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Comparison of spirometry and abdominal height as four-dimensional computed tomography metrics in lung

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computed tomography metrics in lung

Wei Lu, Daniel A. Low,a兲 Parag J. Parikh, Michelle M. Nystrom, Issam M. El Naqa, Sasha H. Wahab, Maureen Handoko, David Fooshee, and Jeffrey D. Bradley

Department of Radiation Oncology, Washington University School of Medicine, St. Louis, Missouri 63110

共Received 22 October 2004; revised 14 February 2005; accepted for publication 26 April 2005;

published 23 June 2005兲

An important consideration in four-dimensional CT scanning is the selection of a breathing metric for sorting the CT data and modeling internal motion. This study compared two noninvasive breathing metrics, spirometry and abdominal height, against internal air content, used as a surrogate for internal motion. Both metrics were shown to be accurate, but the spirometry showed a stronger and more reproducible relationship than the abdominal height in the lung. The abdominal height was known to be affected by sensor placement and patient positioning while the spirometer exhib-ited signal drift. By combining these two, a normalization of the drift-free metric to tidal volume

may be generated and the overall metric precision may be improved. © 2005 American

Associa-tion of Physicists in Medicine.关DOI: 10.1118/1.1935776兴

Key words: breathing motion, spirometry, abdominal height, radiation therapy

I. INTRODUCTION

Internal respiratory organ motion is the principal reason that

intensity modulated radiation therapy 共IMRT兲 has not been

widely accepted for use in lung and upper-abdomen cancer

treatment.1–4 Four-dimensional computed tomography 共4D

CT兲is one technique proposed to reduce this uncertainty by retrospectively constructing three-dimensional 共3D兲 CT im-ages at various parts of the respiratory cycle.5–11Our group has developed a 4D CT technique for free breathing by using a 16-slice CT scanner.8,12

For both 4D CT5–12and gated radiotherapy,13–18a metric that monitors breathing motion must be used since time cannot be directly correlated to tumor motion. Various breathing metrics have been proposed, ranging from implanted marker position,2,5,18–21abdominal height or chest height,6,7,9,10,15,18,22,23 spirometry,8,12,13,16,22–26 abdominal strain gauge,13wraparound inductive plethysmography,22and temperature sensors.13The only commercially available

sys-tem uses abdominal height 共Real-Time Position

Manage-ment, RPM, Varian Medical Systems, Palo Alto, CA兲, but the relationship between internal motion and abdominal height is sensitive to sensor placement and patient positioning.15,16,27 A spirometer measures the air flow into the lungs and may provide a useful, verifiable physiologic metric.12,16We have found that spirometry is an excellent quantitative metric, but its significant signal drift means that it may not be appropri-ate as the sole metric for 4D CT or gappropri-ated radiotherapy.12,26 This study compared spirometer-measured tidal volume and abdominal height against internal air content, a surrogate for

internal motion measurements.12 The relationship between

these two metrics for an entire CT scan session was also examined.

II. MATERIALS AND METHODS A. 4D CT with spirometry

Brief descriptions of the 4D CT process8and internal air content analysis12,28 are given as follows. Transverse slices

共1.5 mm thick兲 were acquired using a 16-slice CT scanner

共Sensation 16, Siemens Medical Systems, Malvern, PA兲

op-erated in 12-slice mode. The scanner was opop-erated in ciné

mode 共couch stationary during scanning兲 with 15 scans

ac-quired repeatedly at each couch position for 11 s. Each scan 共360° rotation兲required 0.5 s to acquire followed by a 0.25 s dead time. The data were acquired continuously in space, but there was usually a pause of 4 s between two neighboring couch acquisitions. This process was conducted while the patient underwent synchronized spirometry measurements. The synchronization was provided by a photoresistor con-nected to the “X-Ray On” light.12Both the spirometry signal and the photoresister signal were measured with approxi-mately 100 samples per second using a customized data ac-quisition program written inLABVIEW共National Instruments, Dallas, TX兲.8,28 The spirometry was calibrated to be linear and accurate for tidal volume flow rates greater than

100 ml/ s 共typical breathing flow rates are in excess of

200 ml/ s兲.28The slow drift in the spirometry signal was cor-rected by retrospectively examining the spirometer-measured tidal volume 共v兲 and the internal air content 共V兲for the 15

CT scans.12 This provided a spirometer-measured tidal

vol-ume 共v兲 for each CT scan. The CT scans were then sorted

into variable number of bins共usually 10–14 bins, depending on the range of tidal volumes the patient breathed兲. Each bin was assigned a specific tidal volume and direction of respi-ration共inspiration or expiration兲.

B. Internal air content analysis

The internal air content analysis provided a measure of

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determined by the Hounsfield values in segmented air-containing tissues共lungs, trachea, bronchi兲.12,28In a previous study, we showed that the internal air content correlated with tissue motion with a residual of less than 1 mm for 12 pa-tients and provided quantitative evaluations for the 4D CT process.12In this study, the internal air content was used as a surrogate for internal motion and the basis for metric com-parison.

C. Abdominal surface height measurement

During the 4D CT procedure, an abdominal surface height

measurement共h兲was simultaneously acquired through

digi-tal video recording of a lightweight block placed on the pa-tient’s abdomen 关Fig. 1共a兲兴. The block was positioned be-tween the umbilicus and the xiphoid process, based on the position of greatest tidal excursion as determined by a phy-sician present at the simulation. We took care to tape the block tightly and straight up so that the motion was mostly in the anterior-posterior direction with negligible rotation ef-fect. A distance scale was attached to the block surface

fac-ing the camera 共DCR-TRV 240, Sony, Tokyo, Japan兲 for

measurement calibration. A dark dot was marked at the cen-ter of the distance scale. It provided a template for automati-cally tracking of the block position on the digital movie frames 关Fig. 1共b兲兴. The video was synchronized to the CT scanner acquisition by a fiber optic cable connected to the same “X-Ray On” light as used for spirometry synchroniza-tion. Figure 1共b兲shows that the end of the fiber optic cable

appears bright in the sample frame when the CT radiation is on. The video was downloaded from the camera and cropped to reduce the video file size with commercial video

process-ing software共PREMIEREV6.5, Adobe Systems Incorporated,

San Jose, CA兲. The video had a sampling rate of

30 frames/ s. The position of the block within each frame was automatically tracked using a two-dimensional template

matching algorithm30 implemented in MATLAB 共The

Math-works, Inc., Natick, MA兲. The template matching algorithm

determines the position of a template in a target frame by finding the maximum normalized correlation between the template and the target. A rectangular region around the cen-ter dark dot in the first frame was manually selected as the template. The size of the template was approximately 2 by 2 mm. The template position determined by the algorithm was superimposed on each frame of the video 关Fig. 1共b兲兴. This generated a new video which was retrospectively viewed and from which the uncertainty of the template tracking was es-timated for every patient to be less than 0.3 mm in both the lateral and anteroposterior directions. The anteroposterior position of the template provided the abdominal height mea-surement, which was calibrated from pixels into distance in millimeters using the imaged distance scale. This inexpen-sive in-house system provided similar surface height mea-surements to those provided by the RPM system with the advantage that it provided synchronization signals with the CT scanner.

D. Comparison of spirometry and abdominal height as 4D CT metrics

The spirometer-measured tidal volume and the abdominal height were compared against internal air content共V兲as 4D CT metrics at each couch position 共11 s兲. A patient-specific

time offset⌬twas assumed to exist between diaphragm

mo-tion 共causing abdominal motion兲, internal lung motion, and

airflow at the mouth. The value of ⌬t between each metric

and V was determined by maximizing a cross-correlation

function共CCF兲between each metric andV. The CCF

evalu-ates the degree to which two functions are correlated and allows for the identification and estimation of⌬tin two re-lated signals.12,18,31–33On the other hand, a specific fractional

error in V would correspond to the same fractional error in

internal motion estimation, the fitting residual␴V共root mean squared error兲of a first-order fit between each metric andV

was used as a measure of the metric precision. Three 4D CT lung cancer patients and two 4D CT abdomen study patients had both spirometry and abdominal height data and were used in this study. Only couch positions that intercepted the lungs were used in this comparison.

E. Comparison of spirometry and abdominal height for entire scan session

The abdominal height measurement 共h兲 was considered

drift-free22,26 and its relationship with the

spirometer-measured tidal volume 共v兲 was examined for the entire CT

session共300–600 s兲. This was done by dividing the CT

ses-sion into 11 s segments 共based on the amount of time

re-FIG. 1. Measuring abdominal height.共a兲Video acquisition system consist-ing of a digital camera pointed at the distance scale movconsist-ing with the abdo-men.共b兲A sample frame taken from a video shows the template position determined by the template matching algorithm. The fiber optic cable ap-pears bright in this sample frame indicating that the CT radiation is on.

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quired to acquire 15 CT scans from a single couch position兲

and correlatinghtovin every segment. When examining the

relationship of these two metrics in each segment, ⌬t

be-tween h and v and a baseline drift in tidal volume were

observed. We adopted an approach to simultaneously

deter-mine⌬tand spirometry drift by maximizing the correlation

betweenhandvfor each segment:共1兲⌬twas determined by shifting vin time to maximize its correlation with h; 共2兲 a

linear spirometer drift correction was applied to v and the

slope of the drift was adjusted to again maximize the

corre-lation between v and h. The mean ratio of drift-corrected

tidal volume change to the abdominal height change 共dv/dh兲, and the mean time offset共⌬th-v兲were tabulated. III. RESULTS

A. Comparison of spirometry and abdominal height as 4D CT metrics

Figure 2共a兲shows the spirometer-measured tidal volume, abdominal height, and internal air content at the times corre-sponding to the 15 successive CT scans for one couch posi-tion. Figure 2共b兲shows the continuous tidal volume and ab-dominal height for the same couch position共11 s兲as shown in Fig. 2共a兲. The abdominal height changed by about 10 mm for the three breaths shown, while the tidal volume changed by about 500 ml. Because of unintended abdomen motion caused by involuntary abdomen muscle motion and cardiac motion, the abdominal trace has more small vibrations than the tidal volume trace. Similar vibrations were noticeable in

surface displacement traces 共abdominal or chest兲 measured

by others.3,34,35

Figure 3 shows the results of linearly fitting each metric to the internal air content for this couch position. The fitting residual was 2.8 ml for tidal volume 关Fig. 3共a兲兴and 4.3 ml for abdominal height关Fig. 3共b兲兴, suggesting a greater preci-sion of the tidal volume. The slopes of the fitted lines共dV/dv

anddV/dh兲represent the ratio of internal air content change to metric change. Figure 4 shows summary plots of these measurements as a function of couch positions for this lung

cancer patient 共couch positions 5–18 are intercepting the

lungs兲. The slopes were normalized to a common range of

0–1 for comparison. The two metrics display the same trend in the slopes关Fig. 4共a兲兴. This indicates that both metrics have equivalent accuracy in determining changes in internal air content. For most couch positions within the lung, spirom-etry showed a better precision共smaller fitting residual兲 than abdominal height 关Fig. 4共b兲兴. This was true for all five pa-tients.

The mean time offset, fitting residual, and correlation be-tween each metric and the internal air content are listed in Table I. We have shown that the mean fitting residuals be-tween v and V 共␴v-V兲 for the lung cancer patients corre-sponded to 3%–8% uncertainties in the overall tidal

volumes.12 For all patients, the spirometer-measured tidal

volume had a better mean precision than the abdominal height. The correlation between the tidal volume and internal air content was slightly greater than or equal to that between the abdominal height and internal air content. With regard to

t, for all patients but patient 3, the abdominal height change led the internal air content change. Patient 3 showed a dif-ferent phase relationship: the internal air content change led the abdominal height change. This was possibly due to the patient’s breathing being driven more by the chest than for the other four patients. Further investigation showed that this patient also had the smallest peak-to-peak change in abdomi-nal height 共6 mm兲. The internal air content change led the spirometry change for all patients. The time offset between the spirometry and internal air content was smaller than that between the abdominal height and internal air content for every patient.

B. Relationship between spirometry and abdominal height for entire scan session

Figure 5 shows the relationship between the abdominal height and tidal volume for an entire scan session共⬃350 s兲. FIG. 2. Breathing samples of spirometer-measured tidal volume, abdominal height, and internal air content vs scan index共a兲and vs time共b兲for a couch position in the middle of lung and intercepting the diaphragm.

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The values of dv/dh were relatively unchanged during the session with a mean of 62.61 ml/ mm and a standard devia-tion共s.d.兲of 3.11 ml/ mm关Fig. 5共a兲兴. The residual共␴h-v兲for

a first-order fit between vandh was relatively small with a

mean of 19 ml or 3.25% of the overall tidal volume 关Fig.

5共b兲兴. The correlation between h and vrh-v兲 was high

throughout the session 关Fig. 5共c兲兴. The time offset 共⌬th-v兲

plot shows that the abdominal height change always led the spirometry change with a mean of 0.12 s and a s.d. of 0.02 s 关Fig. 5共d兲兴. These measurements were tabulated for all five patients共Table II兲. The first three lung cancer patients show less variation indv/dhthan the last two abdomen study pa-tients, which might be the result of longer overall scan

ses-sion times for abdomen study patients 共⬃600 s兲. The time

offsets were relatively unchanged for every patient 共s.d. 艋0.02 s兲 except for patient 4 共s.d. = 0.05 s兲, for whom the time offset increased significantly near the end of the session possibly due to patient relaxation.

IV. DISCUSSION AND CONCLUSION

The results showed that both metrics were accurate with respect to internal air content. The metric precision varied with the location of interest but spirometry was generally a better metric than the abdominal height for a location within the lung. The mean precision of spirometry within the lung

was better for all patients, suggesting a stronger and more reproducible relationship of spirometry with internal air con-tent and tissue motion. The time offset between the internal air content and the spirometry was smaller than that between the internal air content and the abdominal height. A recent fluoroscopic study by Hoisaket al.reached the same conclu-sions for 11 patients with data acquired over extended peri-ods and over multiple days.23

It has been reported that breathing patterns change when one breathes through a spirometer.36,37 Gilbert et al.36 re-ported that the tidal volume increased by 29± 21% for 14 subjects in one study, while Askanaziet al.37found increases of 15.5% for 28 subjects. However, when evaluating metrics for 4D CT or gated radiation therapy, it is the relationship between internal motions and the breathing metrics that are the principal consideration. The fact that the tidal volume changes when a spirometer is employed does not necessarily change the relationship between tidal volume and internal motion. This relationship will need verification, but if the use of spirometry significantly affects this relationship, a spirom-eter can be employed during treatment.

Though the internal air content functioned well as a sur-rogate for tissue motion, and the internal air content change FIG. 3. Linearly fitting spirometer-measured tidal volume共a兲and abdominal

height共b兲to internal air content. Dashed lines represent ± fitting residuals. Finternal air content to tidal volumeIG. 4. Summary plots for a lung cancer patient.dV/dv and to abdominal height共a兲Normalized ratios of

dV/dh兲.共b兲Fitting residuals between tidal volume and internal air content

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can be monitored either locally or globally in the lung, actual tumor motion would be better for evaluating breathing met-ric in radiotherapy. Reliably tracking tumor motion in 3D is

ongoing research. Fluoroscopically tracking implanted

markers2,3,5,18–21may yield the most reliable 3D tumor posi-tion, however, this technique is invasive and has other

limitations.19,21 A recent study showed that tumors in the

lung can be tracked with a biplane digital radiography unit, while implanted markers were still needed for tumors in the

liver and esophagus.18 Fluoroscopically tracking the

superior-inferior diaphragm motion has been conducted but is limited by the fact that only one-dimensional diaphragm

motion was measured.15,17,34,35 The development of

respiration-correlated 4D CT techniques may provide a non-invasive way for tracking and modeling 3D tumor/tissue mo-tion.

For the five patients in this study, there was a high corre-lation between the spirometry and abdominal height 共⬎0.98兲, and their relationship共dv/dh and time offset兲was relatively unchanged for the entire CT session 共300–700 s兲 under free breathing. Zhang et al.26 reported a stable corre-lation between spirometry and chest wall height for healthy volunteers during normal breathing cycles. Because of the large variation exhibited in breathing patterns, it is important to establish and verify thedv/dhrelationship for each scan-ning session and each treatment session. We have so far as-sumed that this relationship would change only slightly dur-ing each treatment session共10–15 min兲, in which the patient is kept at a fixed position and undergoes quiet respiration. Our results, acquired during CT simulation, have shown that TABLEI. Comparison of tidal volume共v兲and abdominal height共h兲against internal air content共V兲as 4D CT

metrics within the lung.

Patient Site

BetweenvandV BetweenhandV

Time offseta Fitting residual Time offseta Fitting residual 共s兲 共ml兲 Correlation 共s兲 共ml兲 Correlation 1 Lung −0.02 1.99 0.99 0.07 2.44 0.98 2 Lung −0.03 2.78 0.98 0.07 3.38 0.96 3 Lung −0.03 2.35 0.99 −0.15 4.25 0.97 4 Abdomen −0.04 4.42 0.99 0.14 4.65 0.99 5 Abdomen −0.06 1.28 1.00 0.11 2.36 0.99

aA positive time offset indicates that the first variable is leading the second variable.

FIG. 5. Relationship between abdominal height共h兲and tidal volume共v兲for the entire scan session.共a兲Ratio of change invto change inhdv/dh兲.共b兲 Fitting residual between h and v共␴h-v兲. 共c兲 Correlation between h and

vrh-v兲.共d兲Time offset betweenhandv共⌬th-v兲.

TABLE II. Relationship between the tidal volume 共v兲 and abdomen height共h兲for the entire scan session

共300–600 s兲. Values are mean共s.d.兲for all 11 s segments. Patient Site Time offseta 共s兲 dv/dh 共ml/ mm兲 Fitting residual共%兲 Correlation 1 Lung 0.12共0.02兲 62.61共3.11兲 3.25共1.04兲 0.993共0.004兲 2 Lung 0.06共0.01兲 61.97共2.19兲 3.05共0.47兲 0.994共0.002兲 3 Lung −0.12共0.02兲 108.20共6.39兲 5.92共0.91兲 0.980共0.004兲 4 Abdomen 0.11共0.05兲 66.60共6.53兲 3.15共1.99兲 0.996共0.004兲 5 Abdomen 0.12共0.02兲 73.91共9.62兲 5.50共1.74兲 0.983共0.012兲 aA positive time offset indicates that the first variable is leading the second variable.

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this assumption is valid for 6–11 min. If this assumption holds, we hypothesize that it will be possible to acquire both metrics for several breathing cycles and normalize the ab-dominal height into tidal volume for each patient just before the treatment.16,25,26After that, the tidal volume measurement

would not be necessary 共unless removing the spirometer is

found to significantly alter the relationship of internal motion

and abdomen height兲. This would be advantageous for

pa-tients who did not want to undergo spirometry during the entire process for which the tidal volume was required.

Finally, one should be cautious when using any external breathing metrics共spirometry and abdominal height兲to infer internal tumor or tissue motion.3,23At the least the following issues need to be addressed. 共1兲 Is there a high correlation between the external metric and internal motion?共2兲 Is this relationship reproducible during the time of consideration?

共3兲 Is there a mechanism to determine and account for the

time offsets between the external metric and internal motion? Nevertheless, external breathing metrics have been demon-strated useful in predicting the tumor motion and thus in reducing the uncertainties caused by respiratory motion for many patients.6–10,12,13,15,16,18,22–26A more thorough verifica-tion of their relaverifica-tionships with tumor moverifica-tions by using real-time, direct tumor or indirect implanted marker imaging is under development in our institution.

ACKNOWLEDGMENT

This work was supported in part by National Institute of Health Grant No. R01 CA 096679.

a兲Author to whom correspondence should be addressed. Electronic mail: low@wustl.edu

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Figure

Figure 2共a兲 shows the spirometer-measured tidal volume, abdominal height, and internal air content at the times  corre-sponding to the 15 successive CT scans for one couch  posi-tion

References

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