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Ann Thorac Surg 1996;62:1588-1597
© 1996 The Society of Thoracic Surgeons

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Original Articles: General Thoracic

Extended Indications for Lung Volume Reduction Surgery in Advanced Emphysema

Divisions of Cardiothoracic Surgery and Pulmonary Medicine, Columbia University College of Physicians and Surgeons, New York, New York

	Abstract

Top Footnotes Abstract Introduction Material and Methods Results Comment References

 
Background. Lung volume reduction surgery has shown early promise as a palliative therapy in severe emphysema. Selection of potential candidates has been based on certain functional and anatomic criteria, and a variety of operative contraindications have been proposed.

Methods. Over 15 months, we performed lung volume reduction surgery in 85 patients selected on the basis of severe hyperinflation with air trapping, diaphragmatic dysfunction, and disease heterogeneity. Patients were not excluded on the basis of severe hypercapnia, steroid dependence, profound pulmonary dysfunction, or inability to complete preoperative rehabilitation.

Results. We observed significant improvements in pulmonary function, exercise capacity, and dyspnea, with an acceptable 30-day perioperative mortality of 7% and actuarial survival of 90% and 83% at 6 and 12 months, respectively. In each "high-risk" group, perioperative mortality, actuarial survival to 1 year, and functional results were equivalent, and in some cases superior, to those in the corresponding "low-risk" patients.

Conclusions. Severe hypercapnia, steroid dependence, profound pulmonary dysfunction, and inability to complete preoperative rehabilitation do not preclude successful lung volume reduction surgery and should not be regarded as absolute exclusionary criteria.

	Introduction

Top Footnotes Abstract Introduction Material and Methods Results Comment References

 
A variety of surgical procedures have been designed in the past century to correct anatomic and physiologic derangements thought to be responsible for respiratory dysfunction in patients with emphysema. These have included such diverse operations as tracheostomy, autonomic denervation, pneumoperitoneum, costochondrectomy, thoracoplasty, and bullectomy [1, 2]. Volume reduction surgery was originally conceived in the 1950s by Dr Otto Brantigan and his associates [3], who believed that loss of elastic recoil was responsible for expiratory airway collapse in emphysema and that excision and plication of lung tissue could restore circumferential traction on small airways. However, frequent complications related to prolonged air leaks and high early mortality resulted in abandonment of the technique. Recently, a modern version of this operation has been developed by Cooper and associates [4], who introduced technical modifications such as the buttressing of staple lines with bovine pericardial strips [5] and bilateral parenchymal reduction via median sternotomy.

Early reports suggest that in properly selected patients, lung volume reduction surgery (LVRS) can provide significant improvements in respiratory function and dyspnea with low perioperative morbidity and mortality [4]. Presently, indications for LVRS include disabling dyspnea associated with certain anatomic characteristics believed to predict success, such as hyperinflation, diaphragmatic dysfunction, and heterogeneous disease distribution. Although all potential candidates for LVRS are by definition at high operative risk due to severe respiratory dysfunction, certain characteristics have been considered as relative or absolute contraindications to the procedure. These "high-risk" categories include severe hypercapnia, high-dose steroid dependence, profound respiratory compromise, inability to participate in preoperative rehabilitation, coexistent thoracic tumors, and prior thoracic operation [1, 4].

Unfortunately, there has been little evaluation of the relative risks of mortality and treatment failure associated with LVRS in any of the above "high-risk" patient populations. This fact, coupled with the dismal prognosis associated with standard medical therapy of end-stage emphysema [6–8], led us to question the importance of these contraindications. Fourteen months ago, we began a prospective trial of LVRS for severe emphysema at our institution. We have attempted to define the safety and efficacy of this procedure and those preoperative screening parameters that would help identify which patients would benefit most (and least) from volume reduction.

	Material and Methods

Top Footnotes Abstract Introduction Material and Methods Results Comment References

 
Patient Selection and Demographics
Two hundred thirty patients with end-stage emphysema and progressive disabling dyspnea were evaluated for LVRS between August 1994 and October 1995. Operative candidates were selected on the basis of hyperinflation, poor diaphragmatic excursion, pulmonary perfusion and ventilation deficits, and significant functional disability. Patients with morbid obesity, chronic bronchitis or excessive sputum production, metastatic cancer, continued or recent cigarette smoking, or less than severe functional disability were excluded from consideration. Because medical therapy (the only available therapeutic alternative) is associated with poor long-term quality of life and survival [9], we have not established other absolute contraindications. Accordingly, patients with severe hypercapnia (arterial carbon dioxide tension [pCO₂] >55 mm Hg), high-dose steroid dependence (10 mg prednisone/day), advanced respiratory dysfunction (forced expiratory volume in 1 second [FEV₁] <500 mL), inability to complete preoperative rehabilitation, and intrathoracic neoplasms have not been categorically excluded.

A total of 85 patients underwent LVRS for end-stage emphysema between October 1994 and December 1995. Informed consent was obtained in all cases. Fifty patients (59%) were female, 59 (69%) dependent on continuous supplemental oxygen, and 48 (56%) on regular doses of oral prednisone. Twenty-six patients (31%) had a daily steroid requirement greater than or equal to 10 mg of prednisone. Mean age was 64 years, with a range of 45 to 80 years. Thirty-one patients (36%) had arterial pCO₂ greater than 45 mm Hg, and 35 (41%) were unable to undergo complete preoperative rehabilitation. Nine patients (11%) had arterial pCO₂ greater than 55 mm Hg. During initial evaluation, 15 patients were found to have intrathoracic neoplasms. Of these, 9 met criteria for LVRS and underwent operation with simultaneous tumor resection.

Preoperative Assessment
RADIOGRAPHIC.
Evaluation included inspiratory and expiratory posteroanterior and lateral chest radiographs as well as inspiratory and expiratory chest computed tomographic scans. In some patients, computed tomographic scans underwent computer-assisted densitometric analysis, allowing objective grading of degree and distribution of parenchymal destruction. Quantitative ventilation-perfusion scans with xenon washout studies were obtained in all patients, and left heart catheterization was performed in patients with suspected coronary artery disease.

PHYSIOLOGIC.
Assessment included standard pulmonary spirometry, including measurement of FEV₁, forced vital capacity (FVC), total lung capacity, residual volume, and maximal voluntary ventilation, as well as lung volume determinations by helium dilution and body plethysmography [10]. Arterial blood gas analysis, quantitative nuclear ventilation-perfusion scan with xenon washout, cardiopulmonary stress testing, and 6-minute walk test were also performed. The difference between total lung capacity determined by helium dilution and body plethysmography was used as an estimate of lung volume not participating in gas exchange (trapped gas volume).

DEGREE OF DYSPNEA.
Patients were asked to subjectively classify their degree of dyspnea according to the modified Medical Research Council dyspnea index [6]. This screening tool grades the degree of dyspnea on a scale ranging from 0 to 5. Grade 0 represents no functional impairment, and grade 5 represents dyspnea at rest:

• 0 = No dyspnea except with strenuous exertion
  
• 1 = Dyspnea while walking uphill
  
• 2 = Stops for breath while walking on the level
  
• 3 = Stops for breath every 100 yards or every few minutes
  
• 4 = Housebound/breathless while dressing
  
• 5 = Dyspnea at rest
  

"High-Risk" Groups
For purposes of analysis, four patient groups possessing characteristics considered contraindications for operation were identified. These "high-risk" groups were composed of patients with (1) severe hypercapnia, defined as arterial pCO₂ greater than 55 mm Hg, (2) steroid-dependence, with a steroid requirement equivalent to or greater than 10 mg prednisone daily, (3) profound pulmonary dysfunction, or FEV₁ less than 500 mL, and (4) inability to complete preoperative rehabilitation (Table 1). Functional results and actuarial survival in each of these groups were compared with those in each of the corresponding "low-risk" patient cohorts.

Statistical Analysis
Data were analyzed using SAS system software (SAS Institute, Inc, Cary, NC). Kaplan-Meier product limit estimates were used to graphically display survival after operation, providing actuarial estimates and 95% confidence intervals. The paired Student's t test was used for analyzing the relationship between preoperative and postoperative data. The Wilcoxon rank-sum test, the nonparametric analogue of the two-sample t test, was used to compare differences in percent change in FEV₁ and FVC and absolute change in 6-minute walk (ft) and dyspnea index (Medical Research Council units) in the various "high-risk" groups. All p values are reported without corrections for multiple comparisons, and p less than 0.05 is considered significant.

Operative Technique
Early in our experience, we used thoracotomy for unilateral reductions and median sternotomy for bilateral reductions. Median sternotomy was initially chosen for bilateral volume reduction because of its ability to provide bilateral apical exposure with low morbidity, especially with respect to chest wall mechanics. We became concerned, however, about its use in patients at risk for sternal wound dehiscence and infection, such as those with severe malnutrition or steroid dependence, and in patients who required better exposure of the lower lobes. Therefore, the most recent 44 patients have been approached via bilateral thoracosternotomy, or clamshell incision, which we believe allows superior simultaneous bilateral thoracic exposure with minimal risk of wound complications. Because the clamshell incision has become our preferred approach, it will be described below.

After placement of a thoracic epidural catheter, the patient is placed in the supine position and intubated with a double-lumen endotracheal tube. The arms are abducted laterally, the skin is incised in the inframammary crease in a curvilinear fashion, and bilateral thoracosternotomy is performed through the fourth intercostal space. The mediastinum is then dissected free from the sternum, fully exposing both lungs, which are easily mobilized by division of the inferior pulmonary ligaments. With the aid of alternating lung deflation, bilateral LVRS is performed, using GIA stapling devices (U.S. Surgical, Inc, Norwalk, CT; Ethicon, Inc, Somerville, NJ) lined with bovine pericardial strips (BioVascular, Inc, St. Paul, MN) to minimize air leakage. Extent of resection is guided by preoperative radiographic and physiologic studies. After staple lines are meticulously checked for major leaks and the lungs are carefully reexpanded, bilateral apical thoracostomy tubes are placed. If significant air leaks or space problems are anticipated, apical pleural tents are created. The chest is closed with pericostal sutures, two sternal wires are placed to avoid sternal override, and the soft tissue and skin are approximated in layers with absorbable sutures. The patient is extubated in the operating room or shortly after arrival to the intensive care unit, and epidural bupivicaine analgesia is carried out for the first few days.

	Results

Top Footnotes Abstract Introduction Material and Methods Results Comment References

 
Mean age was 64 ± 8 years, and age ranged from 45 to 80 years. Fifty patients (59%) were female, 59 (69%) O₂ dependent, and 48 (56%) receiving regular doses of prednisone. The proportion of patients composing each of the "high-risk" groups is listed in Table 2. Preoperative pulmonary function in the patients undergoing operation was severely impaired, and the average 6-minute walk distance and dyspnea index corresponded to profound disability and diminished quality of life (see Table 2). These parameters were similarly or more profoundly abnormal in the "high-risk" patient groups, which will be addressed separately in subsequent sections. Furthermore, lung volume measurements revealed significantly elevated total lung capacity, residual volume, and trapped gas volume, with increased residual volume/total lung capacity ratio, a measure inversely proportional to the vital capacity (Table 3).

There were a total of six deaths within 30 days of operation and five postdischarge deaths (1.5 to 7 months postoperatively), corresponding to a 7% perioperative mortality rate and an actuarial survival of 95%, 90%, and 83% at 1, 6, and 12 months, respectively (Fig 1). Of the perioperative deaths, four were due to respiratory failure, and two of these occurred in patients with previous thoracic operations in whom multiple persistent bronchopleural fistulas developed. One perioperative death was due to peritonitis secondary to duodenal ulcer perforation and another to a cerebrovascular accident in patients with otherwise satisfactory results. Of the five late deaths, two were secondary to sudden death in patients doing well at home. One other patient died of progressive respiratory failure and 1 succumbed to sepsis associated with a Heimlich valve infection. Finally, 1 patient died of pancreatic carcinoma diagnosed 5 months after LVRS.

View larger version (18K): [in this window] [in a new window]   Fig 1. . Kaplan-Meier actuarial survival (all patients).

View larger version (21K): [in this window] [in a new window]   Fig 2. . Kaplan-Meier actuarial survival: high- versus low-risk groups (severe hypercapnia). (pCO2 = carbon dioxide tension.)

View larger version (21K): [in this window] [in a new window]   Fig 3. . Kaplan-Meier actuarial survival: high- versus low-risk groups (steroid dependence). (Pred = prednisone.)

View larger version (21K): [in this window] [in a new window]   Fig 4. . Kaplan-Meier actuarial survival: high- versus low-risk groups (severe pulmonary dysfunction). (FEV1 and FEVpre = preoperative forced expiratory volume in 1 second.)

Of patients with at least 3 months of follow-up, 26 did not complete preoperative rehabilitation. Postoperative FEV₁, FVC, and 6-minute walk improvements paralleled those of patients who had completed preoperative rehabilitation and, interestingly, rehabilitation failures demonstrated a significantly greater improvement in degree of dyspnea (see Table 6). Only one of six perioperative deaths occurred in the rehabilitation failure group (see Table 7), and actuarial survival at 6 and 12 months was not significantly different from that in patients completing preoperative rehabilitation (Fig 5).

View larger version (21K): [in this window] [in a new window]   Fig 5. . Kaplan-Meier actuarial survival of high- versus low-risk groups (preoperative rehabilitation [Rehab]).

	Comment

Top Footnotes Abstract Introduction Material and Methods Results Comment References

Much less clear, however, have been the preoperative characteristics associated with surgical therapeutic failure. Surgical contraindications that were originally proposed, such as severe hypercapnia, significant steroid dependence, profound pulmonary dysfunction, inability to complete preoperative rehabilitation, advanced age, and previous thoracic operation, were reasonably based on classic principles and experience with other thoracic operations. Early to mid-term experience with LVRS, however, has revealed several significant differences from other thoracic procedures, and at the very least has redefined the minimum level of pulmonary functional capacity required for successful pulmonary resection. This latter principle was illustrated by our success in effecting thoracic tumor resections in 9 patients with levels of pulmonary dysfunction traditionally considered incompatible with postoperative survival.

The importance of complete lung mobilization for adequate sizing and targeting in volume reduction and our experience in thoracic reoperations suggested that volume reduction in patients with previous ipsilateral thoracotomy could not be effectively performed without prohibitive technical risks. Deaths due to lung trauma and massive air leaks in 2 such early patients confirmed this concern, and we have subsequently adhered to this operative contraindication. Advanced age has been proposed as a relative contraindication for a variety of medical and surgical therapies. Although we did not exclude patients on the basis of age, only 6 patients older than 75 years met selection criteria and underwent volume reduction. There were two deaths in this group, and functional results in the 4 remaining patients were comparable with those in younger patients. Because the number of patients in this group is small, it remains to be determined whether favorable results can be achieved in patients with advanced age without a prohibitively high mortality. Further refinement of preoperative selection criteria may be able to exclude those elderly patients who are at increased risk of perioperative morbidity and mortality.

Hypercapnia has classically been associated with increased disease severity in emphysema [6]. Accordingly, we observed more severe reductions in FEV₁, FVC, and 6-minute walk distance and well as increased dyspnea in patients classified as severely hypercapneic. Nonetheless, perioperative mortality, 1-year actuarial survival, and functional results, including improvements in dyspnea, were as impressive in this group as in patients with lower pCO₂ levels. Similarly, patients classified with profound pulmonary dysfunction (FEV₁ < 500 mL) suffered no increased risk of early or late mortality and had equally remarkable improvements in FEV₁, 6-minute walk, and dyspnea, and actually demonstrated a significantly greater improvement in FVC than patients with higher preoperative FEV₁. These results demonstrate that these two very high risk groups need not be excluded from the benefits of LVRS.

It is well established that steroid dependence is associated with a variety of adverse effects in surgical patients, from impaired wound and anastomotic healing to systemic immunosuppression and increased infection. With respect to LVRS, an additional concern exists regarding the association of steroid responsiveness and primary airway disease [13]. Patients in whom it is not possible to wean steroid therapy may have a significant component of primary airway and inflammatory disease, pathologic processes not expected to respond to volume reduction. However, because many emphysematous patients seem to have some element of primary airway obstruction, many patients who meet positive selection criteria for volume reduction are in fact dependent on steroids. The low perioperative mortality and excellent functional results in this subgroup of patients in our series are encouraging. Although early actuarial survival estimates are favorable, it remains to be seen whether these patients have a more aggressive progression of disease or decreased survival at greater than 1 year. A factor that may influence long-term survival may be the ability to wean and eliminate steroid therapy postoperatively, as steroids are associated with a variety of unrelated medical causes of morbidity and mortality.

Although our preoperative regimen included that a rehabilitation program be initiated, many patients could not comply on the basis of severe functional disability. A smaller group of patients did not have access to appropriate rehabilitation facilities. Finally, the death of 3 severely compromised patients during preoperative rehabilitation prompted our withdrawal of this requirement from a few patients deemed too profoundly ill to undergo the rehabilitation program. Notwithstanding these considerations, all patients were required to undergo formal postoperative rehabilitation, and in fact most survivors were discharged directly to a nearby rehabilitation facility.

In our series, mortality, actuarial survival, and improvements in pulmonary function were not influenced by the ability to complete preoperative rehabilitation. An interesting observation was a trend toward greater increases in 6-minute walk distance in patients classified as rehabilitation failures, although this discrepancy did not quite meet statistical significance. Extremely significant, however, was the more pronounced improvement in dyspnea index among rehabilitation failure patients. These findings may be explained by realizing that the patient with severe emphysema suffers from both primary pulmonary dysfunction and secondary physical debility due to severe deconditioning. In patients who can participate in preoperative rehabilitation, some improvement in physical functional capacity can be expected on the basis of reconditioning. It may be that patients not completing preoperative rehabilitation programs did not gain this preoperative functional improvement and consequently, despite similar preoperative pulmonary function parameters, demonstrated lower preoperative 6-minute walk distances. Postoperatively, most surviving patients enjoyed improvements in pulmonary function and severity of dyspnea, and participation in postoperative rehabilitation allowed patients without preoperative rehabilitation to "catch up," achieving similar levels of functional capacity at 3 to 6 months. Thus, although preoperative rehabilitation can certainly be expected to improve the general condition of the preoperative patient, our experience did not identify differences in perioperative mortality, actuarial survival, or 3- to 6-month functional results in patients unable to meet this requirement. Because it is important to maximally prepare patients for the rigors of operation and postoperative recovery, it is prudent to strongly recommend that patients initiate rehabilitation programs preoperatively. However, given our findings, patients who meet positive selection criteria for volume reduction but are unable to undergo rehabilitation should not be denied the opportunity for surgical therapy.

In summary, although various preoperative patient characteristics pose increased theoretical risks for operative mortality or therapeutic failure, several of these do not significantly affect early clinical outcomes. Our experience supports the application of LVRS to properly selected patients regardless of the level of hypercapnia, steroid dependence, pulmonary dysfunction, or preoperative rehabilitation status. It must be stressed that our results are preliminary and longer follow-up periods will be required to more confidently eliminate these characteristics as potential causes of late mortality or therapeutic failure.

	Footnotes

Top Footnotes Abstract Introduction Material and Methods Results Comment References

 
Presented at the Poster Session of the Thirty-second Annual Meeting of The Society of Thoracic Surgeons, Orlando, FL, Jan 29–31, 1996.

Address reprint requests to Dr Ginsburg, 161 Fort Washington Ave, Rm 310, New York, NY 10032.

	References

Top Footnotes Abstract Introduction Material and Methods Results Comment References

 

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