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Ann Thorac Surg 1999;68:1792-1798
© 1999 The Society of Thoracic Surgeons

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Original Articles

Two years’ outcome of lung volume reduction surgery in different morphologic emphysema types

^a Pulmonary Division, Department of Internal Medicine, University Hospital, Zürich, Switzerland
^b Division of Thoracic Surgery, Department of Surgery, University Hospital, Zürich, Switzerland

Address reprint requests to Dr Weder, Division of Thoracic Surgery, Department of Surgery, University Hospital, CH-8091 Zürich, Switzerland

Presented at the Thirty-fifth Annual Meeting of The Society of Thoracic Surgeons, San Antonio, TX, Jan 25–27, 1999.

	Abstract

Top Abstract Introduction Patients and methods Results Comment References

 
Background. Lung volume reduction surgery (LVRS) improves dyspnea, pulmonary function, and quality of life in selected patients with severe emphysema. We investigated the role of emphysema morphology in 37 patients as an outcome predictor for up to 2 years after operation.

Methods. Patients selected for bilateral thoracoscopic LVRS were divided, according to a simplified emphysema morphology classification, into three groups (homogeneous, moderately heterogeneous, and markedly heterogeneous) based on a preoperative chest computed tomogram. Pulmonary function, walking distance, and dyspnea were assessed.

Results. Functional improvement after LVRS was best in markedly heterogeneous emphysema with an increase from preoperative forced expiratory volume in 1 second of 31% ± 2% (mean ± standard error of the mean) to 52% ± 4% of predicted postoperatively. It was significantly higher than in homogeneous emphysema (from 26% ± 1% to 38% ± 2% predicted) and in intermediately heterogeneous emphysema (from 29% ± 2% to 44% ± 45% predicted). At 24 months postoperatively, forced expiratory volume in 1 second and dyspnea score continued to be significantly better than preoperative levels in all three morphologic groups. The survival rate was highest in patients with markedly heterogeneous emphysema.

Conclusions. Functional and subjective improvements were maintained after LVRS for at least 24 months in patients with heterogeneous or homogeneous emphysema type.

	Introduction

Top Abstract Introduction Patients and methods Results Comment References

 
Lung volume reduction surgery (LVRS) improves dyspnea, lung function, and quality of life in selected patients with advanced pulmonary emphysema [1–3]. Appropriate patient selection has been stressed by many authors and includes clinical and physiologic features as well as morphologic aspects of emphysema. Most centers select patients for LVRS only if marked differences in the severity of emphysema are present in chest computed tomography (CT) and lung perfusion scan [1, 4].

Based on a simple computed tomography-based radiologic emphysema classification we showed that patients with intermediately heterogeneous or even homogeneous emphysema had clinical improvement at 3 months after the intervention [5, 6]. The purpose of the present study was to prospectively compare the clinical and functional outcomes for 2 years after bilateral thoracoscopic LVRS between patients with the three emphysema types as assessed by CT-based radiologic emphysema classification [5].

	Patients and methods

Top Abstract Introduction Patients and methods Results Comment References

 
Whole cohort
A total of 101 consecutive emphysema patients (38 women) had bilateral LVRS by video-assisted thoracoscopy at our institution between August 1994 and December 1998. Their mean age (± standard error of the mean) at operation was 63 ± 1 years (range, 38 to 78 years). They were severely symptomatic with a mean modified Medical Research Council dyspnea score of 3.6 ± 0.1 and had severe airflow obstruction with a mean forced expiratory volume in one second (FEV₁) of 0.78 ± 0.02 L, which was 28% ± 1% predicted, a mean total lung capacity (TLC) of 8.27 ± 0.14 L (137% ± 2% predicted), a mean residual volume (RV) of 5.36 ± 0.10 L (241% ± 5% predicted), and a mean RV/TLC ratio of 0.65 ± 0.01. All patients consented to be enrolled in a prospective study on outcome after LVR operation, as previously described [5]. The study was approved by the hospital’s ethics committee.

Study group
This study included a subgroup of 37 patients (13 women), mean age 66 ± 2 years, who had follow-up of 2 years. They did not differ from the whole cohort with respect to mean age and preoperative functional characteristics. All patients previously were heavy smokers. None of the 13 patients with ZZ homozygous 1-antiprotease deficiency (3 reaching 24 months) were included in this subgroup, because this feature might be an important confounding variable [7].

Twelve patients had a homogeneous and 7 an intermediately heterogeneous type of emphysema. Thirteen of 18 patients with markedly heterogeneous emphysema had upper lobe predilection and 3 an upper lobe as well as apical lower lobe predilection, whereas lower lobe predilection was observed in only 2 patients.

Clinical, functional, and radiologic evaluation
Preoperative patient evaluation included a medical history and extensive clinical work-up and radiographic CT, and scintigraphic examinations. At 3 and 6 months postoperatively, then at 6-month intervals, a clinical evaluation, pulmonary function tests, determination of the walking distance, and the assessment of dyspnea were done.

Dyspnea was graded with an integer from 0 to 4 according to the modified Medical Research Council dyspnea score [8].

Pulmonary function was tested after inhalation of two puffs of salbutamol, while adhering to standard criteria for the Sensor Medics Autobox plethysmograph (Sensor Medics, Yorba Linda, CA) and using reference values from the European Community for Steel and Coal [9]. For the assessment of 6-minute walking distance, the patients walked uncoached in a hallway without oxygen supplementation. Arterial blood gas values were determined while seated and breathing room air.

Computed tomographic examinations were done with a Somatom Plus 4 scanner (Siemens, Erlangen, Germany) at high-resolution setting, using an increment of 15 mm, a slice thickness of 1 mm, 140 kV, and 11 mA. Conventional spiral CT examinations with 8-mm collimation, 140 kV, 206 mA were used to identify target areas for operation.

Morphologic assessment (computed tomographic grading system)
As previously described [5], we used a validated simplified, surgically oriented classification of emphysema morphology by standardized high-resolution and spiral CT scans without density mask measurements. For the first 28 patients, CT scans were classified retrospectively, but blinded to clinical information by 6 physicians, the remaining 73 CT scans were scored preoperatively. Agreement was obtained in each case by at least two participating physicians.

Briefly, the following definitions were applied:

1. Homogeneous—no regional or only minor differences in the severity of emphysema (ie, decreased density, loss of vascular lung structure) are appreciable.
   
2. Intermediately heterogeneous—a distinct regional difference in the severity of emphysema is present maximally in the area of one or more than one segment but not adjacent lung segments of either lung.
   
3. Markedly heterogeneous—a distinct regional difference in the severity of emphysema is present in at least the area of two adjacent lung segments of either lung.
   

The following features were also assessed for intermediately or markedly heterogeneous cases:

Predominant upper lobe type—emphysema is preferentially located in the upper lobe with or without involvement of the apical segments of the lower lobes.

Predominant lower lobe type—emphysema is preferentially located in the lower lobe and may or may not involve the lingula or the middle lobe, respectively.

Bullae—one or few single bullae with a diameter of less than 7 cm are also present.

Asymmetry between the lungs.

Surgical technique
LVRS was performed bilaterally by video-assisted thoracoscopy [3]. The most destroyed zones of lung parenchyma, ie, target areas for resection, were identified on CT scans and perfusion scintigrams, and in some cases during operation, by delayed resorption atelectasis. A cumulative volume of approximately 20% to 30% of the lung volume on each side was resected using buttressed and nonbuttressed endoscopic staplers (Endo-GIA 30 and 60, Auto Suture; United States Surgical Corporation, Norwalk, CT, or ECL-45; Ethicon Endo-Surgery, Cincinnati, OH). In cases with no target areas (homogeneous type), the resection was done mostly in the upper lobes. Two chest tubes were inserted on each side and connected to suction between 10 and 20 cm H₂O or to Heimlich valves.

Data analysis
Descriptive statistics, expressed as mean and standard error of the mean, two-tailed tests, and linear regressions were used. Paired t test or analysis of variance followed by Tukey post hoc test, where appropriate, were used to detect differences within the same groups, or between groups. Differences between observed proportions of more than two independent samples were analyzed by ² test, whereas Fisher exact test was used for differences between the observed proportions of two independent samples. Survival differences between the three morphologic groups were analyzed using a Kaplan-Meier plot and a stratified Cox regression model. The SYSTAT for Windows software package, release 8.02 (SPSS Inc, Chicago, IL) was used. A p value of 0.05 or less was considered significant.

	Results

Top Abstract Introduction Patients and methods Results Comment References

 
Preoperative findings
The mean age at operation was 66 ± 2 years and did not differ in the three groups. Among 18 patients with markedly heterogeneous emphysema the proportion of men was higher (Table 1) than in the other two groups.

Mean arterial oxygen tension was 66 ± 2 mm Hg, and mean arterial carbon dioxide tension was 39 ± 1 mm Hg. Carbon monoxide diffusing capacity 43% ± 2% of predicted value. These gas exchange parameters did not differ between the groups.

Clinical and functional findings 3 months postoperatively
Bilateral thoracoscopic LVRS (mean hospital stay, 16 ± 1 days; mean drainage time, 9.7 ± 0.7 days; median, 8 days) resulted in significant improvement of dyspnea, pulmonary function, and walking distance in all three study groups (Table 1). Decrease of airflow obstruction and pulmonary hyperinflation was significantly higher in the markedly heterogeneous group compared with the two other groups.

Clinical and functional evolution 2 years after LVRS
Postoperative improvement of dyspnea was comparable in all three groups and remained up to 2 years after the intervention (Table 1 and Fig 1). Forced expiratory volume in 1 second, as a percentage of its predicted value (% predicted) decreased gradually after attaining its maximal value at 3 months. It was still significantly higher up to 24 months postoperatively in all three groups. At 2 years, FEV₁ (% predicted) was higher by 24% compared with baseline in the homogeneous emphysema group, and by 41% and 39% in the intermediately and markedly heterogeneous groups, respectively (Table 1 and Fig 2).

View larger version (17K): [in this window] [in a new window]   Fig 1. Medical Research Council (MRC) dyspnea score over time in the three morphology groups. Values are given as mean ± standard error of the mean.

View larger version (19K): [in this window] [in a new window]   Fig 2. Forced expiratory volume in 1 second (FEV1) as percentage of its predicted value, in the three computed tomographic morphologic groups. Values are given as mean ± standard error of the mean.

View larger version (19K): [in this window] [in a new window]   Fig 3. Residual volume/total lung capacity (RV/TLC) ratio in the three computed tomographic morphologic groups. Values are given as mean ± standard error of the mean.

Slope calculation by linear regression through the FEV₁ data points of all controls from the third postoperative month to 24 months postoperatively corroborated the estimation as given in Table 1 (data not shown).

Mortality rate and loss of follow-up in the entire study cohort
During the 2 years of follow-up after LVRS of each individual there were nine deaths in the entire cohort of 101 patients (one perioperative, eight postoperative) (Table 2). In the whole observation period of the study cohort, ie, 186 patient-years of follow-up (median, 650 days per patient), 16 deaths occurred until December 1998 (6 of 26 patients with homogeneous, 7 of 26 patients with intermediately heterogeneous, 1 of 36 patients with markedly heterogeneous CT morphology, and 2 of 13 patients with 1-antitrypsin deficiency). The difference in survival in the three morphologic groups was significant (p = 0.006) and confirmed the highest survival in the markedly heterogeneous morphology group (Fig 4).

View larger version (30K): [in this window] [in a new window]   Fig 4. Survival in the three different morphologic groups. The difference in survival in the three groups was significant (p = 0.006).

	Comment

Top Abstract Introduction Patients and methods Results Comment References

 
This prospective follow-up study assessed the duration of benefit of bilateral LVRS in respect to differences in emphysema morphology. We previously showed short-term (ie, at 3 months) improvements of dyspnea, exercise performance, and lung function after bilateral thoracoscopic LVR operation in our study population [5]. We also found the most pronounced amelioration in patients with markedly heterogeneous emphysema, but there was clinically relevant improvement in patients with homogeneous or intermediately heterogeneous types of emphysema as well [5].

This 2-year follow-up study of the same cohort confirmed those findings. Despite an expected gradual decline of pulmonary function over time, dyspnea as well as relevant functional variables were still significantly different from their preoperative values for 24 months in all three emphysema morphology groups, even in patients with homogeneous emphysema.

Only few published studies are available on the effect of LVRS on lung function in patients with homogeneous [3, 5, 10, 11] or intermediately heterogeneous [10], compared with markedly heterogeneous, emphysema morphology. Patients with a homogeneous type of emphysema have been excluded a priori from LVRS at many centers, as documented in a recent European Survey performed by us (submitted for publication). Homogeneous emphysema morphology accounted for about two thirds of the rejections from operations in one center reporting on 300 cases [4]. Two to three times more often, that was the reason for rejection rather than medical contraindication to operation. The rationale not to operate on patients with homogeneous emphysema is based on pathophysiologic considerations and the observation that the degree of heterogeneity is a predictor of short-term functional improvement [5, 10, 12].

Problems occur with the emphysema morphology nomenclature, and different authors often use a different terminology. Wisser and associates [11] apply the term "homogeneous emphysema" in contrast to "bullous emphysema," whereas we use it for emphysema without any heterogeneity. A consensus with respect to emphysema morphology is necessary to compare functional results after LVRS between different centers. Several groups have developed and applied sophisticated methods to classify and grade emphysema as assessed by CT scan of the chest. Because the applicability is of limited value in clinical practice, we designed a simplified classification that can be used reliably by clinicians [5].

Improvement in FEV₁ has drawn most attention from the reports on LVR operations [13–15]. However, because the main aim is to relieve symptoms, the outcome should focus more on quality of life. Patients unable to do simple activities of daily life because of severe dyspnea could experience improvement in quality of life despite a small improvement in lung function. Less dramatic improvement of lung function in patients with homogeneous and intermediately heterogeneous morphology must be weighed against those subjective gains. The improvement in dyspnea might be related to the improved elastic recoil and the decreased functional residual capacity, which could increase the diaphragm fiber length that allows the diaphragm to generate more pressure for a given neural output [16, 17]. Not only were FEV₁ (% predicted) and dyspnea (Medical Research Council score) improved in all three emphysema type groups, but the parameters of hyperinflation, such as RV (% predicted) and the RV/TLC quotient, in homogeneous and heterogeneous emphysema patients were also improved up to 2 years after LVR operation. However, which lung function variable correlates best with symptomatic improvement after LVR operation is not yet determined [15].

Gradual decline of FEV₁ was observed in all three groups and averaged 63 to 194 mL per year or 1.9% to 5.7% of predicted FEV₁ per year. These decreases are comparable to the 160 mL per year or 5% predicted FEV₁ decrease per year reported by Gelb and colleagues [18], who recorded 2-year results after bilateral thoracoscopic LVR operations in 12 patients with heterogeneous emphysema. Data from other studies [2, 7, 14] suggest the same range. Follow-up results of the first 20 patients after LVRS by median sternotomy by Cooper and associates [19] suggested an FEV₁ decrease that was at least as favorable as ours from the present report.

Neither the published data nor our data allow conclusions to be drawn on the contribution of LVRS on naturally occurring decreases in FEV₁. In advanced emphysema, FEV₁ decline might be biased by the survivor effect; ie, patients with very low FEV₁ survive, only if they preserve their FEV₁. They seem to fare better in terms of FEV₁ decline than patients with higher FEV₁ [20]. This effect might account for falsely observed or interpreted differences between groups and underlines the difficulty in interpreting low FEV₁.

Overall mortality rates differed between the three groups, and the rate was lowest in the markedly heterogeneous morphology group. Whether lower lung functional status preoperatively or less profit by LVRS correlates with different survival outcomes remains undetermined and needs further analysis. The question of whether survival in general is influenced by LVRS cannot yet be answered. The importance of this consideration, however, is relative in light of a treatment that is intended to improve disabling dyspnea.

We chose the restrictive study design of closed groups in order to analyze the same individual’s data at different time points up to 2 years postoperatively. Subtle data trends such as decline of lung function could be studied more reliably.

Comparisons between each study group and the entire cohort showed only statistically insignificant differences in important outcome variables, such as FEV₁, RV, and TLC as the percentage of predicted value, RV/TLC quotient, as well as 6-minute walking distance and modified Medical Research Council dyspnea score. However, a bias in patient selection toward proposing LVRS preferentially and possibly earlier to candidates with more heterogeneous emphysema might have occurred, as results of several centers including ours were most convincing in that patient group [5, 10, 21, 22]. It might partly explain differences in survival, if patients had more severe lung-function limitations. There was a trend, but no significant difference, in FEV₁ (% predicted) and RV/TLC, as shown in Table 1. Although major selection bias did not occur, the clinical significance of those subtle differences can not be ruled out completely. Treatment, on the other hand, could differ between groups. Quantification of the amount of resected material is intricate [5], and a missing structurally defined target area in homogeneous emphysema could also have contributed to less, or less favorable, resection in that patient group, and consequently to less benefit in terms of FEV₁, which could result in survival differences [23, 24].

Our data show a functional and subjective benefit that was statistically and clinically significant in patients with homogeneous and intermediately heterogeneous emphysema, as well as in patients with marked heterogeneity. The applied validated morphologic classification system was an important predictor of surgical outcome [5]. Whereas clinical outcome in terms of Medical Research Council dyspnea score was not different between the groups during the follow-up period, functional outcome at 24 months and survival could be predicted by morphology. Efforts to unify emphysema nomenclature and classification, especially in regard to LVR operation, should be undertaken to enable comparison of results between centers and to make patient selection more appropriate.

	Acknowledgments

 
Supported by grant no. 3200-043358;95.1 from the Swiss National Science Fund and by a grant from the Zürich Lung League.

	Footnotes

 
This article has been selected for the open discussion forum on the STS Web site: http://www.sts.org/section/atsdiscussion/

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