Ann Thorac Surg 2000;70:1208-1211
© 2000 The Society of Thoracic Surgeons
Original articles: general thoracic
Chest radiograph heterogeneity predicts functional improvement with volume reduction surgery
John C. Baldwin, MDa,
Charles C. Miller, III, PhDa,
Rebecca A. Prince, BSa,
Rafael Espada, MDa
a Department of Surgery, Baylor College of Medicine, Houston, Texas, USA
Address reprint requests to Dr Miller, Division of Clinical Research and Outcomes, Department of Surgery, Baylor College of Medicine, Suite 404D, One Baylor Plaza, Houston, TX 77030
e-mail: cmiller{at}bcm.tmc.edu
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Abstract
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Background. Using a historical cohort study model, we tested the hypothesis that heterogeneity of emphysematous changes on the preoperative chest radiograph correlated with favorable outcome of lung volume reduction surgery.
Methods. The test population consisted of 21 patients with severe emphysema who were being treated at a 1,000-bed university-affiliated tertiary teaching hospital. A simple but quantitative index of heterogeneity has been devised, whereby the preoperative posteroanterior chest radiographic lung fields are divided into four geometric quadrants. Each quadrant is scored (0 to 4) for emphysematous changes by two radiologists blinded as to subsequent patient management and outcome. Criteria for determining presence of emphysema were hyperlucency, decreased vascular markings, and parenchymal crowding indicating compressed lung. Heterogeneity index is the sum of the two highest scores minus the two lowest, with a maximum index of 8 and a minimum of 0. Preoperative chest radiographs and postoperative changes in forced expiratory volume in 1 second were examined.
Results. The heterogeneity index was positively correlated with change in forced expiratory volume in 1 second after operation with an r2 of 0.31 and an average increase of 117 mL per unit increase in heterogeneity index (p < 0.009).
Conclusions. This simple index of heterogeneity may be useful as a predictor of improved pulmonary function after lung volume reduction surgery.
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Introduction
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Since the reintroduction of lung volume reduction surgery by Cooper and colleagues in 1995 [1], this procedure has stimulated enormous interest among patients, physicians, and scientists anxious to evaluate the role of this treatment for advanced pulmonary emphysema [2, 3]. Controversy surrounds the question of patient selection, particularly because results have varied widely between centers. Ideally, this major surgical procedure for highly debilitated patients would be used selectively, and only in that subset of patients most likely to benefit. Identification of preoperative characteristics that could be used to select patients would be a tremendous step forward in the application of this technique to this disease.
Several investigators who have published on lung volume reduction surgery [1–6] have suggested that a heterogeneous pattern of emphysema is associated with better results. Despite the general consensus in the literature that heterogeneity is important, no practical, easily implemented measure of disease heterogeneity has been published. We have recently devised a simple method for measuring the heterogeneity of emphysema based on the preoperative plain posteroanterior chest radiograph.
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Material and methods
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Twenty-one patients who underwent bilateral excisional lung volume reduction through the median sternotomy approach were included in this study. The resection was targeted predominantly at the apices of the lungs, with approximately 30% to 40% of each upper lobe removed. A buttressed stapling device was used for the resection. No lower lobe procedures were performed in this series. Preoperative descriptive statistics for the study population are shown in Table 1. All operations were performed at The Methodist Hospital in Houston, Texas, a Baylor College of Medicine primary affiliated teaching hospital.
To obtain the heterogeneity index, the posteroanterior chest radiograph was geometrically divided into four symmetrical quadrants by drawing a vertical line that bisects the transverse dimension and a horizontal line halfway between the apex and the diaphragm (Fig 1). The criteria for the severity score included increased radiolucency, decreased vascular markings, and increased deviation of parenchymal markings. Lung quadrants without radiographic evidence of severe emphysema based on these criteria were scored as zero. If 25% of the quadrant contained signs of severe emphysema, a score of 1 was assessed. If 50% of the quadrant were involved, a score of 2 was assessed, and so forth, up to a maximum of 4 (100%) for each quadrant. The sum of the two lowest scores was subtracted from the sum of the two highest scores, regardless of their orientation, and this difference was used as the heterogeneity index. The possible range for the overall heterogeneity index is 0 to 8, with 0 being least heterogeneous and 8 being most heterogeneous. Because orientation of the highest and lowest quadrants does not enter into the calculation, the index is an index of overall heterogeneity. Each chest radiograph was read by two thoracic radiologists who were blinded to patient management or outcome, and their joint opinion about each quadrant was entered into the database as the score. Spirometry was performed preoperatively and then 3 months postoperatively in a university hospital pulmonary function laboratory according to American Thoracic Society criteria.
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Fig 1. Posteroanterior chest radiograph showing the division of the field into quadrants and score assignment based on zone severity. In this example, the sum of the two most severe versus the two least severe zones is 2 + 2 - 0 + 0 = 4, so the heterogeneity index is 4.
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The study was designed as a historical cohort study. Heterogeneity score from the preoperative radiograph was used to predict change from baseline of the postoperative forced expiratory volume in 1 second (FEV1). The heterogeneity index is a linear scale, and although it is ordinal rather than continuous, we considered its inherent linearity robust enough to allow for a regression analysis. To estimate the slope of change in FEV1 with change in heterogeneity index, we performed a least-squares linear regression analysis with index as the independent variable and FEV1 change as the dependent variable. For purposes of technical correctness, however, we also performed a one-way analysis of variance with heterogeneity as the independent variable and FEV1 change as the dependent variable. Data were maintained in Microsoft Access databases and analyzed using SAS version 6.12 running under Windows NT.
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Results
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Table 2 shows postoperative descriptive statistics for the population. Figure 2 shows the regression plot of heterogeneity index versus preoperative to postoperative change in FEV1. Table 3 shows the mean FEV1 change by score category and the corresponding 95% t distribution confidence intervals. Patients with scores of 3 and 4 had significantly greater mean change in FEV1 after operation. As heterogeneity increases, gains in FEV1 after operation also increase. Patients with the least heterogeneous patterns of disease tended to have little improvement or even to have worse pulmonary function after operation. No patient who had a heterogeneity score greater than 2 got worse, and all but one had at least some improvement in FEV1 postoperatively. One third of the patients with heterogeneity scores of 2 or more had improvements in FEV1 of 500 mL or more.
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Fig 2. Scatter plot of preoperative to postoperative change in forced expiratory volume in 1 second (FEV1) against heterogeneity index. The line is a least-squares linear regression line. Patients with heterogeneity indices of 0 or 1 tended to stay the same or get worse, whereas patients with indices of 3 or 4 had improvements ranging from approximately 50 to approximately 850 mL.
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Comment
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In this study, we report a simple, semiquantitative measure of emphysema disease heterogeneity. The scoring method subtracts the sum of the two lowest-scored quadrants from the sum of the two highest-scored quadrants, regardless of their orientation. It is important to recognize that this index is an index of heterogeneity and not inherently an index of severity, even though the scoring system is based on severity. A patient with moderately advanced radiographic evidence of emphysema, 2 + 2 minus 0 + 0, or 4 - 0 = 4, would have the same score as a patient with extensive radiographic evidence, 4 + 4 minus 2 + 2, or 8 - 4 = 4. Patients with differing magnitudes of underlying parenchymal destruction can have the same score, as long as the relationship between the regional differences is equivalent. We are unable, unfortunately, to evaluate the degree of emphysema by computed tomographic scan for purposes of correlating computed tomography findings with heterogeneity on chest radiograph. These cases came from our center’s early experience, and we did not have standardized computed tomography protocols in place at the time. We are unable to expand the series beyond the initial 21 patients because we have a National Emphysema Treatment Trial (NETT) clinical center at our institution, and our surgeon is principal investigator. The trial’s regulations forbid non-NETT volume reduction surgery, and we obviously cannot release NETT clinical data until that study is completed and results are disseminated by the coordinating center.
Because of the small sample size, we did not evaluate reliability of the radiographic interpretations. The two radiologists decided to read together and use a consensus score for each quadrant. In this unfunded study, we found it difficult to get enough radiologist time for one reading per film. For interrater and intrarater reliability studies to be done right, we would need large enough samples to permit the construction of Fleiss reliability statistics by random-effects analysis of variance [7].
The score produced by this simple method accounted for 31% of the variance in FEV1 change after operation, and the findings support the general consensus of the volume reduction literature, that patients with a heterogeneous disease pattern derive greater benefit from operation. Given the wide variation in the characteristics of underlying disease in this patient population and the wide variability in outcome that has been reported in the literature, a correlation coefficient of 0.31 is substantial, and indeed is higher than we expected it to be.
The slope coefficient can be multiplied by the heterogeneity index, and the intercept can be added to produce an expected change in postoperative FEV1 for a given level of heterogeneity. If our findings hold in larger populations, the simple better criteria for selecting patients who are likely to benefit most from operation, simple indices such as the one we present bear further investigation. Future studies should validate the method prospectively and evaluate it in concert with other predictors to determine where measures of disease heterogeneity fit into the overall patient selection picture.
Slone and Gierada [8] have written previously regarding the importance of radiologic factors, including inspiratory and expiratory chest radiographs and computed tomography examination in assessing severity of disease and in correlating with postoperative spirometric outcomes. However, we have developed what we believe is a simple and useful screening tool based on the simple posteroanterior and lateral chest radiograph. It should also be noted that Wisser and colleagues [9] have commented on "morphorlogic grading" and its relationship to lung volume reduction results. In their system, they do include a reference to "degree of heterogeneity" and use a grading system of 0 to 4. We believe that this simple method of assessing the preoperative chest radiograph is a useful predictor of results of volume reduction surgery.
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References
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Cooper J.D., Trulock E.P., Triantafillou A.N., et al. Bilateral pneumectomy (volume reduction) for chronic obstructive pulmonary disease. J Thorac Cardiovasc Surg 1995;109:106-116.[Abstract/Free Full Text]
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Brenner M., Yusen R., McKenna R., et al. Lung volume reduction surgery for emphysema. Chest 1996;110:205-218.[Abstract/Free Full Text]
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Cooper J.D. The history of surgical procedures for emphysema. Ann Thorac Surg 1997;63:312-319.[Free Full Text]
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Slone R.M., Gierada D.S., Yusen R.D. Preoperative and postoperative imaging in the surgical management of pulmonary emphysema. Radiol Clin North Am 1998;36:57-89.[Medline]
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Gierada D.S., Slone R.M., Bae K.T., Yusen R.D., Lefrak S.S., Cooper J.D. Pulmonary emphysema. Radiology 1997;205:235-242.[Abstract/Free Full Text]
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Gierada D.S., Hakimian S., Slone R.M., Yusen R.D. MR analysis of lung volume and thoracic dimensions in patients with emphysema before and after lung volume reduction surgery. AJR Am J Roentgenol 1998;170:707-714.[Abstract/Free Full Text]
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Fleiss J.L. The design and analysis of clinical experiments. New York: John Wiley & Sons, 1986.
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Slone R.M., Gierada D.S. Radiology of pulmonary emphysema and lung volume reduction surgery. Semin Thorac Cardiovasc Surg 1996;8:61-82.[Medline]
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Wisser W., Klepetko W., Kontrus M., et al. Morphologic grading of the emphysematous lung and its relation to improvement after lung volume reduction surgery. Ann Thorac Surg 1996;65:793-799.[Abstract/Free Full Text]
Accepted for publication January 21, 2000.
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Abstract
Introduction
