion within the right pulmonary artery.
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COPD Patients With CPA Lesions Versus Those Without
COPD patients with and without CPA lesions were similar in age,
prevalence of atrial fibrillation, hematocrit value,
PaO2, FEV1/FVC
ratio, and RV/TLC ratio (Table 4). The
right atrial and ventricular sizes and prevalence of
tricuspid regurgitation were similar in COPD patients
with and without CPA lesions. Among patients in whom it could be
assessed (75% and 38% of those with and without CPA lesions,
respectively), PASP tended to be greater in those with CPA lesions than
in those without (49±18 versus 38±18 mm Hg, respectively;
P=NS). PASP could be assessed in 7 of 9 patients with type 2
CPA lesions and was 
40 mm Hg in 4 patients and <40 mm Hg
in 3. The diameters of the pulmonary trunk and right
pulmonary artery were significantly greater in patients with
CPA lesions than in those without (P=<0.05 for both).
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Discussion |
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We have hypothesized that patients with chronic pulmonary disease and no pulmonary embolism may show CPA lesions at TEE. In COPD patients, in fact, reversible or fixed pulmonary hypertension,18 19 prothrombotic state,20 and hypoxemia22 might promote metabolic and structural changes in the artery wall resulting in in situ thrombosis or atherosclerosis. Confirming our hypothesis, CPA lesions were detected by TEE in 48% of our COPD patients, who were clinically stable and did not have previous pulmonary embolism. Specifically, 12% of COPD patients had slightly motile masses that were protruding into the pulmonary trunk (type 1 lesions), and 36% of them had flat or rounded lesions that were totally adherent to the right pulmonary artery wall (type 2 lesions). CPA lesions were remarkably frequent in COPD patients in comparison with the low prevalence (7.4%) in cardiac patients.
These findings in COPD patients can be explained by silent thromboembolism, in situ thrombosis, or pulmonary atherosclerosis. The first mechanism is convincing only for type 1 CPA lesions. These lesions, in fact, were morphologically similar to typical thromboembolism except for their modest motility and absence of obstruction.1 2 3 4 5 6 7 8 9 10 11 12 The localization of type 2 CPA lesions in the right pulmonary artery may be in favor of thromboembolism, because the right branch is prone to receive emboli for flow continuity with the pulmonary trunk.5 Conversely, they were morphologically different from thromboembolism. Moreover, silent thromboembolism is rare, being described only in patients with prolonged immobilization from bed rest, recent major surgery, severe congestive heart failure, intubation, etc,16 a clinical context different from that of our study patients, who did not have recent or worsening dyspnea or peripheral vein thrombosis. Thus, although we did not perform pulmonary scintigraphy or lung and abdominal CT scans as a protocol, we judge silent thromboembolism to be an unlikely pathogenetic mechanism because of the high prevalence of CPA lesions and their peculiar occurrence in stable COPD patients.
Type 2 CPA lesions may be more appropriately explained by in situ thrombosis or, alternatively, by wall thickening with superimposed atherosclerotic debris. In fact, pulmonary arteries often develop thrombosis or wall hypertrophy in response to injury.23 24 25 Thrombotic lesions are common in the peripheral nonelastic pulmonary arteries of patients with pulmonary hypertension.26 27 28 Similar lesions have also been detected in the central elastic pulmonary arteries of a few patients with primary pulmonary hypertension and were considered to be engrafted on intimal injury caused by prolonged exposure to high blood pressure.15 However, atherosclerosis also may develop in the presence of increased pulmonary flow or pressure.24 25 A definitive distinction between layered in situ thrombus and atheroma is probably very difficult by available techniques, including intravascular ultrasound.29 Helical CT scans and MR angiography were available in some of our COPD patients with CPA lesions. The presence of some CPA abnormality was in most cases confirmed by both CT and MR angiography, but the lesions were less evident by these techniques than by TEE. Most importantly, also at CT and at MR angiography, CPA type 2 lesions appeared to be different from typical pulmonary thrombotic lesions. Rather, they showed some morphological similarities with the atherosclerotic lesions of the aorta.30 Consequently, even in the absence of firm anatomic confirmation, we suggest that TEE type 2 lesions may actually represent CPA atherosclerosis.
We never found lesions within the left pulmonary artery. However, having imaged this artery only proximally and only in 76% of COPD patients, we could not exclude a more distal localization of lesions in it. It is possible, then, that CPA lesions are more frequent in COPD patients than found in this study.
CPA lesions were rare in our control patients with left heart disease, although PASP was not lower in them than in COPD patients. In particular, the 2 patients with mitral valve stenosis showing CPA lesions (1 of type 1 and the other of type 2) had only mild pulmonary hypertension. Our data then suggest that at least type 2 CPA lesions may be peculiar to COPD. However, more data are necessary to determine their exact prevalence in various cardiac diseases.
When we compared PASP, FEV1/FVC ratio, RV/TLC ratio, PaO2, and the right atrial and ventricular size in COPD patients with and without CPA lesions, no significant differences were found. CPA lesions were not closely related to the degree of pulmonary dysfunction or to PASP, as assessed at the time of the study. We emphasize that CPA lesions were also present in some patients with mild ventilatory obstruction and without significant pulmonary hypertension. The only parameter separating COPD patients with and without CPA lesions was the size of the main and the right pulmonary arteries, which was greater in the former group. It remains to be determined whether dilatation, either primary or secondary to reversible pulmonary hypertension, may predispose CPA to development of shear-related wall lesions. The absence of a relation in our patients between the degree of pulmonary hypertension and the severity of airflow obstruction, which was in general not severe, may be explained in part by lung hyperinflation: in fact, some of our patients with elevated PASP estimates but only moderate airflow obstruction showed disproportionate increase in the RV/TLC ratio, indicative of significant air trapping. In these patients, however, unsuspected chronic thromboembolic pulmonary vascular disease with extensive downstream vascular obstruction could not be definitively excluded.
It can be hypothesized that coagulation disorders and endothelial dysfunction may also promote in situ thrombosis or atherosclerosis within CPA in COPD patients. The only pertinent parameter assessed in our study was the hematocrit, which was not different in COPD patients with and without CPA lesions. However, platelet functions31 or hemocoagulative parameters, including prothrombin F1+2 fragment and fibrinogen plasma levels,20 may be more relevant and warrant further studies.
Conclusions
Our findings may have some clinical implications. In the absence
of thromboembolism arising from peripheral veins,
unexplained acute respiratory failure might be attributed in some COPD
patients to distal migration of atherothrombotic material from the
great pulmonary arteries. Moreover, the progressive growth of
CPA lesions might contribute to further increase in pulmonary
artery pressure, with possible therapeutic implications, such as
long-term anticoagulation. Further studies in large populations are
necessary, however, to confirm our TEE findings in obstructive and
nonobstructive forms of chronic pulmonary disease and to
understand their mechanisms.
Received April 9, 1999; revision received June 28, 1999; accepted July 2, 1999.
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References |
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|---|
1. Wittlich N, Erbel R, Eichler A, Schuster S, Jakob H, Iversen S, Oelert H, Meyer J. Detection of central pulmonary artery thromboemboli by transesophageal echocardiography in patients with severe pulmonary embolism. J Am Soc Echocardiogr. 1992;5:515–524.[Medline] [Order article via Infotrieve]
2. Lengyel M. The role of transesophageal echocardiography in the management of patients with acute and chronic pulmonary thromboembolism. Echocardiography. 1995;12:359–366.[Medline] [Order article via Infotrieve]
3. Klein AL, Stewart WC, Cosgrove DM, Mick MJ, Salcedo E. Visualization of acute pulmonary emboli by transesophageal echocardiography. J Am Soc Echocardiogr. 1990;3:412–415.[Medline] [Order article via Infotrieve]
4. Barton CW, Eisenberg MJ, Schiller N. Transesophageal echocardiographic diagnosis of massive pulmonary embolism during cardiopulmonary resuscitation. Am Heart J. 1994;127:1639–1642.[Medline] [Order article via Infotrieve]
5. Fishel RS, Merlino JD, Felner JM. Diagnosis of main-stem pulmonary thromboemboli by transesophageal echocardiography. Echocardiography. 1994;11:189–195.[Medline] [Order article via Infotrieve]
6.
Pruszczyk P, Torbicki A, Kuch-Wocial A, Chlebus M,
Miökiewicz ZC, Jedrusik P. Transesophageal
echocardiography for definitive diagnosis of
haemodynamically significant pulmonary embolism. Eur
Heart J. 1995;16:534–538.
7.
Torbicki A, Pacho R, Jedrusik P, Pruszczyk P.
Noninvasive diagnosis and treatment of a saddle pulmonary
embolism. Chest. 1996;109:1124–1126.
8. Rittoo D, Sutherland GR, Samuel L, Flapan AD, Shaw TRD. Role of transesophageal echocardiography in diagnosis and management of central pulmonary artery thromboembolism. Am J Cardiol. 1993;71:1115–1118.[Medline] [Order article via Infotrieve]
9.
Rittoo D, Sutherland GR. Acute pulmonary
artery thromboembolism treated with thrombolysis:
diagnostic and monitoring uses of
transesophageal echocardiography.
Br Heart J. 1993;69:457–459.
10.
Chan RKM, Johns JA, Calafiore P. Clinical implications
of the morphological features of central pulmonary artery
thromboemboli shown by transesophageal
echocardiography. Br Heart J. 1994;72:58–62.
11. Neökovic AN, Popovic AD, Babic R, Otasevic P, Bojic M. Color Doppler transesophageal echocardiography in detection of massive pulmonary embolism. Echocardiography. 1996;13:631–633.[Medline] [Order article via Infotrieve]
12.
Cerel A, Burger AJ. The diagnosis of a
pulmonary artery thrombus by transesophageal
echocardiography. Chest. 1993;103:944–945.
13.
American College of Chest Physicians Consensus
Committee on Pulmonary Embolism. Opinions regarding diagnosis
and management of venous thromboembolic disease. Chest. 1996;109:233–237.
14.
Goldhaber SZ, Morpurgo M, for the WHO/ISFC Task Force
on Pulmonary Embolism. Diagnosis, treatment and prevention of
pulmonary embolism. JAMA. 1992;268:1727–1733.
15.
Moser KM, Fedullo PF, Finkbeiner WE, Golden J. Do
patients with primary pulmonary hypertension develop extensive
central thrombi? Circulation. 1995;91:741–745.
16.
Patel JJ, Chandrasekaran K, Maniet AR, Ross JJ, Weiss
RL, Guidotti JA. Impact of the incidental diagnosis of clinically
unsuspected central pulmonary artery thromboembolism in
treatment of critically ill patients. Chest. 1994;105:986–990.
17. Mitchell RS, Silvers GW, Dart GA, Petty TL, Vincent TN, Ryan SF, Filley GF. Clinical and morphologic correlations in chronic airway obstruction. Am Rev Respir Dis. 1968;97:54–62.
18.
Burghuber OC, Hartter E, Punzengruber C, Weissel M,
Woloszczuk W. Human atrial natriuretic peptide secretion in
precapillary pulmonary hypertension. Chest. 1988;93:31–37.
19.
Miguéres M, Escamilla R, Coca F, Didier A, Krempf
M. Pulsed Doppler echocardiography in the
diagnosis of pulmonary hypertension in COPD. Chest. 1990;98:280–285.
20. Alessandri C, Basili S, Violi F, Ferroni P, Gazzaniga PP, Cordova C, COBH Group. Hypercoagulability state in patients with chronic obstructive pulmonary disease. Thromb Haemost. 1994;72:343–346.[Medline] [Order article via Infotrieve]
21. Evangelista A, Garcia-del-Castillo H, Gonzalez-Alujas T, Dominguez-Oronoz R, Salas A, Permanyer-Miralda G, Soler-Soler J. Diagnosis of ascending aortic dissection by transesophageal echocardiography: utility of M-mode in recognizing artifacts. J Am Coll Cardiol. 1996;27:102–107.[Abstract]
22. Ingram RH. Chronic bronchitis, emphysema, and airways obstruction. In: Isselbacher KJ, et al, eds. Harrison's Principles of Internal Medicine. 13th ed. New York, NY: McGraw-Hill; 1994; 2:1197–1206.
23. Chaouat A, Weitzenblum E, Higenbottam T. The role of thrombosis in severe pulmonary hypertension. Eur Respir J. 1996;9:356–363.[Abstract]
24. Heath D, Wood EH, DuShane JW, Edwards JE. The relation of age and blood pressure to atheroma in the pulmonary arteries and thoracic aorta in congenital heart disease. Lab Invest. 1960;9:259–272.[Medline] [Order article via Infotrieve]
25. Langleben D. Atherosclerosis and the lung. Can J Cardiol. 1990;6:VI.
26.
Wagenvoort CA, Mulder PGH. Thrombotic lesions in
primary plexogenic arteriopathy. Chest. 1993;103:844–849.
27.
Wagenvoort CA. Lung biopsy specimens in the evaluation
of pulmonary vascular disease. Chest. 1980;77:614–625.
28.
Moser KM, Bloor CM. Pulmonary vascular lesions
occurring in patients with chronic major vessel thromboembolic
pulmonary hypertension. Chest. 1993;103:685–692.
29.
Kravitz KD, Scharf GR, Chandrasekaran K. In vivo
diagnosis of pulmonary atherosclerosis.
Chest. 1994;106:632–634.
30.
Summers RM, Andrasko-Bourgeois J, Feuerstein IM, Hill
SC, Jones EC, Busse MK, Wise B, Bove Ke, Rishforth Ba, Tucker E, Spray
TL, Hoeg JM. Evaluation of aortic root by MRI: insights from patients
with homozygous familial hypercholesterolemia.
Circulation. 1998;98:509–518.
31. Christman BW, McPherson CD, Newman JH, King GA, Bernard GR, Groves BM, Loyd JE. An imbalance between the excretion of thromboxane and prostacyclin metabolites in pulmonary hypertension. N Engl J Med. 1992;327:70–75.[Abstract]
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