Ann Thorac Surg 2005;80:1853-1858
© 2005 The Society of Thoracic Surgeons
Original article: General thoracic
Quantitative Computed Tomography Versus Spirometry in Predicting Air Leak Duration After Major Lung Resection for Cancer
Kazuhiro Ueda, MD
a
,
*
,
Yoshikazu Kaneda, MD
a
,
Manabu Sudo, MD
a
,
Jinbo Mitsutaka, MD
a
,
Tao-Sheng Li, MD
a
,
Kazuyoshi Suga, MD
b
,
Nobuyuki Tanaka, MD
b
,
Kimikazu Hamano, MD
a
a First Department of Surgery, Yamaguchi University School of Medicine, Ube Yamaguchi, Japan
b Department of Radiology, Yamaguchi University School of Medicine, Ube Yamaguchi, Japan
Accepted for publication May 9, 2005.
* Address correspondence to Dr Ueda, First Department of Surgery, Yamaguchi University School of Medicine, 1-1-1 Minami-Kogushi, Ube Yamaguchi 755-8505, Japan (Email: kaueda{at}c-able.ne.jp).
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Abstract
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BACKGROUND: Emphysema is a well-known risk factor for developing air leak or persistent air leak after pulmonary resection. Although quantitative computed tomography (CT) and spirometry are used to diagnose emphysema, it remains controversial whether these tests are predictive of the duration of postoperative air leak.
METHODS: Sixty-two consecutive patients who were scheduled to undergo major lung resection for cancer were enrolled in this prospective study to define the best predictor of postoperative air leak duration. Preoperative factors analyzed included spirometric variables and area of emphysema (proportion of the low-attenuation area) that was quantified in a three-dimensional CT lung model. Chest tubes were removed the day after disappearance of the air leak, regardless of pleural drainage. Univariate and multivariate proportional hazards analyses were used to determine the influence of preoperative factors on chest tube time (air leak duration).
RESULTS: By univariate analysis, site of resection (upper, lower), forced expiratory volume in 1 second, predicted postoperative forced expiratory volume in 1 second, and area of emphysema (<1%, 1% to 10%, >10%) were significant predictors of air leak duration. By multivariate analysis, site of resection and area of emphysema were the best independent determinants of air leak duration. The results were similar for patients with a smoking history (n = 40), but neither forced expiratory volume in 1 second nor predicted postoperative forced expiratory volume in 1 second were predictive of air leak duration.
CONCLUSIONS: Quantitative CT is superior to spirometry in predicting air leak duration after major lung resection for cancer. Quantitative CT may aid in the identification of patients, particularly among those with a smoking history, requiring additional preventive procedures against air leak.
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Introduction
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Prolonged air leak is a common problem in the postoperative management of patients who have undergone major lung resection for cancer. The risk of developing air leak or persistent air leak can be evaluated by assessing the severity of emphysema because the fragile lung parenchyma is easily torn during anatomic pulmonary resection and may not be resolved even long after surgery. Emphysema is diagnosed pathologically, and the risk of air leak can be predicted as well by lung radiographic morphology as by spirometry. Quantitative computed tomography (CT) is an objective diagnostic technique that uses computer software to distinguish pixels with abnormally low attenuation, representing emphysema, from those representing normal lung parenchyma [1]. The aim of this prospective study was to determine whether quantitative CT-derived variables are more sensitive than spirometric variables in predicting the duration of air leak after pulmonary resection.
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Patients and Methods
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Patients
During the period April 2003 through September 2004, 62 consecutive patients who were scheduled to undergo major lung resection at our institution for diagnosed or suspected lung malignancy were enrolled in this study. This study was approved by the Institutional Review Board of the Yamaguchi University School of Medicine. Operability was determined according to the existing guidelines for pulmonary resection [2]. Patient data obtained before surgery included age, sex, smoking habits, documented breathlessness, performance status, body mass index, site of resection (upper versus lower), spirometric variables, predicted postoperative forced expiratory volume in 1 second (FEV1, FEV1ppo), area of emphysema, and arterial blood gas values. Smoking data included pack-years smoked (smoking index: average number of packages of cigarettes smoked per day multiplied by the number of years smoked). Upper resection was defined as right or left upper lobectomy or right upper bilobectomy, and lower resection was defined as right or left lower lobectomy, right lower bilobectomy, or middle lobectomy. The FEV1ppo was calculated by Nakahara's formula [3]: FEV1ppo = FEV1 [1 - (b - n) / (42 - n)], where n is the number of obstructed subsegments, and b is the total number of removed subsegments. The total number of pulmonary subsegments was 42, with 10 each of the left upper lobe and left lower lobe, 6 of the right upper lobe, 4 of the right middle lobe, and 12 of the right lower lobe. Vital capacity (VC), FEV1, and FEV1ppo were expressed as percentage of predicted for age, sex, and height. In addition, we determined the area of emphysema by quantitative CT (described below).
Patients were 40 men and 22 women with a mean age of 68 ± 9.4 years (range, 50 to 86), mean body mass index of 22 ± 2.9 kg/m2 (range, 14.7 to 27.6 kg/m2), mean smoking index of 39 ± 38 pack-years (range, 0 to 180), and mean number of resected segments of 4.1 ± 1.2 (range, 2 to 7 segments). All patients underwent major lung resection: as lobectomy in 58 and as bilobectomy in 4.
Computed Tomography Technique and Measurement of Emphysematous Area
Computed tomography scan was performed using a four detector-row CT scanner (Siemens Volume Zoom, Siemens-Asahi Medical, Tokyo, Japan). With the patient in the supine position, high-resolution CT images covering the entire lungs were obtained in a 512 x 512 matrix at deep inspiratory breath-hold, using 10-mm collimation, scan time 1.5 seconds, 120 to 140 kVp, 280 to 320 mA. Transaxial CT images were reconstructed with the lung algorithm. To evaluate the distribution of emphysematous areas in each patient, volume-rendering three-dimensional density-masked images, which highlighted the lung areas with attenuation values of less than –910 HU representative of emphysematous lung areas were created, using the imaging software (M900 QUADRA, Zio Soft K.K., Osaka, Japan). Threshold limits of –600 to –1024 Hounsfield units (HU) were applied to segment the entire lungs and to exclude soft tissues surrounding the lung and large vessels within the lung. On the three-dimensional density-masked lung images, emphysematous lung areas were displayed by a red color (Fig 1). The proportion of the number of voxels with attenuation values less than –910 HU to the total number of voxels for the entire lung was taken as the area of emphysema (low-attenuation area [LAA]) because the low-attenuation thresholds that have been used most often to identify emphysema on conventional 10-mm-thick CT sections are –900 or –910 HU [4–7].
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Fig 1. Images obtained from a 65-year-old man with panlobular emphysema. (A) Three-dimensional shaded surface display of the lungs, representing attenuation values of –600 to –1024 HU. (B) Volume-rendering three-dimensional images of the low-attenuation areas, representing attenuation values of less than –910 HU. Note that the tracheobronchial and gastrointestinal tracts have been selectively removed. With this model, the proportion of voxels with attenuation values representing emphysema is readily determined by defining a threshold value. (C) Axial computed tomography image shows upper lobar emphysema, indicated by areas of low attenuation (–910 to –1,024 HU) highlighted in red.
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Surgical Procedures and Chest Tube Management
During lobectomy, an endoscopic stapler (Ethicon, Tokyo, Japan) was used to divide incomplete fissures and to excise the bronchus. Staple lines were never reinforced. After lobectomy, a water-seal test was performed to ensure pneumostasis. We did not perform pleural tenting to obliterate residual pleural space after upper lobectomy. Evident pulmonary fistulae in the surgical stump were closed with sutures and sealed with fibrin glue. A 20F chest tube was placed within the hemithorax, and the wounds were closed. Postoperatively, chest tubes were suctioned continuously at –10 cm H2O, and the presence of air leak was assessed visually via the suction device. Chest tubes were removed the day after disappearance of the air leak, regardless of pleural drainage; this management plan was verified previously [8]. Removal of the chest tube appeared to be the best way to confirm disappearance of the air leak (air leak stop). Therefore, chest tube removal was taken as the study endpoint.
Statistical Analysis
Unpaired Student's t test was used to test relations between categorical variables and numerical variables, and the 
2 test was used to compare categorical variables. Because LAA for consecutive lung cancer patients does not follow a normal distribution, we used LAA as a categorical variable (minimal LAA, <1%; moderate LAA, 1% to 10%; maximal LAA, >10%) in the univariate and multivariate analysis. Univariate and multivariate proportional hazards analyses were used to determine the influence of any preoperative variable on air leak duration. Stepwise variable selection was used in the multivariate analysis. A p value less than 0.05 was considered significant.
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Results
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All patients were extubated postoperatively in the operating room. A total of 6 cardiopulmonary complications occurred in 5 patients: ventilatory inefficiency (n = 1), pneumonia (n = 2), lobar atelectasis (n = 2), and atrial fibrillation (n = 1). Two patients required postoperative intervention for pulmonary complications before chest tube removal: reoperation due to prolonged air leak on postoperative day 14 in 1 patient, and completion pneumonectomy on postoperative day 4 in the other. Because these interventions could influence air leak duration, data from these 2 patients were censored.
Time to air leak stop is shown in Figure 2. Mean and median time to air leak stop were 3.1 days and 2 days, respectively. None of the patients showed pneumothorax or fluid collection after chest tube removal, with the exception of 1 patient who subsequently required chest tube reinsertion due to pneumothorax. The mean and median LAA values were 6.7% and 3.6%, respectively (range, 0.1% to 32.6%), and did not follow a normal distribution. Thus, we used LAA as a categorical variable (minimal LAA [n = 18], <1%; moderate LAA [n = 29], 1% to 10%; maximal LAA [n = 15], >10%) in the later statistical analysis.
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Fig 2. Time to air leak stop in all patients (n = 62). Two patients required postoperative interventions for pulmonary complication before air leak stopped, and these patients were flagged (open circles). Median time to air leak stop was 2 days.
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Patient characteristics are shown in Table 1. Relation between patient characteristics and LAA are shown in Table 2. The LAA was significantly dependent on variables related to obstructive lung disease. By univariate analysis (Table 3), sex, smoking history, site of resection, FEV1, FEV1ppo, and LAA were identified as possible predictors of air leak duration (p < 0.1). By multivariate analysis of these variables, site of resection (p = 0.005 and RR = 2.27 for lower resection) and LAA (p < 0.001, RR = 0.214 for maximal LAA, and p = 0.020, RR = 0.462 for moderate LAA) were selected as the best independent determinants of air leak duration. All of the patients with minimal LAA were free of chest tubes on postoperative day 3, whereas 65% and 42% of those with moderate LAA and maximal LAA, respectively, were free of chest tubes on the same postoperative day (log-rank test, p < 0.001). Similar results were obtained when analysis was further restricted to patients with an upper resection (Fig 3) or patients with a lower resection (Fig 4). When analysis was restricted to 40 patients with a smoking history, LAA was also significantly dependent on air leak duration, whereas FEV1 and FEV1ppo showed no significant relation to air leak duration (p > 0.05) by univariate proportional hazard analysis. Multivariate analysis showed site of resection (p = 0.005 and RR = 2.95 for lower resection) and LAA (p = 0.002, RR = 0.191 for maximal LAA, and p = 0.017, RR = 0.328 for moderate LAA) as significant independent predictors of air leak duration in the same patient subgroup, similar to the results for all 62 patients.
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Fig 3. Time to air leak stop in patients with upper resections (n = 38), according to low-attenuation area (LAA). Median time to air leak stop in patients with LAA less than 1% (solid line) was 1 day, that in patients with LAA 1% to 10% (dotted line) was 3 days, and that in patients with LAA greater than 10% (dashed line) was 5 days (log-rank test, p < 0.01). Flagged cases (n = 2) are denoted by open circles.
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Fig 4. Time to air leak stop in patients with lower resections (n = 24), according to low-attenuation area (LAA). Median time to air leak stop in patients with LAA less than 1% (solid line) was 1 day, that in those with LAA 1% to 10% (dotted line) was 1 day, and that in those with LAA greater than 10% (dashed line) was 3 days (log-rank test, p = 0.026).
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Comment
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Air leak duration after pulmonary resection is a primary determinant of postoperative hospital stay. In the present study, air leak duration was linearly dependent on postoperative hospital stay (r = 0.514, p < 0.0001). Therefore, predicting air leak duration may be clinically useful in terms of preventing prolonged air leak, reducing medical expenditures, and counseling patients at increased risk of prolonged air leak. There is only one published study of preoperative risk factors for prolonged air leak after major lung resection [9]. In that study, limited FEV1ppo and upper lobe resection were associated with prolonged air leak (more than 7 days) by logistic regression analysis. However, there are some limitations to logistic regression analysis; air leak lasting more than 7 days is not a universal definition of prolonged air leak and appears to be inadequate in the fast-track hospital setting of today. Some patients with complications, such as those requiring mechanical ventilation or reoperation before postoperative day 7, are not appropriate for this type of analysis. The proportional hazards model used in the present study allows for the determination of predictors of air leak duration (not risk factors for prolonged air leak) without excluding patients with complications.
Emphysema is the most frequent underlying pulmonary disease in patients undergoing lung resection for cancer. This disease is defined pathologically as an increase in the size of the airspaces distal to the terminal bronchiole, accompanied by destruction of the alveolar walls [10]. Therefore, a preoperative diagnosis of emphysema without lung tissue biopsy is indirect. Pulmonary function studies rely on the detection of increased airway resistance and decreased surface area of the alveolar-capillary membrane. These tests are relatively insensitive and nonspecific with respect to determining the cause of airway obstruction [11, 12]. Quantitative CT is an objective technique that uses computer software to distinguish voxels with abnormally low attenuation, representing emphysema, from those representing normal lung [1]. Voxel attenuation values can now be measured without the need to transfer data to other computer systems. With software that is available on most modern commercial scanners, three-dimensional lung models can be generated with volumetric data acquired in the helical mode. The lungs are easily differentiated from softtissue structures and from structures with lower attenuation, such as the trachea, mainstem bronchi, and esophagus. With these models, the proportion of voxels with attenuation values within the range representing emphysema is readily determined by moving a boundary line to a defined threshold. This computer-assisted quantification of lung morphology reflects the extent of emphysema more directly than conventional visual grading techniques [13] and is more effective than pulmonary function tests in detecting early-stage emphysema [14]. In the present study, the quantitative CT-defined emphysematous area, which reflects the severity of obstructive lung disease, was found to be more sensitive than spirometric variables in predicting air leak duration after major lung resection for cancer.
Pulmonary air leak is usually caused by dissection of the hilar area at lobar resection, particularly in patients with evident incomplete fissures or fragile, thin parenchyma that may correspond to emphysematous lung. The emphysematous lung may be torn easily during surgery and not be easily restored postoperatively, resulting in prolonged air leak. Intraoperative closing or sealing of the dissected hilar area is important for reducing the incidence of air leak. Reducing the residual pleural space after upper lobectomy or bilobectomy (ie, pleural tenting or mobilization of residual lung) is also important for promoting adhesion [15, 16]. Postoperative chest tube management with a water-seal technique may reduce air leak duration in situations where water seal drainage does not result in collapse of the residual lung [17].
Low-attenuation area cannot detect interstitial lung disease that occasionally causes prolonged air leak after pulmonary resection because the proliferating parenchyma in this disease usually enhances lung density. Although the number of patients was limited in the present study, 2 of the 3 patients with interstitial lung disease required chest tube insertion for more than 7 days because of prolonged air leak. When analysis was restricted to patients with a smoking history, the results were similar to those for all 62 subjects, but neither FEV1 nor FEV1ppo was predictive of air leak duration. These results suggest that LAA could be a useful marker in predicting air leak duration, particularly in patients with a smoking history.
With respect to qualitative evaluation of emphysema on CT images, patients with maximal LAA were classified into 2 groups according to the presence or absence of bulla formation; bullae were apparent in 7 patients in whom LAA ranged from 12% to 33%, whereas bullae were absent in the remaining 8 patients in whom LAA ranged from 12% to 29%. Emphysematous areas were distributed diffusely but were predominantly in the upper lobe in all of these patients. There was no statistical difference between the two groups in air leak duration (log-rank test, p = 0.123) or LAA (t test, p = 0.812). Therefore, we believe that qualitative evaluation of CT images in addition to quantitative analysis may add no relevant information to the prediction of air leak duration in patients with emphysema.
In conclusion, quantitative CT is superior to spirometry in predicting air leak duration after pulmonary resection. Quantitative CT may aid in the identification of patients, particularly among those with a smoking history, requiring additional preventive procedures against air leak.
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Abstract
Introduction
