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1
Department of Radiology, Kobe University Graduate School of Medicine, 7-5-2
Kusunoki-cho, Chuo-ku, Kobe 650-0017, Japan.
2
Department of Radiology, Pulmonary Functional Imaging Research, University of
Pennsylvania Medical Center, 3600 Market St., Ste. 370, Philadelphia, PA
19104-2649.
3
Philips Medical Systems Corporation, Philips Bldg. 2-13-37, Kohnan, Minato-ku,
Tokyo 108-8507, Japan.
Received September 27, 2000;
accepted after revision January 3, 2001.
Address correspondence to Y. Ohno.
Abstract
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SUBJECTS AND METHODS. Seven healthy volunteers, 10 lung cancer patients, and eight lung cancer patients with pulmonary emphysema were studied. A respiratory synchronized inversion-recovery single-shot turbo-spin-echo sequence (TE, 16; inversion time, 720 msec; interecho spacing, 4 msec) was used for data acquisition. The following paradigm of oxygen inhalation was used: 21% oxygen (room air), 100% oxygen, 21% oxygen. MR imaging data including maximum mean relative enhancement ratio and mean slope of relative enhancement were correlated with forced expiratory volume in 1 sec, diffusing lung capacity, high-resolution CT emphysema score, and mean distribution ratio of 81mKr ventilation scintigraphy.
RESULTS. Oxygen-enhanced MR ventilation images were obtained in all subjects. Maximum mean relative enhancement ratio and mean slope of relative enhancement of lung cancer patients were significantly decreased compared with those of the healthy volunteers (p < 0.0001, p < 0.0001). The mean slope of relative enhancement in lung cancer patients with pulmonary emphysema was significantly lower than that of lung cancer patients without pulmonary emphysema (p < 0.0001). Maximum mean relative enhancement ratio (r2 = 0.81) was excellently correlated with diffusing lung capacity. Mean slope of relative enhancement (r2 = 0.74) was strongly correlated with forced expiratory volume in 1 sec. Maximum mean relative enhancement had good correlation with the high-resolution CT emphysema score (r2 = 0.38). The maximum mean relative enhancement had a strong correlation with the distribution ratio (r2 = 0.77).
CONCLUSION. Oxygen-enhanced MR ventilation imaging in human subjects showed regional changes in ventilation, thus reflecting regional lung function.
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Currently, the standard lung function tests, including spirometry, plethysmography, and carbon monoxide—diffusing capacity, are performed to determine whole-lung function before and after therapy. The only means for imaging regional lung ventilation is through a nuclear medicine study with krypton-81m, xenon-133, or a radiolabeled aerosol and 99mTc-labeled diethylentriaminepentaacetic acid. The use of nuclear medicine in pulmonary functional imaging for lung cancer patients has been well documented, but the need to inhale a radioactive substance and poor spatial resolution remain major limitations of this method [3,4,5].
The use of oxygen as a paramagnetic contrast agent was first explored by Young et al. [6]. The paramagnetic effect of molecular oxygen promotes longitudinal relaxation of protons nearby, mostly protons in water molecules in the tissue [6,7,8,9,10]. Recently, several investigators have reported that oxygen-enhanced MR ventilation imaging could show regional ventilation [11,12,13,14,15]. Unlike standard lung function tests that determine global pulmonary ventilation, this new MR imaging method may provide information about the regional delivery of oxygen. Although oxygen-enhanced MR ventilation imaging has been described in the physiologic assessment in healthy volunteers and in pathophysiology in animal models of pulmonary embolism and airway obstruction, to our knowledge, there are few reports on the application of this technique in patients with pulmonary diseases [11,12,13,14].
We have successfully applied oxygen-enhanced MR ventilation imaging in patients with lung cancer with or without pulmonary emphysema. These patients with lung cancer underwent extensive preoperative pulmonary function tests, such as spirometry, plethysmography, diffusing capacity of the lung for carbon monoxide, and 81mKr nuclear medicine ventilation scan and imaging studies, including chest radiography and CT. Patients with pulmonary emphysema had various degrees of obstructive pulmonary-function abnormality indicated by forced expiratory volume in 1-sec values (percentage predicted). Lung cancer patients without definite pulmonary emphysema may have subclinical changes of emphysema without apparent forced expiratory volume in 1-sec values (percentage predicted) abnormality. Therefore, our patient population provided a spectrum of obstructive pulmonary-function abnormality. In addition, there have been reports that oxygen-enhanced MR ventilation imaging may reveal delivery of oxygen from air space to pulmonary capillary beds (i.e., diffusion) [12]. We correlated oxygen-enhanced MR imaging data with diffusing capacity of the lung for carbon monoxide in these patients and found a surprisingly strong correlation between the degree of oxygen-enhancement and diffusion capacity. The purpose of this article is to describe the preliminary results of the application of oxygen-enhanced MR ventilation imaging in a clinical setting with detailed correlation to standard pulmonary function tests, high-resolution CT, and nuclear medicine ventilation studies.
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The institutional review board approved this study, and informed consent was obtained from each subject before entering the study. Although all patients diagnosed with associated pulmonary emphysema had high-resolution CT emphysema scores greater than or equal to 2, half of the patients without pulmonary emphysema had scores of 1. These results reflect the existence of subclinical emphysematous changes in the lung tumors "without pulmonary emphysema" cohort.
The diagnosis of lung cancer was based on cytologic and histologic findings of transbronchial and CT-guided biopsy. Six of 18 patients were diagnosed with squamous cell carcinoma; nine patients, with adenocarcinoma; two patients, with large cell carcinoma; and one patient, with small cell carcinoma.
The diagnosis of pulmonary emphysema was based on physiologic findings, a history of long-term cigarette smoking ranging from 450 to 2300 on the Brinkman index (cigarette consumption per day x years), pulmonary functional tests, high-resolution chest CT according to American Thoracic Society criteria [16], or nuclear medicine ventilation-perfusion scans. All subjects underwent pulmonary function tests and high-resolution CT. Ten of 18 patients underwent 81mKr scintigraphy.
CT
All examinations were performed with a single-detector helical CT (HiSpeed
Advantage scanner; General Electric Medical Systems, Milwaukee, WI) and a
spiral single-detector volumetric helical CT (Somatom Plus 4 VB50; Siemens
Medical Systems, Forchheim, Germany). The scans were from the area of the lung
apex to the diaphragm (collimation, 2-3 mm; interval, 2-3 mm; table speed, 2-6
mm [pitch 1-2]; field of view, 300-350; matrix, 512 x 512; 120 kVp, 150
mA), and they were reconstructed with a high-spatial-frequency algorithm. The
scans were viewed at window levels appropriate for pulmonary parenchyma
(window width, 1600 H; window center, -600 H) for evaluation of pulmonary
emphysema. The severity of emphysema of lung cancer patients was judged by a
visual scoring method. First, high-resolution CT scans were scored according
to National Emphysema Treatment Trial scores for six regions: upper, middle,
and lower lung areas for each lung. The scores in each region of the lung
reflect the percentage area with emphysema: 0, normal; 1, less than 25%; 2,
26-50%; 3, 51-75%; 4, greater than 75%. Then, an overall score for emphysema
(high-resolution CT emphysema score) was also given for both lungs. In this
study, the final overall scores were used for correlation with MR imaging
data. Each subject was examined independently by two chest radiologists
without the benefit of clinical information or of the results of pulmonary
function tests. Final interpretation of each subject was based on a consensus
of the two reviewers.
Oxygen-Enhanced MR Imaging Technique
Oxygen-enhanced MR ventilation images were acquired with inhaled oxygen as
a contrast agent on T1-weighted imaging. T1-weighted images were obtained with
a respiratory synchronized inversion-recovery half-Fourier acquisition
single-shot turbospin-echo inversion recovery (HASTE) pulse sequence using
1.5-T whole-body scanner (Gyroscan ACS-NT PT6000; Philips Medical Systems,
Best, The Netherlands). For a 128 x 128 matrix, 68 phase-encoding steps
were obtained, including three steps for phase correction. The interecho
spacing was 4.0 msec. The effective TE was 16 msec, section thickness was 10
mm, field of view was 450 x 450 mm with an inversion time of 720 msec.
MR ventilation images from four coronal sections for each patient were
obtained for all studies.
Patients and healthy volunteers inhaled room air first, followed by 100% oxygen (15 L/min), using a nonrebreathing ventilation mask. The following paradigm for oxygen inhalation was used: subjects first breathed 21% oxygen (room air) for 80 sec; then breathed 100% oxygen for 140 sec; and then room air, for 80 sec. During data acquisition, all subjects resumed normal respiration, breathing room air.
Analysis of Oxygen-Enhanced MR Images
After image reconstruction, the data were transferred to a remote
workstation (Easy Vision; Philips Medical Systems). To visualize the relative
enhancement map of oxygen-enhanced MR ventilation imaging, oxygen-enhanced MR
ventilation images were expressed as a percentage change from the
oxygen-enhanced and room-air images. Each pixel in the percentage change map
was calculated as follows:
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The regional distribution of relative enhancement in each pixel was expressed as a color-coded map. Pixels with 0-50% enhancement were shown as color-coded shading from dark blue to red; pixels with more than 50% enhancement were red.
The signal intensity (SI) time course curve was calculated for each coronal section in six spatially defined regions of interest (ROIs) in the lung (three ROIs for each lung analyzed with standalone software [Quantitative Analysis, Philips]). Enhancement curves were automatically plotted, and the data were transferred to a Power Macintosh G3 (Apple Computer, Curpertino, CA).
To compare the slopes between healthy volunteers and patients, points in the SI—time course curve from the baseline to the maximal value of SI during the breathing of 100% oxygen were fitted by a straight line. Then, we created a mean relative enhancement ratio time-course curve, using the 100% oxygen data, and calculated the maximum mean relative enhancement ratio and mean slope value of oxygen concentration by using Excel 98 for Macintosh software (Microsoft, Redmond, WA).
To compare the difference in mean relative enhancement ratio time course curve between the healthy volunteers and patients, we calculated the time of maximum mean relative enhancement (peak time), the maximum mean relative enhancement ratio of lung parenchyma (mean of maximal relative enhancement ratio of lung parenchyma), and the mean slope of mean relative enhancement of lung parenchyma by oxygen concentration.
Maximum relative enhancement ratio was determined with the following
formula:
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Maximum mean relative enhancement ratio was calculated from the mean of relative enhancement ratio of 24 ROIs.
The mean slope of mean relative enhancement of lung parenchyma by oxygen
concentration (mean slope of relative enhancement) was determined with the
following equation:
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Physiological Index and Outcome Measures
Pulmonary function testing was performed according to American Thoracic
Society standards [16] with an
automatic spirometer (System 9; Minato Ikagaku, Osaka, Japan). Spirometry
values obtained after administration of aerosolized albuterol were used in all
patients. Lung volumes were determined with plethysmography, and the diffusing
capacity of the lung for carbon monoxide was measured with the
single-breathing technique. Arterial blood samples were obtained with patients
at rest breathing room air, and partial pressures of oxygen and carbon dioxide
were measured with a model G3 blood gas analyzer (Instrumentation Laboratory,
Lexington, MA).
All preoperative physiologic testing was performed at least 1 month before surgery (mean, 7 days ± 6).
81mKr Ventilation Scintigraphy Technique
Pulmonary ventilation scintigraphy was performed using krypton-81m
(81mKr) with the patient in a sitting position. Images were
obtained in the anterior and posterior views with a gamma camera (Shimazu
SNC500R; Shimazu, Kyoto, Japan) with a medium-energy collimator.
81mKr gas was inhaled through a mouthpiece with the patient's nose
clamped. After several normal tidal breaths, the patient was instructed to
exhale as much as possible to the level of residual volume. A deep slow
inspiration of 81mKr gas to the total lung capacity level was held
for approximately 10 sec, depending on the patient's breathing status.
A 185 MBq (5 mCi) 81mKr generator (rubidium-81) was used for 81mKr gas inhalation. An 18-gauge needle connected to a small tube from the generator was inserted into the mouthpiece, and the elution of 81mKr with oxygen was begun immediately before inhalation at the level of residual volume and was stopped at the end of inhalation at the level of total lung capacity. Total radioactivity in each lung was calculated, and the distribution ratios of radioactivity in the right and left lungs were determined. The right and left lungs were horizontally divided into three equal ROIs by equalizing the number of pixels including lung tumor. The distribution ratios of radioactivity in six ROIs (three in each lung) were calculated and averaged as mean distribution ratios of radioactivity of ventilation scintigraphy (mean distribution ratio).
Data Analysis
For the assessment of mean relative enhancement ratio time-course curves
between healthy volunteers and patients with lung disease, maximum mean
relative enhancement ratios and mean slopes of relative enhancement were
compared with Fisher's protected least significant difference test.
To determine the relationship between parameters of the mean relative enhancement ratio time-course curve and those of the standard lung function test, we correlated the mean slope of relative enhancement with the forced expiratory volume in 1 sec (percentage predicted) and the maximum mean relative enhancement ratio, with the diffusing capacity of the lung for carbon monoxide (percentage predicted).
High-resolution CT emphysema scores and mean distribution ratios of 81mKr ventilation scintigraphy of lung cancer patients were correlated with maximum mean relative enhancement ratios of oxygen-enhanced MR imaging.
Data entry procedures and statistical analyses were performed with the statistical software, Stat-View for Macintosh, version 5 (Abacus Concepts, Berkeley, CA), Microsoft Excel 98 for Macintosh, and a commercially available computer (Power Macintosh G3). A p value less than 0.05 was considered significant.
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The mean relative enhancement ratio time course curves from both lungs in each group of patients are shown in Figure 5. After switching to 100% oxygen, maximum mean relative enhancement ratios in lung cancer patients (without emphysema, 18.4 ± 1.3 %SI; with emphysema, 15.5 ± 3.3 %SI) were significantly decreased compared with those of healthy volunteers (31.8 ± 2.7 %SI) (p < 0.001). We found no significant difference between lung cancer patients with and without pulmonary emphysema (p = 0.23) (Table 1).
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The mean slopes of relative enhancement of lung cancer patients (without emphysema, 0.50 ± 0.02 %SI/sec (percentage increase of signal intensity per second); with emphysema, 0.28 ± 0.02 %SI/sec) were significantly less than those of healthy volunteers (0.69 ± 0.06 %SI/sec) (p < 0.001). The mean slope of mean relative enhancement of lung cancer patients with pulmonary emphysema was significantly decreased compared with that of lung cancer patients without emphysema (p < 0.001) (Table 2).
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The mean slope of relative enhancement was strongly correlated to the forced expiratory volume in 1 sec (percentage predicted) (r = 0.86, r2=0.74, p < 0.0001) (Fig. 6). The maximum mean relative enhancement ratio was excellently correlated to the diffusing capacity of the lung for carbon monoxide (percentage predicted) (r = 0.90, r2=0.81, p < 0.0001) (Fig. 7).
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Maximum mean relative enhancement ratio showed good correlation with high-resolution CT emphysema scores (r = 0.62, r2 = 0.38, p = 0.007) (Fig. 8). Maximum mean relative enhancement ratio showed strong correlation with the mean distribution ratio (r = 0.88, r2 = 0.77, p = 0.004) (Fig. 9).
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Parameters of oxygen-enhanced MR imaging of healthy volunteers were significantly higher than those of lung cancer patients with or without pulmonary emphysema. Additionally, in lung cancer patients, the mean slope of relative enhancement of lung cancer patients with pulmonary emphysema was significantly lower than that of lung cancer patients without pulmonary emphysema. Molecular oxygen is weakly paramagnetic with a magnetic moment of 2.8 Bohr magnetons. Oxygen modulates the MR imaging signal of blood and fluid through two different mechanisms: the paramagnetic property of deoxyhemoglobin and the paramagnetic property of molecular oxygen itself [6]. Because deoxyhemoglobin is compartmentalized in RBC, tissue water protons do not have access to coordination sites, which is required for spin-lattice interactions causing T1 shortening [6, 8]. Therefore, deoxyhemoglobin with RBC has a T2*-shortening effect with little T1-shortening effect [8, 17]. When oxygen is exchanged between air in the alveoli and blood in the capillary beds, oxygen not only couples to hemoglobin but also dissolves as molecular oxygen in the blood [8, 17]. Dissolved molecular oxygen will shorten the T1 relaxation time of pulmonary venous blood because molecular oxygen is paramagnetic. The areas of the lung affected by pulmonary emphysema were pathologically characterized as having a decrease in pulmonary capillary beds, abnormal permanent enlargement of the air spaces distal to the terminal bronchiole, accompanied by destruction of their walls, and without obvious fibrosis. Therefore, the areas of the lung affected by pulmonary emphysema showed marked decrease in oxygen enhancement due to the decrease in distribution of deoxyhemoglobin and the decrease in the direct diffusion of molecular oxygen to the capillary bed.
Moreover, the areas of the lung affected by lung cancer or atelectasis showed markedly decreased oxygen enhancement. Most oxygen is delivered to tissue by binding to hemoglobin molecules in RBC. The high concentration of oxygen in alveoli increases the oxygen concentration of lung parenchyma severalfold by means of direct diffusion of oxygen molecules [18]. However, there is only a small increase in oxygen delivery to other organs and tissues because the increase in dissolved oxygen in arterial blood serum is relatively small compared with oxygen contained in RBC bonded to hemoglobin molecules. Thus, only a small increase in oxygen concentration in other organs is expected unless the organs have a high arterial flow, such as in the spleen and in the kidneys [19]. Lung-tumor tissue does not receive direct diffusion of oxygen, so an increase in oxygen supply is limited. Therefore, the lack of oxygen enhancement in the tumor is explained.
The atelectatic lung has little ventilation. Therefore, there is little increase in oxygen concentration in atelectatic lung tissue when 100% oxygen is inhaled.
Lung tissue adjacent to the tumor also showed decreased enhancement. Obstruction of large and small airways by lung tumor may impair regional ventilation in areas adjacent to the tumor. The changes in volume in adjacent lung tissue may be decreased and may result in decreased regional ventilation. Moreover, it has been reported that obstruction and destruction of pulmonary vasculature by lung tumor may facilitate regional changes in pulmonary blood volume, ventilation-perfusion distribution, and decreased diffusing capacity of the lung for carbon monoxide (percentage predicted) [3, 4].
Observation of dynamic oxygen enhancement by MR imaging was also feasible. In patients with associated emphysema, the mean slope of relative enhancement was significantly decreased. The forced expiratory volume in 1 sec (percentage predicted) values correlated strongly with the mean slope of relative enhancement (r2 = 0.74). The delivery of oxygen was markedly delayed and impaired the forced expiratory volume in 1-sec (percentage predicted) decrease because destruction and decreased elasticity of lung parenchyma result in expiratory air-flow obstruction, air trapping, hyperinflation, and impaired respiratory mechanics. The narrowing of small airways may also contribute to the decrease in oxygen delivery.
There was excellent correlation between the maximum mean relative enhancement ratio and the diffusing capacity of the lung for carbon monoxide (percentage predicted) (r2 = 0.81). This result is particularly interesting because diffusing capacity of the lung for carbon monoxide reflects diffusion capacity. Alveolocapillary gas transfer is usually regarded as the definition of pulmonary diffusion capacity. The alveolocapillary membrane separating gas from blood in the lung constitutes a diffusive barrier for oxygen uptake in the lung and likewise for carbon dioxide excretion or exchange of any gas. The existence of specific carrier mechanisms for oxygen and carbon monoxide that would facilitate their transfer across the tissue barrier has not been confirmed. Therefore, the diffusion capacity of oxygen is replaced by the diffusing capacity of the lung for carbon monoxide because of the similar molecular sizes of molecular oxygen and carbon monoxide. The transfer of gas through the membrane is determined according to the law of diffusion. In patients with pulmonary emphysema, the thickness of the barrier remains unchanged unless there is an associated infection, inflammation, fibrosis, or scar from previous infections. Therefore, diffusing capacity in patients with emphysema is proportional to the remaining surface area for gas exchange [18]. On the other hand, the maximum mean relative enhancement ratio should be proportional to the surface area for gas exchange because oxygen enhancement of lung parenchyma is the result of the transfer of oxygen to lung tissue by direct diffusion of molecular oxygen. The fact that there was excellent correlation between maximum mean relative enhancement measured by oxygen-enhanced MR ventilation imaging and diffusing capacity of lung for carbon monoxide supports this hypothesis.
Correlation of oxygen-enhanced MR ventilation imaging and high-resolution CT resulted in good correlation between the maximum mean relative enhancement ratio and high-resolution CT emphysema score (r2 = 0.38). Oxygen-enhanced MR ventilation imaging shows the degree of enhancement by inhaled molecular oxygen, whereas high-resolution CT scores reflect the macroscopically destructed lung. These two phenomena may be different. Moreover, the high-resolution CT emphysema scoring system uses a 5-scale ranking and is only semi-quantitative.
The results of our study revealed that the degree of oxygen-enhancement was reflected by the forced expiratory volume in 1 sec and the diffusing capacity of the lung. 81mKr ventilation scintigraphy was reported to have strong correlation with the forced expiratory volume in 1 sec [20]. Therefore, it is not surprising that oxygen-enhanced MR ventilation imaging data had a strong correlation with the mean distribution ratios of 81mKr ventilation scintigraphy.
Recently developed hyperpolarized noble gas MR imaging with helium-3 and xenon-129 is a superb new method for pulmonary function imaging [21,22,23,24,25,26,27,28,29]. This technique visualizes gas itself, thus demonstrating airway and air spaces. This method is particularly powerful when used for underlying physiology, such as regional mapping of helium-3 gas diffusion or regional oxygen concentration measurement [26,27,28,29].
The only drawback of hyperpolarized noble gas techniques is the necessity for laser equipment and specialized radiofrequency transmitter—receiver coils.
In contrast, oxygen is safe and widely available. The usual clinical proton MR scanner can be used. Whereas the underlying physiology for oxygen-enhanced MR ventilation imaging is different from that for hyperpolarized noble gas, we understand that functional information derived from hyperpolarized noble gas imaging and oxygen-enhanced MR ventilation imaging is different and possibly complementary.
This study had several limitations. First, the administration of oxygen in patients with pulmonary diseases may alter or modify existing pulmonary pathophysiology. For example, increased oxygenation in the airway may reverse existing hypoxic vasoconstriction [30]. Thus, oxygen-enhanced MR ventilation imaging could show falsely increased oxygen delivery in a previously hypoxic segment or lobe.
Second, other investigators have suggested that prolonged hyperoxia due in 100% oxygen inhalation can cause diffuse alveolar damage and lung fibrosis [31,32,33,34]. However, this effect is unlikely because diffuse alveolar damage is reported to occur after exposure to a high concentration of oxygen, usually for periods from 24 to 120 hours [34]. In our study, exposure to high-concentration oxygen was less than 10 min per study.
Third, the numbers of patients who underwent high-resolution CT (n = 18) and 81mKr ventilation scintigraphy (n = 10) were relatively small. Furthermore, oxygen-enhanced MR ventilation imaging provides tomographic images, and 81mKr ventilation scintigraphy provides only a projection image. Thus, accurate spatial correlation is difficult and impractical. Therefore, further study for comparing ventilation scintigraphy with single-photon emission CT and high-resolution CT of primary pulmonary emphysema without lung cancer is warranted.
In conclusion, oxygen-enhanced MR ventilation imaging was applicable in patients with lung cancer and pulmonary emphysema. Detailed correlation between oxygen-enhanced MR ventilation data and pulmonary function test data, including forced expiratory volume in 1 sec and diffusing capacity of the lung for carbon monoxide, revealed the oxygen-enhancement ratio may reflect the amount of surface area of gas exchange, thus correlating with the diffusing capacity of the lung for carbon monoxide value. Therefore, oxygen-enhanced MR ventilation imaging may be useful in evaluation of interstitial lung diseases, pulmonary edema, and adult respiratory distress syndrome, in which the increased alveolocapillary barrier for molecular oxygen transport plays a major role in pathophysiology. Oxygen-enhanced MR ventilation imaging provides a new method for clinical functional lung imaging.
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ler CJ, Peller M, et al. Optimization and
evaluation of the signal intensity change in multisection oxygen-enhanced MR
lung imaging. Magn Reson Med
2000;43:860
-866[Medline]
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| HOME | HELP | FEEDBACK | SUBSCRIPTIONS | ARCHIVE | SEARCH | TABLE OF CONTENTS |
), in lung cancer patients without pulmonary
emphysema (
), and in lung cancer patients with pulmonary emphysema
([UNK]). Maximum mean relative enhancement ratios in lung cancer patients
(without emphysema, 18.4 ± 1.3 %SI [percentage increase of signal
intensity]; with emphysema, 15.5 ± 3.3 %SI) are significantly less than
those of healthy volunteers (31.8 ± 2.7 %SI) (p < 0.001).
Mean slopes of relative enhancement of lung cancer patients (without
emphysema, 0.50 ± 0.02 %SI/sec; with emphysema, 0.05 ± 0.02
%SI/sec) are significantly less than those of healthy volunteers (0.69
± 0.06 %SI/sec) (p < 0.001). Mean slope of relative
enhancement of lung cancer patients with pulmonary emphysema is significantly
less than that of lung cancer patients without emphysema (p <
0.001).
