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Ann Thorac Surg 1996;62:994-999
© 1996 The Society of Thoracic Surgeons

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Original Articles: General Thoracic

Role of Lung Reduction in Lung Transplant Candidates With Pulmonary Emphysema

Divisions of Cardiothoracic Surgery and Pulmonary Medicine, University of Pittsburgh Medical Center, Pittsburgh, Pennsylvania

	Abstract

Top Footnotes Abstract Introduction Material and Methods Results Comment References

 
Background. The average waiting time for candidates for lung transplantation (LTx) with end-stage emphysema is 21 months with a 15% mortality. We hypothesized that lung reduction might offer an alternative to LTx.

Methods. Of 95 patients with end-stage emphysema evaluated by our LTx program, 45 were accepted for both lung reduction and LTx and 35 underwent lung reduction.

Results. All 35 patients survived lung reduction. Thirty patients had a follow-up of 3 months. There was a significant improvement (p < 0.05) of forced expiratory volume in 1 second (0.64 to 0.97 L), forced vital capacity (2.12 to 2.76 L), residual volume (5.62 to 4.26 L), maximum voluntary ventilation (28.1 to 38.5 L/min), 6-minute walk (904 to 1,012 feet), Borg dyspnea index (3.7 to 2.4), and arterial carbon dioxide tension (44.9 to 41.6 mm Hg). Twenty patients (66%) were removed from the LTx list due to their significant improvement (group A). Compared with the remaining 10 patients with 3 months of follow-up (group B), percent increase in forced expiratory volume in 1 second (70% in group A versus 27% in group B) and in forced vital capacity (41% group A versus 18% group B) and percent decrease in residual volume (26% group A versus 1.5% group B) were significantly better in group A (p < 0.01). Seven patients in group B were bridged to LTx; 6 of these patients (86%) had hypercarbia before lung reduction compared with 8 (40%) in group A (p < 0.05). All are alive after LTx: the forced expiratory volume in 1 second is 53% and the forced vital capacity is 64% of predicted.

Conclusions. Lung reduction is safe and effective in selected LTx candidates with end-stage emphysema and has the potential to provide an alternative to LTx. Long-term follow-up is warranted to confirm these results.

	Introduction

Top Footnotes Abstract Introduction Material and Methods Results Comment References

 
End-stage pulmonary emphysema (COPD) is the most common indication for lung transplantation (LTx); the 1-year survival after single LTx for COPD is 75% [1]. Due to a large mismatch between the number of LTx candidates and that of donor organs available, the average waiting time for LTx candidates with COPD at our institution is 18 to 24 months [2]. Although the 15% mortality while waiting for LTx in the COPD group is lower than in candidates with other disease processes, it is still significant [3].

Surgical therapy for COPD has been reintroduced in the recent years following on Brantigan's pioneering work [4]. Our group has been actively studying the thoracoscopic approach to lung reduction (LR) and we have found it associated with significant improvement in pulmonary mechanics and functional impairment [5]. We have demonstrated an increase in lung elastic recoil after LR and correlated it to enhanced expiratory flow rates, decreased lung hyperinflation, reduced end-expiratory intrathoracic pressures, and improved right ventricular systolic function [6]. The best candidates for LR in our experience appear to be those patients with moderate degree of functional impairment, heterogeneous disease with areas of relative preservation and hyperinflation, percent predicted diffusing capacity for carbon monoxide (DLCO) of more than 25 and an arterial carbon dioxide tension (PaCO₂) of less than 50 mm Hg.

Because the optimal operation for patients with COPD has not yet been determined, we hypothesized that LR might be beneficial in LTx candidates with COPD to reduce the mortality of the waiting period and improve their functional status, or as a potential alternative to LTx.

	Material and Methods

Top Footnotes Abstract Introduction Material and Methods Results Comment References

 
Patient Population
From July 1994 through December 1995, 95 patients with COPD were referred to and evaluated by the Lung Transplant Program at the University of Pittsburgh. All of these patients had severely impaired quality of life despite maximal medical therapy and disabling dyspnea at less than 50 yards of walking. Twenty-two of these patients were accepted for LTx but were turned down as LR candidates. Seven patients were denied LTx and were offered LR as the only surgical alternative. Twenty-one patients were turned down as candidates for both LTx and LR. Forty-five patients (47%) were accepted as candidates for LTx and/or LR; 3 of these patients received LTx before completing work-up for LR and 7 patients are currently waiting for LTx or LR.

Thirty-five patients of the 45 accepted for LTx/LR (78%) received LR and are the object of this study.

Evaluation Before Lung Transplantation
All patients underwent routine work-up for LTx. Our evaluation protocol was previously published [7]; selection criteria for LTx currently used at the University of Pittsburgh are as follows:

• Indications
  • End-stage pulmonary disease with
    
  • Projected life expectancy <2 years
    
  • New York Heart Association class III or IV
    
  
  
• Relative contraindications
  • Weight outside predicted ±10% range
    
  • Prednisone >10 mg every day or 20 mg every other day
    
  • Bilateral surgical pleurodesis
    
  
  
• Absolute contraindications
  • Physiologic age >65 y for single LTx; >60 y for double LTx
    
  • Psychosocial instability
    
  • Inadequate financial resources
    
  • Tobacco use within 1 y
    
  • Mechanical ventilation
    
  • Another life-limiting illness
    • Human immunodeficiency virus infection
      
    • Recent malignancy
      
    • Bone marrow failure
      
    • Liver failure (total bilirubin >2 mg/dL)
      
    • Renal failure (serum creatinine >2 mg/dL)
      
    • Left ventricular failure (left ventricular ejection fraction <0.35)
      
    • Significant coronary artery disease
      
    
    
  
  

Evaluation Before Lung Reduction
The protocol for LR evaluation at our center is as follows:

• Standard pulmonary function tests (forced vital capacity [FVC], FEV₁, FEV₁/FVC, maximum voluntary ventilation)
  
• Single breath DLCO
  
• Body plethysmography (total lung capacity, residual volume [RV], functional reserve capacity)
  
• 12-lead electrocardiogram and two-dimensional cardiac echocardiogram
  
• Routine blood work
  
• Posteroanterior and left lateral chest roentgenogram
  
• Computed tomographic scans of chest with density mask imaging
  
• Ventilation and perfusion scans
  
• Single-photon emission computed tomographic perfusion imaging
  
• Exercise capacity (6-minute walking [6MW] distance)
  
• Baseline dyspnea index and Borg dyspnea index
  Standard preoperative studies to evaluate patients with poor pulmonary reserve were performed. These include an electrocardiogram, routine blood work (arterial blood gases, complete blood cell count, serum chemistry profile, coagulation profile including prothrombin time, partial thromboplastin time, thromboplastin time, platelets). Standard posteroanterior and lateral chest radiography is done to confirm hyperinflation and no obvious infection, tumor, or other process that would exclude the patient from the surgical procedure.
  A two-dimensional Doppler echocardiogram is performed to assess global left and right ventricular function and to check for evidence of pulmonary hypertension, valvular incompetence, or both.
  Exercise capacity is tested with a 6MW using pulse oximetry [9] and a complete exercise study using stationary bicycle; this exercise study is used to confirm ventilatory limitation. A modified Borg dyspnea score is recorded immediately before and at completion of the 6MW.
  Standard pulmonary function tests were conducted 1 to 3 weeks before operation including spirometry to measure FVC, FEV₁, FEV₁/FVC, maximal voluntary ventilation and single breath DLCO. Body plethysmography is used to measure thoracic gas volumes (RV, total lung capacity, fractional reserve capacity). Values were compared with standard predicted measures [10–12].
  A chest computed tomographic scan is performed at full inspiration with 10-mm slices every 10 mm using a HiSpeed Advantage CT Scanner (General Electric, Milwaukee, WI) in the axial mode. High-resolution computed tomographic scans are obtained at 1 mm every 20 mm using a bone algorithm technique. Images are filmed at a window of 1,500 and a level of -600 HU. The General Electric Density Mask program highlights voxels from -910 to -1,024 HU, which corresponds to areas of emphysema. Once the optimal attenuation level to define areas of emphysema is determined for a particular scanner, the density mask assesses accurately the extent of emphysema and eliminates interobserver and intraobserver variability, having the advantage of determining the exact percentage of lung parenchyma showing changes consistent with emphysema [13].
  The nuclear medicine evaluation includes ventilation and perfusion lung scanning. Ventilation imaging is performed with 10 to 20 mCi of xenon 133. We use a high-resolution collimator and image with an 81-keV photopeak and a 20% window. Patients are imaged posteriorly in the upright position. The initial breath image is acquired for 100,000 counts or 30 seconds, whichever comes first. The equilibrium image is at 2 minutes of breathing the xenon. Equilibrium images in the posterior and both oblique posterior washout images for 30 seconds each for 5 minutes. For the perfusion scan, approximately 5 mCi of technetium 99m-macroaggregated albumin is administered slowly with the patient in the supine position. The patient is then positioned upright. Posterior, anterior, both lateral, both anterior oblique, and both posterior oblique projections are obtained for 1 million counts each using a high resolution collimator and a 140-keV photopeak and a 20% window. After planar imaging, single photon emission computed tomographic perfusion imaging is performed using a dual head gamma camera (BIAD, Trionix, Twinsburg, OH) with high resolution collimators [14]. The data are reconstructed into transaxial, sagittal, and coronal projections using a Hanning filter. Images are displayed in a rotating mode. The nuclear images are used to determine the side that has the worst ventilation and perfusion and to aid in determining the areas of lung to be resected.
  The daily experience with dyspnea is measured by use of the baseline dyspnea index. A health care provider selects from one to five grades of dyspnea based on a brief history. Several studies have documented the validity and reliability of this tool in patients with chronic respiratory disease [15]. In addition, patients were also categorized using the modified Borg scale that uses a subjective perspective to assess the extent of activity necessary to cause dyspnea; the higher the score, the worse the breathlessness.
  Inclusion and exclusion criteria for LR were as follows:
  • Inclusion criteria
    • End-stage diffuse emphysema
      
    • Severely impaired quality of life despite maximal medical therapy
      
    • Postbronchodilator FEV₁ of <30% predicted
      
    • Disabling dyspnea at <50 yards of walking
      
    
    
  • Exclusion criteria
    • Pulmonary hypertension (systolic pulmonary artery pressure >55 mm Hg)
      
    • Smoking history within last 3 months
      
    • Large bullae with compressive signs on chest computed tomograms
      
    • Morbid obesity (>1.5 lean body weight)
      
    • Unstable coronary artery disease
      
    • End-stage cancer
      
    • Nonambulatory
      
    • Ventilator-dependent
      
    
    
  
  Exclusion criteria included known pulmonary hypertension (systolic pulmonary artery pressure >55 mm Hg), history of smoking tobacco within the past 3 months, morbid obesity (>1.5 lean body weight), unstable coronary artery disease, end-stage cancer, nonambulatory, and ventilator-dependent patients. Patients who had previously undergone open thoracic surgical procedures on the side designated for unilateral LR were also excluded. Patients whose disease was characterized by large bullae with compressive signs on chest computed tomographic scan were excluded from the study. Patients were seen in consultation by the nutrition service for assessment of nutritional status. Patients taking more than 20 mg of prednisone/day were not eligible for operation until they were weaned below this level. Participation in a cardiopulmonary rehabilitation program was not required for inclusion in the study. Selection of patients was performed by a multidisciplinary team including thoracic surgeons, pulmonologists, radiologists, and transplant coordinators.
  Three months after operation, pulmonary function, diagnostic imaging, and the 6MW were repeated to evaluate the extent of improvement. Change in the degree of functional impairment after operation was determined using a transitional dyspnea index. This index measures the change from baseline in three categories: functional impairment, the magnitude of the task needed to evoke dyspnea, and the magnitude of the effort needed to evoke dyspnea. Scoring ranged from -9 (major deterioration) to +9 (major improvement) [5].
  

Surgical Technique
All LRs were performed with electrocardiographic monitoring, radial artery cannulation, and central venous access for monitoring of pulmonary artery pressure and cardiac output. An epidural catheter was placed to provide postoperative analgesia and also to augment the intraoperative anesthetic management.

Airway intubation was performed using a left-sided double-lumen endotracheal tube. Pulse oxymetry and end-tidal carbon dioxide monitoring was followed throughout the case.

Lung reduction was performed on the side most severely affected by the emphysematous process; in particular, the density mask images of the computed tomographic scan highlighted the areas of worst anatomic disease as well as zones of more normal lung, whereas the single photon emission computed tomographic perfusion study demonstrated zones of significant hypoperfusion. These areas were focused on during the resection, especially when the ventilation studies had shown washout abnormalities. When both lungs demonstrated an equal degree of parenchymal destruction, a bilateral approach was used with sequential thoracoscopic LR or bilateral LR through a median sternotomy [16].

Unilateral thoracoscopic LR was performed with the patient in lateral decubitus position. In the majority of cases, three to five ports were used for access. The thoracoscope was introduced into the chest through the seventh or eighth intercostal space at the mid to posterior axillary line. In three patients (8%) neodymium:yttrium-aluminum garnet laser ablation of emphysematous tissue was the sole modality of LR. In these patients areas of diffuse disease were diffusely scarified with the neodymium:yttrium-aluminum garnet laser set at 10 to 15 W in the noncontact mode. In 12 patients (35%), a combination of endostapler resection (for about 90% of the total volume reduction) together with sparing use of neodymium:yttrium-aluminum garnet laser was used. Laser was used mainly in areas of diffuse bullous formation near the pulmonary hilum or located at angles difficult to reach with the endostapler. Endostapler resection was the preferred method of LR in 20 patients (57%); according to the extent of the area to be resected we used either a 30-mm (United States Surgical Corp, Norwalk, CT) or a 60-mm (Ethicon Endo-Surgery, Cincinnati, OH) stapler. The staple line was buttressed with bovine pericardium.

The goal of LR was to reduce the volume of the lung by 25%. The extent of resection was dictated by the preoperative perfusion studies. Strips of lung tissue were resected along the edges of each lobe such as along the fissures or anteriorly and posteriorly to the apex of the upper lobe and along the basal segments or superior segment of the lower lobe. Lung was periodically inflated during the procedure to evaluate the extent of resection accomplished in each lobe of the lung so as to avoid overresection. Staple lines were buttressed with bovine pericardium. At the end of the procedure three chest tubes were placed into the pleural cavity through the intercostal access ports used during the procedure. No pleural abrasion or pleurectomy was performed. Lungs were reexpanded and ventilation was reestablished aiming to keep peak airway pressure at the minimum required to achieve an adequate tidal volume (<30 mm Hg). Chest tubes were placed on -10 cm of water suction in the operating room and adjusted thereafter.

Statistical Analysis
Data were expressed as mean ± standard deviation. Student's t test for paired samples was used to compare matched variables. Fisher's exact test was used to assess differences between risk groups. A p value of less than 0.05 was considered significant.

The protocol for this study was approved by the Institutional Review Board of the University of Pittsburgh and all the patients provided written informed consent.

	Results

Top Footnotes Abstract Introduction Material and Methods Results Comment References

 
Thirty-five patients underwent LR between July 1994 and December 1995. There were 21 men and 14 women; age was 57.8 ± 7.2 years (range, 39 to 68 years). Seven patients had COPD secondary to ₁-antitrypsin deficiency. Twenty-eight patients (80%) were taking oral steroids and 29 patients (83%) were on supplemental oxygen. Hypercarbia (PaCO₂ 45 mm Hg) was present in 18 patients (51%) and 10 patients had a PaCO₂ of more than 50 mm Hg (29%). The percent predicted postbronchodilator FEV₁ was 22% ± 6.2% and the FEV₁/FVC ratio was 0.28 ± 0.06. Baseline dyspnea index was 0.9 ± 0.4 indicating severe functional impairment. The 6MW distance was 863 ± 292 feet and the modified Borg dyspnea index was 3.94 ± 1.9.

Operative procedures (Table 1) were: unilateral thoracoscopic LR in 26 patients (74%), bilateral thoracoscopic LR in 5 patients (14%) of which 3 were done in one stage and 2 in two stages, and bilateral LR through a median sternotomy in 4 patients (12%). All patients survived LR and all patients are currently alive with a follow-up of 13.6 ± 3 months. The length of stay in hospital after LR was 18 ± 10 days (range, 7 to 48 days). Chest tubes were in place for 16 ± 11 days (range, 4 to 50 days). The most common complication was prolonged (>5 days) air leak:

Follow-up testing at 3 months was complete in 30 patients (86%); 2 patients refused follow-up testing and 3 patients had LR performed within 3 months of the closure of this study (12/95).

Pulmonary Function Studies
Compared with pre-LR values, the 3-month follow-up after LR (Table 2) demonstrated an improvement of 330 mL in FEV₁: from 0.64 L (22% predicted) to 0.97 L (35% predicted) (p < 0.0001), representing a 51% increase. Similarly, 3 months after LR FVC increased from 2.12 L (53% predicted) to 2.76 L (71% predicted) (p < 0.001) for a 30% increase. The RV decreased from 5.62 L (265% predicted) to 4.26 L (214% predicted) (p < 0.001): a 25% decrease. There was a trend toward reduction of total lung capacity, from 7.8 L to 7.2 L, that did not reach statistical significance (p = 0.07). The DLCO did not change significantly after LR and passed from 40% predicted to 42.9% predicted (p = 0.2). Maximum voluntary ventilation increased from 28.1 L/min to 38.5 L/min (p < 0.01). Room air PaO₂ did not change after LR (64.4 mm Hg to 65.5 mm Hg; p = 0.3). There was a significant decline in PaCO₂ from 44.9 mm Hg to 41.6 mm Hg (p < 0.05).

Lung Reduction as Alternative to Lung Transplantation
In 20 patients (57%) subjective and objective results after LR were remarkable (group A: "LR as Alternative to LTx" in Table 3); these patients remained on the LTx list only because of uncertainties regarding the long-term efficacy of this procedure. The increase in FEV₁ in group A was 70% ± 38%, the increase in FVC was 41% ± 18% and the decrease in RV was -26% ± 12%. Patients in group A were compared with 10 patients (group B) that had 3-month follow-up testing after LR, but that were considered "Not Alternative to LTx." The increase in FEV₁ (70% in group A versus 27% in group B) and in FVC (41% group A versus 18% group B) and the decrease in RV (-26% group A versus -1.5% group B) were significantly better in group A compared with group B (p < 0.01). Furthermore the transitional dyspnea index at 3 months was significantly better in group A (1.82) compared with group B (1.17).

Seven patients in group B underwent subsequent LTx and 3 remain on the waiting list for LTx.

Lung Reduction as Bridge to Lung Transplantation
Seven patients (20%) underwent LTx after LR. The interval between LR and LTx was 11 ± 4 months. All LTx were single lung transplants. Four patients (57%) had LTx on the same side as LR; adhesions were managed with the aid of an argon beam coagulator. All patients are alive after LTx with a follow-up of 6.7 ± 5 months. The FEV₁ after LTx is 1.5 ± 0.2 L (53.4% predicted) and improved significantly compared with pre-LR FEV₁ in the same patients (0.63 ± 0.2 L; p < 0.0001). The FVC is 2.6 ± 0.5 L (64% predicted), but we did not observe a significant improvement compared with pre-LR FVC (2.13 ± 1 L; p = not significant). Compared with the 30 patients with 3 months of follow-up after LR, FEV₁ was significantly better after LTx (1.51 ± 0.2 L versus 0.97 ± 0.38 L; p < 0.001).

Six of these patients (86%) had pre-LR hypercarbia (PaCO₂ >45 mm Hg) compared with 8 patients (40%) in group A (p < 0.05).

Medium Term (>6 months) Follow-up Results After Lung Reduction
Seven patients (20%) had follow-up testing performed 6 or more months after LR; compared with their pre-LR tests, they still showed a significant increase in FEV₁ (0.77 to 1.1 L; p < 0.05), FVC (2.49 to 3.54 L; p < 0.01), and a decrease in RV (6.1 to 4.5 L; p < 0.01).

	Comment

Top Footnotes Abstract Introduction Material and Methods Results Comment References

 
Lung disease secondary to emphysema is a major cause of morbidity and disability and is the fifth leading cause of death in the United States and in Europe [17]. Until recently LTx, either single or bilateral, was the only therapeutic option for end-stage COPD patients [18].

Brantigan [4] in 1957 proposed the idea of resecting nonfunctional parts of emphysematous lung to improve the function of the remaining lung. The rationale of lung reduction is to remove severely diseased and hyperexpanded lung thereby improving lung elastic recoil, decreasing the thoracic hyperinflation, and improving chest and diaphragmatic function.

Recently, encouraging early results with various approaches to LR in diffuse pulmonary emphysema have been reported [19–21]. Our group has gained a significant experience with video-assisted thoracic surgery (VATS) [22] and naturally we extended it to COPD patients. With VATS it is possible to approach all parts of the lung, including posterior and inferior aspects with better control of adhesions. Video-assisted thoracic surgery also permits greater flexibility in applying the endostapler in any region of the lung. Our initial experience with unilateral VATS LR showed significant improvements in FVC, FEV₁, RV, DLCO, and 6MWD; the use of laser and the combination of hypercarbia and reduced DLCO were identified as predictors of poor outcome [5]. Since then we have abandoned the use of laser as the sole modality of LR and we have used it very sparingly only as a complement to staple LR. Recently we analyzed our experience with bilateral VATS LR; when results were compared with unilateral VATS LR we found that bilateral LR produced more extensive improvements in function [23]. Since September 1995 bilateral LR has become our approach of choice.

End-stage COPD is currently the principal indication for LTx [1]. The shortage of donor organs greatly limits the number of patients that can benefit from this therapy. Furthermore, there is a long waiting period that is continuously expanding; the mortality while waiting is 15%. As we gained experience with LR, we initiated a program aimed to identify those LTx candidates with COPD that could benefit from LR. Our hypothesis was that LR could serve as a temporizing measure in some patients [24] or as an alternative to LTx in others.

Thirty-five LTx candidates with end-stage COPD received LR. The severity of the functional status of these patients is reflected in the poor mean percent predicted FEV₁ of 22% (versus 30% in our general LR population) [5], mean percent predicted RV of 265% (versus 239% in the general LR population). The mean FEV₁/FVC ratio was 0.28 and the baseline dyspnea index was 0.9 (versus 1.3 in the general LR population). We observed no mortality and no major morbidity. Functional results have been gratifying with significant improvement of FEV₁, FVC, RV, maximum voluntary ventilation, 6MW, PaCO₂, and Borg dyspnea index. Twenty patients (group A) experienced such significant symptomatic relief from LR that they do not wish to be considered for LTx at this time. These patients were also found to have experienced excellent objective improvement in pulmonary function. Our medium-term results (>6 months) after LR in a small sample of patients suggests a lasting effect of LR.

Ten patients (group B) experienced variable symptomatic or objective changes after LR but wished to remain as active transplant candidates; 7 patients underwent successful LTx an average of 11 months after LR. Six of these 7 patients (86%) had pre-LR hypercarbia, a recognized risk factor for LR [5], compared with 8 of 20 patients in group A (p < 0.05).

In conclusion, in our experience LTx candidates with end-stage COPD can be managed by a strategy that selects the optimal surgical option based on extensive emphysema work-up. Hypercarbia appears to be a risk factor for suboptimal results after LR and necessity for LTx. On the basis of our medium-term follow-up results, we believe that LR has the potential to offer an alternative to LTx in selected candidates. Longer term follow-up is warranted to define the duration of the benefit.

	Footnotes

Top Footnotes Abstract Introduction Material and Methods Results Comment References

Address reprints requests to Dr Zenati, Division of Cardiothoracic Surgery, University of Pittsburgh Medical Center, 200 Lothrop St, Suite C-700 PUH, Pittsburgh, PA 15213.

	References

Top Footnotes Abstract Introduction Material and Methods Results Comment References

 

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This Article Abstract 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): Marco Zenati Robert J. Keenan Rodney J. Landreneau Bartley P. Griffith Permission Requests Citing Articles Citing Articles via HighWire Citing Articles via Google Scholar Google Scholar Articles by Zenati, M. Articles by Griffith, B. P. Search for Related Content PubMed PubMed Citation Articles by Zenati, M. Articles by Griffith, B. P.