(Radiology. 1999;211:549-553.)
© RSNA, 1999
Hypoxemia and Liver Cirrhosis (Hepatopulmonary Syndrome) in Eight Patients: Comparison of the Central and Peripheral Pulmonary Vasculature1
Ki-Nam Lee, MD,
Ha-Jong Lee, MD,
Woo Won Shin, MD and
W. Richard Webb, MD
1 From the Departments of Diagnostic Radiology (K.N.L., H.J.L.) and Internal Medicine (W.W.S.), Dong-A University College of Medicine, 3-1 Ga, Tong-daesin-Dong, Seo-Ku, Pusan 602-103, Korea, and the Department of Radiology, University of California San Francisco, Calif (W.R.W.). Received February 16, 1998; revision requested April 16; final revision received September 14; accepted October 28. Address reprint requests to K.N.L.
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Abstract
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PURPOSE: To evaluate the pulmonary vasculature in patients with hepatopulmonary syndrome.
MATERIALS AND METHODS: Conventional computed tomographic (CT) scans in eight patients with hepatopulmonary syndrome were retrospectively evaluated to compare the diameters of the pulmonary trunk, right and left main pulmonary arteries, and peripheral pulmonary vasculature in the right posterior basal segment with those in eight healthy subjects and in four patients with normoxemic cirrhosis. With thin-section CT, the ratio of segmental arterial diameter to adjacent bronchial diameter in the right lower lobe in four patients with hepatopulmonary syndrome was compared with that in four patients with normoxemic cirrhosis.
RESULTS: In patients with hepatopulmonary syndrome, the peripheral pulmonary vasculature was significantly dilated compared with that in control subjects and in patients with normoxemic cirrhosis (P = .002); however, the central pulmonary arteries were not significantly dilated (P > .05). At thin-section CT, the ratio of segmental arterial diameter to adjacent bronchial diameter was significantly greater than that in patients with normoxemic cirrhosis (P < .05).
CONCLUSION: In patients with hepatopulmonary syndrome, the peripheral pulmonary vasculature is significantly dilated. Dilatation of the peripheral pulmonary vasculature may be helpful in the diagnosis of hepatopulmonary syndrome.
Index terms: Computed tomography (CT), 68.1211, 68.12118 • Liver, diseases, 761.794 • Lung, CT, 68.1211, 68.12118 • Pulmonary arteries, abnormalities, 564.1551 • Pulmonary arteries, CT, 564.1211, 564.12118
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Introduction
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Hepatopulmonary syndrome is defined as the triad of hepatic dysfunction, intrapulmonary vascular dilatation, and abnormal arterial oxygenation (hypoxemia) (1–5). It may also result in dyspnea, platypnea, and orthopnea (1,4). Clinical hepatopulmonary syndrome manifests with progressive dyspnea and hypoxemia in patients with cirrhosis (6).
Radiographic findings in patients with hepatopulmonary syndrome may include bibasilar nodular or reticular opacities on chest radiographs, dilated peripheral lung vessels at conventional computed tomography (CT), and peripheral arteriolar dilatation at pulmonary angiography (7). However, to our knowledge, a comprehensive description of both the central and peripheral arterial diameters in patients with hepatopulmonary syndrome has not been reported. Therefore, we undertook a retrospective review of the conventional CT studies in eight patients with hepatopulmonary syndrome to evaluate the diameters of the central and peripheral pulmonary vessels and to compare them with those in eight healthy subjects and those in four patients with normoxemic cirrhosis (ie, cirrhosis without hypoxemia). We also compared the ratio of segmental arterial diameter to bronchial diameter, which was measured by using thin-section CT, in four patients with hepatopulmonary syndrome and in four patients with normoxemic liver cirrhosis.
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MATERIALS AND METHODS
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We reviewed the CT scans obtained in 12 patients who had liver cirrhosis, hypoxemia (partial pressure of oxygen less than 70 mm Hg at arterial blood gas analysis), and dyspnea and who underwent a CT examination of the thorax at our institution between August 1993 and December 1996. Four of the 12 patients had pulmonary tuberculosis (n = 3) or bronchogenic carcinoma (n = 1); these patients were excluded from the study because other combined lung disease might influence dyspnea or hypoxemia. Therefore, the study group included eight patients (five men, three women; age range, 54–70 years; mean age ± SD, 63.5 years ± 5.3).
To provide a control group, we randomly selected eight healthy individuals (four men and four women older than 54 years; age range, 54–66 years; mean age, 59.6 years ± 4.4) who had undergone conventional CT. In addition, we reviewed the CT scans obtained in four patients (all men aged 55–64 years; mean age, 59.5 years ± 3.7) who had liver cirrhosis without hypoxemia or dyspnea between August 1996 and December 1996. These patients underwent both conventional CT and thin-section CT of the thorax.
We reviewed the clinical and laboratory data on the eight patients with hepatopulmonary syndrome, eight control subjects, and four patients with normoxemic liver cirrhosis (Table 1). The present study was based on a retrospective analysis of their CT scans. The scans were obtained with use of a Highlight scanner (GE Medical Systems, Milwaukee, Wis) with the patient in the supine position at full inspiration. Mediastinal window settings (level, 30 HU; width, 450 HU) were used to measure the diameters of the central pulmonary arteries (ie, main pulmonary trunk and both right and left main pulmonary arteries). The lung window settings (level, -600 HU; width, 1,500 HU) were used to measure the peripheral pulmonary vasculature.
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TABLE 1. Clinical and Laboratory Data at or near CT Measurements of the Central and Peripheral Pulmonary Vascular Diameters in Patients with Hepatopulmonary Syndrome, Healthy Subjects, and Patients with Normoxemic Cirrhosis
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The diameters of the pulmonary trunk at the level above the pulmonic valve, of the right main pulmonary artery between the anterior wall of the right main bronchus and posterior wall of the superior vena cava, and of the left main pulmonary artery at the level above the left main bronchus were measured (8,9) with a Vernier caliper (millimeters, with two decimals) by consensus between two of the authors (K.N.L., H.J.L.). To determine the peripheral pulmonary vessel size, three to five pulmonary arteries in the basal right lower lobes, within 2 cm of the pleural surface, were measured with conventional CT, and their diameters were averaged. This location was chosen to avoid cardiac pulsation artifacts.
We correlated the peripheral pulmonary vascular diameter with the partial pressure of arterial oxygen, total bilirubin level, and serum albumin level in patients with hepatopulmonary syndrome. The interval between the CT examination and laboratory study ranged from 1 to 3 days.
Eight thin-section CT scans were obtained in four patients with hepatopulmonary syndrome and in four patients with normoxemic cirrhosis (bone algorithm window width/window level, 700 HU/-1,500 HU). We calculated the ratio of the diameter of the segmental artery to the luminal diameter of its accompanying bronchus in the basal segments of the right lower lobe (n = 24, 12 segmental arteries and 12 bronchi in each patient with hepatopulmonary syndrome and normoxemic cirrhosis).
Pulmonary angiography was performed in one patient with hepatopulmonary syndrome to evaluate whether dilated peripheral pulmonary vessels represented pulmonary arterioles or dilated arteriovenous connections.
Statistical Analyses
Statistical analyses were performed with SAS software (SAS Institute, Cary, NC) on a minicomputer. The difference in the mean diameters of the central and peripheral pulmonary vessels between groups was tested according to the Kruskal-Wallis test. The correlation coefficients were calculated with linear regression analysis.
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RESULTS
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The diameters of the pulmonary trunk, right and left main pulmonary arteries, and peripheral vessels of the basal right lower lobes in the patients with hepatopulmonary syndrome, healthy subjects, and patients with liver cirrhosis without hypoxemia or dyspnea are listed in Table 1. The mean diameters of the pulmonary trunk and right main pulmonary arteries in the patients with hepatopulmonary syndrome were slightly larger than were those in the healthy subjects and the patients with normoxemic cirrhosis, but these differences were not significant (P > .05) (Table 2). However, the diameters of the right basal peripheral vessels were significantly larger in patients with hepatopulmonary syndrome compared with those in the healthy subjects (P < .05) (Fig 1) and in the patients with liver cirrhosis without hypoxemia or dyspnea (P = .002)
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TABLE 2. Mean Diameters of the Pulmonary Vasculature in Eight Patients with Hepatopulmonary Syndrome, Eight Healthy Subjects, and Four Patients with Normoxemic Cirrhosis
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Figure 1a. CT scans of the right lower lobe. (a) CT scan obtained in a 64-year-old man with hepatopulmonary syndrome shows tortuous dilated peripheral vessels (arrows) 2 cm from the pleura. The vessels were measured by using a Vernier caliper. (b) CT scan obtained in a 63-year-old man, a healthy control subject, near the same level as in a shows smaller peripheral pulmonary vessels (arrows).
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Figure 1b. CT scans of the right lower lobe. (a) CT scan obtained in a 64-year-old man with hepatopulmonary syndrome shows tortuous dilated peripheral vessels (arrows) 2 cm from the pleura. The vessels were measured by using a Vernier caliper. (b) CT scan obtained in a 63-year-old man, a healthy control subject, near the same level as in a shows smaller peripheral pulmonary vessels (arrows).
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In the patients with hepatopulmonary syndrome, the diameters of the peripheral pulmonary vessels were inversely correlated with the partial pressure of arterial oxygen (r = -0.907, P = .002); this was also true when the patients with hepatopulmonary syndrome and those with normoxemic cirrhosis were considered together (r = -0.91, P = .001) (Fig 2). However, the correlation of peripheral pulmonary vessel diameter to serum albumin level and total bilirubin level was not significant (P > .05). The diameter of the main pulmonary artery did not correlate significantly with the bilirubin level, albumin level, or partial pressure of arterial oxygen in patients with hepatopulmonary syndrome or in the combined group of patients with hepatopulmonary syndrome and patients with normoxemic cirrhosis (all P > .05).
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Figure 2. Correlation of peripheral pulmonary vessel diameter and partial pressure of arterial oxygen in eight patients with hepatopulmonary syndrome and four patients with normoxemic cirrhosis. The peripheral pulmonary vessel diameter correlated significantly and inversely with the partial pressure of arterial oxygen (PaO2) (r = -0.91, P = .001). ABGA = arterial blood gas analysis.
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At thin-section CT, the mean diameters of the right basal segmental arteries and adjacent bronchi were 7.6 mm and 3.8 mm, respectively, in the patients with hepatopulmonary syndrome, and 4.7 mm and 4.3 mm, respectively, in the patients with normoxemic liver cirrhosis (Fig 3). The ratio of segmental arterial diameter to bronchial diameter was 2.0 ± 0.2 in the patients with hepatopulmonary syndrome and 1.2 ± 0.2 in the patients with normoxemic liver cirrhosis; this difference was significant (P < .05) (Table 3).
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Figure 3a. Thin-section CT scans of the right lower lobe. (a) CT scan obtained in a 68-year-old woman with hepatopulmonary syndrome. The right basal segmental pulmonary arteries are dilated. The ratio of the diameter of the segmental arteries (arrows) to the diameter of the accompanying bronchi (arrowheads) is increased compared with that in a 64-year-old man with normoxemic liver cirrhosis, whose CT scan is shown in b. Minimal pulmonary edema is likely to result in a slight increase in apparent arterial diameter. Even considering some peribronchial cuffing, the size of the arteries is clearly increased relative to that of the adjacent bronchi. (b) CT scan obtained in a 64-year-old man with normoxemic liver cirrhosis. The peripheral pulmonary arteries (arrows) are proportionally smaller than those in a. The vessels appear to be slightly larger than the adjacent bronchi (arrowheads). The ratio of basal segmental arterial diameter to bronchial diameter was 1.2, which was the average ratio in the patients with normoxemic cirrhosis in the present study.
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Figure 3b. Thin-section CT scans of the right lower lobe. (a) CT scan obtained in a 68-year-old woman with hepatopulmonary syndrome. The right basal segmental pulmonary arteries are dilated. The ratio of the diameter of the segmental arteries (arrows) to the diameter of the accompanying bronchi (arrowheads) is increased compared with that in a 64-year-old man with normoxemic liver cirrhosis, whose CT scan is shown in b. Minimal pulmonary edema is likely to result in a slight increase in apparent arterial diameter. Even considering some peribronchial cuffing, the size of the arteries is clearly increased relative to that of the adjacent bronchi. (b) CT scan obtained in a 64-year-old man with normoxemic liver cirrhosis. The peripheral pulmonary arteries (arrows) are proportionally smaller than those in a. The vessels appear to be slightly larger than the adjacent bronchi (arrowheads). The ratio of basal segmental arterial diameter to bronchial diameter was 1.2, which was the average ratio in the patients with normoxemic cirrhosis in the present study.
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TABLE 3. Diameters of the Basal Segmental Artery and Adjacent Bronchus, and Their Ratio, in Four Patients with Hepatopulmonary Syndrome, and Four Patients with Normoxemic Cirrhosis at Thin-Section CT
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The pulmonary angiogram obtained in one patient with hepatopulmonary syndrome showed peripheral vessel dilatation and tortuosity (Fig 4).
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Figure 4. Pulmonary angiogram obtained in a 68-year-old woman with hepatopulmonary syndrome shows dilated and tortuous peripheral pulmonary arteries (arrows) but no evidence of arteriovenous shunting.
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DISCUSSION
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Hepatopulmonary syndrome represents a combination of liver dysfunction, intrapulmonary vascular dilatation, and hypoxemia (1–6). The radiologic manifestations of this disease have been recently reviewed by McAdams et al (7). CT findings of hepatopulmonary syndrome include distal vascular dilatation associated with an abnormally large number of visible terminal vessel branches, which are always concentrated in the lower lung zones. Although the pathogenesis of vascular dilatation is unknown, some investigators (10–12) have suggested that nitric oxide associated with portal hypertension might influence the autoregulation of the peripheral pulmonary vasculature, with the result being vasodilatation. Some have reported that in patients with liver cirrhosis and portal hypertension, increased nitric oxide in exhaled gas induced the decrease in pulmonary vascular tone, which accounted for increased pulmonary blood flow (12). Arterial hypoxemia in patients with hepatopulmonary syndrome is thought to occur because of ventilation-perfusion mismatch, limitations in oxygen diffusion due to vascular dilatation (ie, diffusion-perfusion impairment), and, in some patients, intrapulmonary shunt through dilated vascular malformations (10,12,13).
In the present study, the peripheral pulmonary vessels in the patients with hypoxemic liver cirrhosis were significantly dilated compared with these vessels in the healthy subjects and patients with cirrhosis who were not hypoxemic. The diameters of the central pulmonary trunk and right pulmonary artery in the patients with hepatopulmonary syndrome were slightly larger, on average, than were those in the healthy subjects and patients with normoxemic cirrhosis, but the differences were not significant (P > .05), and the left pulmonary artery did not show similar enlargement. Furthermore, the diameter of the main pulmonary artery did not correlate with the partial pressure of arterial oxygen.
Kuriyama et al (9) reported the mean diameters of the pulmonary trunk and right and left main pulmonary arteries to be 24.2 mm ± 2.2, 15.3 mm ± 2.9, and 13.0 mm ± 2.0, respectively, in healthy subjects and that the diameter of pulmonary arteries increased with age. In our study, the mean diameters of the pulmonary trunk and right and left pulmonary arteries in the healthy subjects were 28.3 mm ± 2.2, 16.2 mm ± 2.0, and 17.3 mm ± 3.6 mm, respectively, which are slightly larger than the diameters reported by Kuriyama et al and in a study performed by O'Callaghan et al (14). This may relate to the fact that the patients in our study were older than those examined in these two studies.
On thin-section CT scans, the diameter of an artery and its neighboring bronchus should be approximately equal, although vessels may appear slightly larger than their accompanying bronchi, particularly in dependent lung regions (15). In the present study, the ratio of segmental arterial diameter to bronchial diameter in patients with normoxemic cirrhosis was 1.2 ± 0.2; however, in patients with hepatopulmonary syndrome, the ratio was 2.0 ± 0.2. It seems clear that hepatopulmonary syndrome is related to pulmonary vasodilatation.
Although our conclusions are somewhat limited because of the small numbers of patients with hepatopulmonary syndrome and with normoxemic cirrhosis who were examined by using thin-section CT, hepatopulmonary syndrome is relatively uncommon, with an occurrence rate of approximately 15% in patients with end-stage liver disease (12).
In conclusion, in patients with liver cirrhosis and hypoxemia, or hepatopulmonary syndrome, the peripheral pulmonary vasculature is significantly dilated compared with that in healthy subjects and in patients with normoxemic liver cirrhosis. Dilatation of the peripheral pulmonary vessels correlates significantly with the partial pressure of arterial oxygen but not with the total bilirubin level or serum albumin level. Detection of dilated segmental pulmonary vessels, dilated peripheral pulmonary vessels, or both, may also be helpful in the diagnosis of hepatopulmonary syndrome in patients with chronic liver disease.
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Footnotes
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Author contributions: Guarantor of integrity of entire study, K.N.L.; study concepts and design, K.N.L.; definition of intellectual content, K.N.L., W.W.S.; literature research, K.N.L., W.W.S.; clinical studies, W.W.S., K.N.L., H.J.L.; experimental studies, K.N.L., H.J.L.; data acquisition, K.N.L., H.J.L.; data analysis, K.N.L., W.R.W.; statistical analysis, H.J.L.; manuscript preparation, K.N.L.; manuscript editing, K.N.L., W.R.W.; manuscript review, W.R.W.
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Abstract
Introduction
