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Ann Thorac Surg 1998;65:314-318
© 1998 The Society of Thoracic Surgeons

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Original Articles: General Thoracic

Lung Reduction Operation and Resection of Pulmonary Nodules in Patients With Severe Emphysema

Division of Cardiothoracic Surgery, Columbia University College of Physicians and Surgeons, Columbia-Presbyterian Medical Center, New York, New York USA
Division of Pulmonary Medicine, Columbia University College of Physicians and Surgeons, Columbia-Presbyterian Medical Center, New York, New York, USA

Accepted for publication July 29, 1997.

Dr Ginsburg, Columbia-Presbyterian Medical Center, 161 Fort Washington Ave, Rm 310, New York, NY 10032.

	Abstract

Top Abstract Introduction Material and Methods Results Comment References

 
Background. Severe pulmonary dysfunction has been considered a relative contraindication to surgical resection in patients with solitary pulmonary nodules. We report our initial experience with the combined use of lung volume reduction operation and tumor resection in this patient population.

Methods and Patients. Between January 1995 and July 1996, 14 patients underwent combined lung volume reduction operation and pulmonary nodule resection. Ten (71%) patients were oxygen dependent, 5 (36%) had a room air partial pressure of carbon dioxide 45, and 5 (36%) were steroid dependent preoperatively. Mean preoperative pulmonary function tests included a forced expiratory volume in 1 second of 680 ± 98 mL (24% ± 5% predicted), forced vital capacity of 54% ± 5% predicted, and a forced expiratory volume in 1 second to vital capacity ratio of 37% ± 2% predicted.

Results. Sixteen lesions were resected in the 14 patients and included 9 non-small cell carcinomas. There was one postoperative death. All other patients are alive and well through a mean follow-up of 22.6 ± 2.3 months (12 to 35 months). At 6-month follow-up improvements were noted in dyspnea index, forced expiratory volume in 1 second forced vital capacity, and 6-minute walk distance. Mediastinal recurrence at 12-month follow-up developed in 1 patient with two separate bronchioalveolar carcinomas.

Conclusions. Simultaneous lung volume reduction operation and tumor resection should be considered in patients with emphysema with marginal reserve in the hope of maximizing postoperative lung function.

	Introduction

Top Abstract Introduction Material and Methods Results Comment References

 
Patients with chronic obstructive pulmonary disease have an increased risk of the development of bronchogenic carcinoma. They have common etiologic factors. It has been estimated that 90% of lung cancer patients have signs and symptoms of chronic obstructive pulmonary disease and at least 20% have severe pulmonary dysfunction [1]. Surgical resection provides the best chance for cure. However, even some patients with early stage peripheral tumors are considered inoperable because of inadequate pulmonary reserve.

Lung volume reduction (LVR) has been used in the surgical treatment of severe emphysema to produce improvements in dyspnea, exercise capacity, and pulmonary function [2] [3] [4] [5] [6] [7] [8]. Patients with severe disability, hyperinflation, a heterogeneous distribution of disease, and a paucity of bronchitic symptoms appear to be the best candidates for LVR. Improvements in patient selection, anesthetic techniques, surgical instrumentation, and postoperative care have allowed for successful resections of emphysematous lung tissue in these select patients with multiple preoperative risk factors.

By applying the rationale and techniques of LVR, it has been possible to resect pulmonary nodules and improve pulmonary function at the same operative setting. Herein we report the Columbia-Presbyterian Medical Center experience with combined LVR and pulmonary nodule resection.

	Material and Methods

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Preoperative Evaluation
Between January 1995 and July 1996, 327 patients were evaluated for LVR at Columbia-Presbyterian Medical Center. Twenty-one patients (6.4%) were found to have suspicious pulmonary nodules. Routine preoperative assessment of these patients included a careful history of previous pulmonary infections, bronchitic symptoms, or thoracic operation, as well as a detailed review of old radiologic studies. Subjective evaluation of dyspnea and physical limitation was made at initial evaluation as measured by the medical research council of Great Britain dyspnea index scale.

Physiologic evaluation included a room air arterial blood gas, standard spirometry studies, lung volume measurements by plethysmography and nitrogen washout, 6-minute walk distance, and selective use of dobutamine thallium stress test/stress echocardiogram. Radiologic studies included inspiratory and expiratory chest films, computed tomographic (CT) chest scans with cuts beyond the adrenal glands, and quantitative ventilation and perfusion scans with xenon washout. Metastatic workup included whole body bone scans and head CT scans.

The inclusion and exclusion criteria for combined LVR and pulmonary resection are as follows:

Inclusion criteria

Severe dyspnea

Localized or diffuse disease

Hyperinflation with air trapping

Impaired diaphragmatic excursion

Regional heterogeneity of disease with appropri ate target areas for resection

Pulmonary nodule 3.0 cm

Exclusion criteria

Predominant airway disease such as asthma, bron chiectasis or chronic bronchitus with excessive purulent secretions

Obliteration of pleural space by previous disease or operation

Inappropriate emphysematous target areas for re section

Evidence of unrespectable locoregional neoplastic disease

Evidence of metastatic disease

Anatomic location of tumor necessitates resection of an unacceptable amount of functional lung parenchyma

Neither a minimum forced expiratory volume in 1 second (FEV₁) value nor pulmonary hypertension were used as exclusion criteria. Lung volume reduction was directed toward target areas of hyperinflation, and unilateral or bilateral procedures were performed based on target area distribution.

Using these criteria, 14 patients were considered suitable candidates for LVR and tumor resection. All patients gave informed consent for LVR and unilateral or contralateral nodule resection. Seven additional patients with severe emphysema and pulmonary nodules evaluated at our center were deemed inappropriate candidates for LVR and pulmonary resection. Five of these patients were unsuitable candidates for LVR and 2 patients had nodules situated deep within normal lung parenchyma making safe resection impossible.

Technique of Operation
All patients had thoracic epidural catheters placed preoperatively. A left-sided double lumen endotracheal tube was routinely used for selective single lung ventilation. Anesthetic technique included epidural local anesthetic and strict avoidance of parenteral narcotics.

Mediastinoscopy was performed only if suspicious lymph nodes (1 cm) were detected on chest CT. Because no patient in this series had mediastinal adenopathy on preoperative CT scanning, mediastinal node sampling was not performed before thoracotomy. Although our preferred incision for routine LVR is the bilateral anterior thoracosternotomy ("clam shell"), we tailored our surgical approach based on the anatomic distribution of the lesion in relation to the preoperative target areas when concomitant tumor resection was to be done. Eight patients underwent unilateral resections through a posterolateral thoracotomy (7) or by video-assisted thoracoscopy (1). Six patients had bilateral resections through either a median sternotomy (3) or a bilateral anterior thoracosternotomy (3). Intraoperative hilar and interlobar node sampling was not routinely performed for fear that such dissection would result in severe persistent leaks and bronchopleural fistulae.

After selective one-lung ventilation, target areas for lung reduction were identified by isolating those portions of the nonventilated lung that remained distended after deflation. Resections were performed with successive firings of a linear stapling device buttressed with strips of bovine pericardium. Eleven patients underwent wide wedge resections of their pulmonary nodules. In 3 patients with marked focal bullous changes of the right upper lobe (1) or left upper lobe (2), tumor resection was accomplished with a formal lobectomy. Twelve of the pulmonary nodules were within target areas and pulmonary resection was performed as part of the nonanatomic LVRS. The remaining four pulmonary nodules were outside target areas and wedge resection of the lesion was performed in conjunction with LVR of the targeted emphysematous regions of lung.

All patients were extubated in the operating room. Postoperative pain control was provided with epidural bupivicaine and intramuscular ketorolac tromethamine. Intensive chest physiotherapy was instituted immediately postoperatively, and all patients were enrolled in an inpatient physical therapy program after discharge from the thoracic surgery service.

Patients
The preoperative characteristics of the 14 patients in this series are shown in Table 1 and are compared to the baseline indices of the 7 patients who were deemed inappropriate candidates for combined LVRS and pulmonary resection. In the operated group there were 8 men and 6 women, and the mean age was 69 years old (54 to 80 years). Ten patients were oxygen dependent preoperatively, 5 patients had been on chronic steroids, and 6 patients underwent preoperative rehabilitation. The mean preoperative room air partial pressure of carbon dioxide was 43 ± 2.4 mm Hg (33 to 62 mm Hg) and 5 patients had a partial pressure of carbon dioxide of more than 45 mm Hg. The mean preoperative room air partial pressure of oxygen was 60 ± 2 mm Hg (46 to 63 mm Hg). Before operation the mean FEV₁ was 680 ± 98 mL (300 to 1,400 mL), 24% ± 5% predicted (12% to 58% predicted); the mean forced vital capacity was 54% ± 5% predicted (25% to 101% predicted); and the mean FEV₁ to vital capacity was 37% ± 2% predicted (30% to 47% predicted). Mean preoperative dyspnea index was 3.7 ± 0.3 (1 to 5) and mean 6-minute walk distance was 816 ± 93 ft (425 to 1,710 ft). All of these parameters were not statistically different from those observed in the unoperated group (Table 1).

	Results

Top Abstract Introduction Material and Methods Results Comment References

 
The preoperative lung function, surgical data, and pathology for each of the 14 patients in this series are shown in Table 2.

There were 16 nodules detected in the 14 patients. Pathologic examination determined 7 benign lesions and 9 malignant tumors. The lesions included non-small cell carcinoma (9), caseating granuloma (3), hamartoma (2), and aspergilloma (2). Of the nine non-small cell carcinomas there were four squamous cell carcinomas, three bronchioalveolar carcinomas, and two adenocarcinomas. One patient had two separate suspicious lesions, both of which were caseating granulomas. A second patient had two separate brochioalveolar carcinomas resected. The mean nodule size was 1.7 cm (0.7 to 3.5 cm). The anatomic distribution of the nodules was as follows: right upper lobe (5), right middle lobe (0), right lower lobe (5), left upper lobe (5), and left lower lobe (1). All patients had grossly clear surgical margins. One patient had microscopic evidence of vascular and lymphatic invasion at the resected surgical margin.

All patients are alive and well through a mean follow-up period of 22.6 ± 2.3 months (12 to 35 months). At 6-month follow-up there has been an improvement in dyspnea index (3.6 ± 0.3 versus 1.9 ± 0.3, p = 0.0004), FEV₁ (27% ± 4% predicted versus 35% ± 5% predicted, p = 0.0077), forced vital capacity (54% ± 6% versus 69% ± 5% predicted, p = 0.02), and 6-minute walk distance (817 ± 100 ft versus 1,100 ± 308 ft, p = 0.007) (Table 3). All but 1 patient has had a reduction in preoperative oxygen requirement. One patient has a suspected new primary neoplasm in unoperated lung tissue at 12 months follow-up. A mediastinal metastasis developed at 12 months follow-up in the patient with two separate bronchioalveolar carcinomas.

	Comment

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Without therapy, lung cancer is 100% fatal. Although some investigators have found 5-year survival rates of up to 35% for patients with stage I disease who are treated with radiation therapy alone [9], overall survival rates in most series are low [10] [11]. To date, operation remains the only significant chance for cure in patients with early stage lesions. After lobectomy, patients with T1 N0 non–small cell lung cancer experience up to an 80% 5-year cancer-free survival [12].

It has been difficult to assess the lower limit of tolerance for surgical resection in patients with severe emphysema. Preoperative pulmonary function testing has been used in an attempt to define postoperative morbidity and mortality after lung resection in the high-risk emphysematous patient. An FEV₁ of 800 mL or less (30% to 35% predicted), a forced vital capacity of 50% predicted or less, and a MVV of 40% predicted or less, as well as a room air partial pressure of carbon dioxide of greater than 45 mm Hg and a partial pressure of oxygen less than 50 mm Hg have all been historically associated with a marked increase in morbidity and mortality after a lung resection of any type [13] [14] [15] [16] [17]. In an effort to extend the criteria for operability, tests of regional lung function have been used to predict postoperative functional loss after resection [1] [18]. Gass and Olsen [19] suggest that a predicted postoperative FEV₁ of 30% to 35% is an acceptable value for operation. Other researchers have used exercise testing and measurements of oxygen consumption to determine risk. Walsh and colleagues [20] have reported a 0% 30-day operative mortality in "high-risk" patients who have a preoperative exercise oxygen consumption of >15 mL · kg^-1 · min^-1.

With the advent of LVR, many of the classic criteria for determining operability in lung cancer must be reassessed. McKenna and colleagues [21] recently reported their experience with resection of 51 lung masses in 325 patients undergoing LVR. Only 11 of the lesions in their series were non-small cell carcinoma and follow-up was short. Nonetheless, an acceptable mortality of 3.5% was achieved and no evidence of recurrent or metastatic disease was detected through a mean follow-up of 9 months. As in our series, a significant improvement in pulmonary function was observed in all patients undergoing combined LVR and tumor resection. McKenna and colleagues [21] concluded that LVR allowed operation for lung cancer in patients who otherwise would be considered to have physiologically inoperable disease.

All of the patients in the present series would be considered high risk by present preoperative indices. Nonetheless, morbidity and mortality were acceptable after combined LVR and tumor resection. Most important, resection was accompanied by an improvement in pulmonary performance. Of all 13 surviving patients, none had a deterioration in pulmonary function, oxygen requirement, or degree of dyspnea. Furthermore, improvements in exercise tolerance and dyspnea after combined LVR and pulmonary nodule resection can improve quality of life.

Eleven of the resections in this series were wide wedge resections with only three formal lobectomies. The Lung Cancer Study Group study has shown lobectomy to be superior to wedge resection in terms of early locoregional recurrence without a significant difference in overall survival for stage I lung cancer [13]. Although lobectomy is our preferred cancer operation for stage I and II lesions, the heterogeneous distribution of emphysematous changes frequently results in the removal of a large portion of functional lung tissue with such a resection. When very focal target areas of emphysema exist isolated to the upper lobe, formal lobectomy may be acceptable. However, it should be noted that the behavior of a lung cancer arising in emphysematous lung tissue with severely damaged regional lymphatic channels is not entirely known. In these select patients, wide wedge resection may provide adequate excision of both the primary lesion and the poorly preserved surrounding lymphatic basin. Long-term follow-up of combined wedge resection and LVR will be needed to determine whether adequate local control and survival advantage is conferred by this operation.

All lesions in this series were highly suspicious for malignancy based on CT scan criteria before resection. Invasive preoperative evaluation of these lesions by transthoracic needle biopsy was believed to be contraindicated because of severe emphysema. Given the peripheral location of the lesions, bronchoscopy was deferred until the time of operation. Although 7 of the 16 resected nodules were benign, potentially life-saving information was frequently gleaned from pathologic examination. In five of the seven benign nodules (caseating granuloma and aspergilloma) resected in this series, appropriate pharmacologic therapy was instituted based on the pathologic findings. Combining tumor resection with LVR allows definitive diagnosis as well as treatment of the benign or infectious nodule. In the hope of better defining the preoperative nature of solitary lung lesions in severely emphysematous patients, we recently have instituted a pilot study using positron emission scanning.

In conclusion, with the techniques of LVR surgery, emphysematous patients with suspicious pulmonary nodules and severe pulmonary dysfunction can be offered resection aimed at both cure of tumor and improvement in quality of life. The currently used predictors of perioperative risk in lung resection do not accurately apply to LVR candidates. As such, new criteria based on LVR risk factors and tumor location will need to be developed to assess accurately the operability and resectability of patients with severe emphysema and pulmonary nodules.

	References

Top Abstract Introduction Material and Methods Results Comment References

 

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