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Ann Thorac Surg 1998;65:793-799
© 1998 The Society of Thoracic Surgeons

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Original Articles: General Thoracic

Morphologic Grading of the Emphysematous Lung and Its Relation to Improvement After Lung Volume Reduction Surgery

Department of Cardiothoracic Surgery, University of Vienna, Vienna, Austria
Department of Anesthesiology, University of Vienna, Vienna, Austria
Department Radiology, University of Vienna, Vienna, Austria,
Department of Medical Computer Sciences, University of Vienna, Vienna, Austria
Pulmonary Department, Lainz Hospital, Vienna, Austria

Accepted for publication August 18, 1997.

Dr Wisser, Department of Cardiothoracic Surgery, University of Vienna, Währinger Gürtel 18-20, A-1090 Vienna, Austria.

	Abstract

Top Abstract Introduction Material and Methods Results Comment Acknowledgments References

 
Background. The morphologic criteria for lung volume reduction surgery, such as severity and heterogeneity of disease, differ widely between patients, and this makes any comparison of functional results between centers difficult. Here we present a morphologic scoring system and describe its possible relation to functional results after lung volume reduction operations.

Methods. Between September 1994 and December 1996, 47 consecutive patients underwent bilateral lung volume reduction operations. The morphology of emphysema was quantified with standard chest roentgenograms and computed tomographic imaging, which were used to define the following four variables: degree of hyperinflation (grade 0 to 4), degree of impairment in diaphragmatic mechanics, degree of heterogeneity (grade 0 to 4), and severity of parenchymal destruction (range, 0 to 48).

Results. All four variables showed good reproducibility. Degree of heterogeneity had a significant influence on functional improvement in terms of forced expiratory volume in 1 second (p = 0.0413, r² = 0.11). Severity of parenchymal destruction was significantly associated with 30-day mortality: patients who died after operation (n = 4) had a severity of parenchymal destruction of 28.4 ± 2.1 compared with 21.3 ± 1.0 for those who survived (n = 43) (p = 0.003).

Conclusions. This morphologic scoring system is easy to use, is reproducible, and allows quantification of the morphology of emphysema, thereby allowing definition of different patient subgroups. Such an exact morphologic quantification may help in the comparison of functional results between centers. Furthermore, the risk factors for certain morphologic subgroups, such as patients with a homogeneous distribution pattern, may be clarified in the future.

	Introduction

Top Abstract Introduction Material and Methods Results Comment Acknowledgments References

 
Lung volume reduction surgery (LVRS) for patients with severe emphysema is now an established procedure [1][2]. However, the selection criteria for LVRS still are being discussed and differ widely between centers. Although the basic values of lung function variables (eg, forced expiratory volume in 1 second [FEV₁] < 35% of predicted, residual volume > 250% to 300% of predicted, and TLC total lung capacity > 120% of predicted) required for such a procedure are often used, there is controversy about the morphologic criteria for the severity and the distribution of emphysema that make a patient a possible candidate for LVRS.

Most studies state only that patients with "heterogeneity of disease" underwent surgical intervention. However, in clinical practice, a wide range of severity and heterogeneity of emphysema can be observed. Whereas most North American centers consider the absence of heterogeneity a contraindication to LVRS, we and other European groups have operated on patients with a completely homogeneous distribution pattern of emphysema. As a result, these varying morphologic criteria make a comparison of operative and functional results between centers difficult. It is important that future reports on LVRS be based on a widely accepted grading system that classifies and quantifies the different morphologic forms of emphysema.

In its optimal form, such a system must be easy to work with and must be reproducible with a high degree of conformity. It should include definitions for degree of hyperinflation (DHI), degree of impairment of diaphragmatic mechanics (DIDM), degree of heterogeneity (DHG), and severity of parenchymal destruction (SPD). Values of the last two variables must be representative of the lungs and must be expressed in a way that allows their inclusion in a mathematical analysis.

Recently, Slone and Gierada [3] described the radiologic assessment for the LVRS program at Washington University School of Medicine in St. Louis. The authors introduced a grading scale for regional assessment of SPD and heterogeneity based on computed tomographic (CT) scans that comes close to our desired definitions but, in our opinion, does not fulfill them completely. We therefore have modified this system in a way that should allow both a higher degree of reproducibility and the mathematical quantification of heterogeneity and severity of disease. Here we present this modified morphologic scoring system and describe its relation to outcome.

	Material and Methods

Top Abstract Introduction Material and Methods Results Comment Acknowledgments References

 
Design
The study comprised 47 consecutive patients (27 men and 20 women with a mean age of 55.9 ± 1.4 years; range, 38 to 75 years) who underwent bilateral LVRS between September 1994 and December 1996. The first 15 patients underwent operation through a median sternotomy, and the remaining 32 patients, by a videoendoscopic approach. In 5 patients, conversion from a videoendoscopic approach to a thoracotomy was necessary because of multiple adhesions. The operative procedure was performed as described previously [2].

Functional Assessment
All patients underwent a complete clinical workup preoperatively and 3 months postoperatively. It consisted of pulmonary function tests with spirometry and measurement of lung volumes, arterial blood gas testing, and measurement of work of breathing and intrinsic positive end-expiratory pressure [4].

Morphologic Assessment
Preoperative patient evaluation was performed using standard chest roentgenograms in anteroposterior and lateral views in full inspiration and expiration. In addition, CT imaging with high-resolution CT scan and spiral CT scan (both, Siemens Somatom Plus S; Siemens Medical Systems, Erlangen, Germany) was done. High-resolution CT scans were performed with a 1-mm slice thickness and 15-mm gap interval in deep inspiration. Spiral CT imaging was done with an 8-mm slice thickness, a 16-mm table feed, and a 1-second rotation time. The CT imaging was triggered spirometrically (Erich Jaeger GmbH & CoKG, Hoechberg, Germany) during inspiration with a cutoff at 80% of individual vital capacity.

The area of lung and the density were calculated at every layer of spiral CT images using semiautomated image software (Siemens Pulmo CT; Siemens Medical Systems). All areas between -950 and -1024 Hounsfield units were computed and visualized by depicting them in white. This enabled detection of the target areas for resection and quantification of the degree of disease easily.

The following variables were assessed by three different blinded readers: DHI, DIDM, DHG, and SPD. The DHI was measured as outlined by Slone and Gierada [3]. On the lateral view of the chest roentgenogram at full expiration, hyperinflation was graded according to the position of the diaphragm from grade 0 (normal curved diaphragm) to grade 3 (marked hyperinflation, ie, flattened diaphragm) and grade 4 (severe hyperinflation, ie, inverted diaphragm).

The DIDM was assessed by measuring the maximal movement between full inspiration and expiration on the respective lateral chest roentgenograms and was expressed in centimeters. The less the diaphragmatic excursion becomes, the higher is the degree of mechanical impairment.

The DHG was determined in the following manner: Three distinct layers of spiral CT imaging, which were exactly defined by anatomic structures, were chosen as reference levels in each patient. The first layer was at the upper border of the aortic arch, the second was 2 cm below the level of the carina, and the third was 2 cm above the highest diaphragmatic dome. At each level, each lung was divided into two extraanatomic segments. The separation line between both segments was chosen according to the most prominent difference in this layer. Each segment had to be at least 30% of the whole lung area.

The amount of destroyed lung parenchyma in all of the resulting 12 segments was graded. The grading scale for regional assessment of severity of emphysema that was proposed by Slone and Gierada [3] was used: grade 0 = normal lung; grade 1 (mild) = less than 25% air space compared with lung; grade 2 (moderate) = 25% to 50% air space compared with lung; grade 3 (marked) = more than 50% air space compared with lung; and grade 4 (severe) = no normal lung. The difference between the median of the three worst sections and the three best sections was calculated and used to express the overall DHG from 0 to 4.

The severity of emphysema, or the SPD, in regard to the overall amount of destroyed lung parenchyma was characterized by the sum of all 12 graded extraanatomic segments.

With these four variables taken into account, seven different distribution patterns of emphysema were characterized: homogeneous, upper, lower, anterior, posterior, lobar, and indifferent. A DHG of 0 and 1 determined a homogeneous type of distribution. When the DHG was 2 or higher, the distribution was considered heterogeneous. If the worst areas were in the upper or lower layer of the CT scan, an upper or lower type of distribution, respectively, was defined. If the worst areas were in the anterior or posterior portion of all three layers and involved all lobes equally, an anterior or posterior type of distribution, respectively, was present. Preponderant destruction of one lobe and a DHG of 2 or more was considered a lobar type. A DHG of 2, or higher combined with a patchy, uneven distribution of lung destruction identified an indifferent type. Fig 1Fig 2Fig 3Fig 4 are examples of typical findings in patients with upper, anterior, and homogeneous types of distribution with the respective morphometric variables.

View larger version (141K): [in this window] [in a new window]   Typical findings in patient with upper type of distribution with low severity of parenchymal destruction (SPD). On the preoperative computed tomographic images, all areas between -950 and -1024 Hounsfield units are depicted in white. (A) Layer at upper border of aortic arch, (B) layer 2 cm below level of carina, and (C) layer 3 cm above highest diaphragmatic dome, (D) results of our scoring system. This patient had a preoperative forced expiratory volume in 1 second of 10.7% of predicted, which increased to 33.3% of predicted after 3 months. (DHG = degree of heterogeneity; DHI = degree of hyperinflation; DIDM = degree of impairment in diaphragmatic mechanics.)

View larger version (143K): [in this window] [in a new window]   Typical findings in patient with upper type of distribution with high severity of parenchymal destruction (SPD). This patient had a preoperative forced expiratory volume in 1 second of 41% of predicted, which increased to 86.3% of predicted after 3 months. See Fig 1 for imaging technique and other abbreviations.

View larger version (143K): [in this window] [in a new window]   Typical findings in patient with anterior type of distribution. This patient had a preoperative forced expiratory volume in 1 second of 23% of predicted, which increased to 35.1% of predicted after 3 months. See Fig 1 for imaging technique and abbreviations.

View larger version (140K): [in this window] [in a new window]   Typical findings in patient with homogeneous type of distribution. This patient had a preoperative forced expiratory volume in 1 second of 25.5% of predicted, which increased to 38.5% of predicted after 3 months. See Fig 1 for imaging technique and abbreviations.

Statistical Analysis
Three blinded readers graded the DHG and SPD on the CT images and DHI and DIDM on the chest roentgenograms. The degree of agreement was estimated by the weighted kappa coefficient [5] for DHG and DHI. The interobserver difference for SPD was analyzed according to the method of Bland and Altman [6]. Regression analysis was used to evaluate the dependence of the functional improvement on DHG and DHI. To test for a possible nonlinear dependence, a quadratic term was included in the regression model. The correlations of SPD and DIDM with FEV₁ improvement were calculated using Spearman correlation coefficients. Comparisons between two morphologic subsets were performed with the Student t test. Comparison between preoperative and postoperative values of FEV₁ was performed with the paired Student t test. A p value smaller than 0.05 was considered significant. All values are expressed as the mean ± the standard error of the mean.

	Results

Top Abstract Introduction Material and Methods Results Comment Acknowledgments References

 
Morphologic Assessment
The DHI, DIDM, DHG, and SPD data are summarized in Table 1Table 2. The DHI showed good interobserver agreement (weighted kappa = 0.687, 0.712, and 0.752 for the three readers). A similar agreement was observed for the DHG (weighted kappa = 0.682, 0.539, and 0.785, respectively). The interobserver differences for the SPD were also small. Of the differences in the scores between the readers, 97.9% were within the ±3 interval.

Functional Assessment
The perioperative mortality rate was 8.5% (4/47 patients). No patient was lost to follow-up. The preoperative FEV₁ for all patients was 25.3% ± 1.4% of predicted and improved to 42.4% ± 4.5% of predicted 3 months after LVRS (p < 0.001).

Correlation of Morphologic Variables With Functional Improvement
Grouping of the patients according to DHI demonstrated that the only patient with a DHI = 1 had an increase in FEV₁ of 2%; patients with a DHI = 2, of 61.3% ± 28.5%; patients with a DHI = 3, of 71.4% ± 11.7%; and patients with a DHI = 4, of 80.8% ± 26.4% from preoperative to postoperative values. There was no significant influence of DHI on FEV₁ (p = 0.618; r² = 0.06).

No significant correlation was found between DIDM and FEV₁ (r = 0.059, p = 0.73).

Grouping of the patients according to DHG showed that patients with a DHG = 1 had an increase in FEV₁ of 60.5% ± 20.0%; patients with a DHG = 2, of 41.9% ± 10.1%; patients with a DHG = 3, of 81.7% ± 19.9%; and patients with a DHG = 4, of 160.3% ± 28.7% from preoperative to postoperative values. Regression analysis revealed a linear influence of DHG on functional improvement (p = 0.0413, r² = 0.11). Inclusion of a quadratic term for DHG showed an even stronger relation (p = 0.0335, r² = 0.21).

No significant difference in terms of FEV₁ improvement was calculated for SPD (r = 0.295, p = 0.068). However, when correlated with the 30-day mortality (4/47), a strong impact of SPD on survival was found. Patients who died within the first 30 days after operation had an SPD of 28.4 ± 2.1 (n = 4), whereas patients who survived had an SPD of 21.3 ± 1.0 (n = 43) (p = 0.003).

	Comment

Top Abstract Introduction Material and Methods Results Comment Acknowledgments References

 
Lung volume reduction surgery has been introduced to treat patients with diffuse nonbullous emphysema [7][8]. Several reports [1][9][10][11][12][13] have demonstrated its beneficial effects on lung function and on chest wall mechanics as well. However, the reported range of improvement in lung function variables, especially FEV₁, varies widely. In part, this is due to the application of different surgical techniques (eg, unilateral versus bilateral reduction) and, in part, to different patient selection criteria. In this context, one of the most important criteria is the morphologic status of the emphysematous lung. Whereas LVRS was initially proposed for the treatment of patients with marked heterogeneity of disease only, several centers have also operated on patients with a completely homogeneous distribution type. Therefore, results from individual centers can be compared only inadequately as long as there is no uniform system to describe the structural changes in the lungs of patients undergoing the operation.

A number of other arguments can be added to support use of uniform grading system. Several authors have prosed that heterogeneity of disease is a prerequisite for substantial improvement after LVRS. However, to date, no clear published data exist about the impact of DHG on functional improvement. It also remains unproven whether the overall degree of parenchymal destruction increases the risk of operation. Finally, it is still unknown whether the degree of mechanical impairment of diaphragmatic function correlates with postoperative improvement in lung function. These points as well as others mandate a morphologic grading system.

Much of such a system has already been proposed by Slone and Gierada [3]. They presented an excellent grading system for DHI and degree of impaired diaphragmatic movement, which should be part of a morphologic assessment. In addition, they suggested classification of the regional heterogeneity of disease on the CT scan. Their system provides an excellent definition for grading the regional distribution pattern of heterogeneity on a single CT image only, but it did not define the overall heterogeneity in an adequate way. We adopted this system for regional assessment of heterogeneity but modified it so as to allow expression of the overall DHG in mathematical terms, thus making further statistical analysis possible. In addition, this system enabled us to quantify the overall SPD of the lungs.

Reproducibility of this system was high and interobserver differences were low. These findings suggest that this new system should be easy to use for comparison of data between different institutions.

We found an almost equal distribution of patients with homogeneous disease (DHG 1, n = 15), patients with mild heterogeneity (DHG = 2, n = 16), and patients with marked heterogeneity (DHG 3, n = 16). Most likely this is contrary to the distribution in other centers, which generally consider heterogeneity a necessary prerequisite for LVRS. However, because of the lack of a precise morphologic definition of these patient subgroups, this must remain speculative.

It was striking that not only patients with heterogeneous disease but also patients with homogeneous disease showed a substantial improvement in lung function. The improvement in the homogeneous subgroups was even higher than the mean improvement for all patients in some previous reports [11]. Further analysis of this now well defined homogeneous subgroup for the influence of additional factors, such as mechanics of breathing [4], will be necessary to clarify the role of LVRS in the treatment of homogeneous disease.

We were surprised at the wide range of parenchymal destruction observed in our patient population—from an SPD = 7 (parenchyma with almost normal structure) to an SPD = 33 (extensive destruction of the lung parenchyma). This is evidence that despite identical preoperative lung function variables and similar degrees of heterogeneity (see Fig 1 Fig 2), patients can have a striking difference in structure. Although SPD had no influence on the amount of postoperative functional improvement, it had a clear correlation with perioperative mortality. Severity of parenchymal destruction could be a valuable morphologic variable to describe the operative risk of a patient.

In summary, the use of a morphologic grading system is important for an exact definition of different patient population. In our hands, it was easy, reproducible, and feasible. With this system we were able to define morphologic subgroups and to prove that not only patients with severe heterogeneity but also patients with homogeneous disease can show substantial improvement after LVRS. Further analysis of different subgroups for the influence of additional factors, such as intrinsic positive end-expiratory pressure or work of breathing, should be undertaken and will perhaps provide more precise selection criteria.

	Acknowledgments

Top Abstract Introduction Material and Methods Results Comment Acknowledgments References

 
We acknowledge the contributions of Marlene Thiem, RTA, and Sylvia Kiss, RTA, for their extra efforts computing the regions of interest in the CT scans.

	References

Top Abstract Introduction Material and Methods Results Comment Acknowledgments References

 

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This Article Abstract Full Text (PDF) Alert me when this article is cited Alert me if a correction is posted Citation Map Services Email this article to a friend Similar articles in this journal Similar articles in PubMed Alert me to new issues of the journal Add to Personal Folders Download to citation manager Author home page(s): Wilfried Wisser Walter Klepetko Ernst Wolner Permission Requests Citing Articles Citing Articles via HighWire Citing Articles via Google Scholar Google Scholar Articles by Wisser, W. Articles by Wolner, E. Search for Related Content PubMed PubMed Citation Articles by Wisser, W. Articles by Wolner, E.