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Ann Thorac Surg 2006;81:1996-2003
© 2006 The Society of Thoracic Surgeons

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Original article: General thoracic

Video-Assisted Thoracic Surgery Pulmonary Resection for Lung Cancer in Patients with Poor Lung Function

Division of Cardiothoracic Surgery, Chinese University of Hong Kong and Minimally Invasive Surgery Center, Union Hospital, Hong Kong, China

Accepted for publication January 5, 2006.

^_* Address correspondence to Dr Yim, Division of Cardiothoracic Surgery, Chinese University of Hong Kong, Prince of Wales Hospital, Minimally Invasive Center, Union Hospital, Shatin, NT, Hong Kong SAR, China (Email: yimap{at}cuhk.edu.hk).

	Abstract

Top Abstract Introduction Material and Methods Results Comment Acknowledgments References

 
BACKGROUND: The aim of this study is to evaluate the early outcome of patients with poor lung function who underwent video-assisted thoracic surgery (VATS) pulmonary resection for primary non-small cell lung carcinoma.

METHODS: We reviewed retrospectively the records of patients with lung cancer undergoing VATS lung resection over a period of 5 years. Twenty-five patients with preoperative poor lung function defined as forced expiratory volume in 1 second less than 0.8 L or the percentage predicted value for forced expiratory volume in 1 second less than 50% were identified. Thirteen patients underwent VATS lobectomies and 12 VATS wedge resections. Data were analyzed with respect to demographics, risk factors, and early postoperative outcome and survival.

RESULTS: There were 8 cases of morbidities (29%) and no surgical mortality. Five of these 8 patients had respiratory-related complications after surgery. A deterioration in pulmonary performance as indicated by the Eastern Cooperative Oncology Group (ECOG) score was seen in 7 patients (28%), with only 1 patient having an ECOG score greater than 2. No patient required home oxygen supplementation beyond the third month postoperatively. After a median follow-up period of 15.1 months (range, 1 to 24), 5 patients died. Only 1 patient (4%) died of a respiratory complication (pneumonia 6 weeks after surgery). The other 4 deaths were due to recurrent or metastatic disease. The actuarial survival rates at 1 and 2 years were 80% and 69%, respectively.

CONCLUSIONS: Video-assisted thoracic surgery pulmonary resection for cancer in patients with poor lung function can achieve acceptable functional and oncologic outcome.

	Introduction

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Despite progress in chemotherapy and radiotherapy, surgery remains an important therapeutic approach for patients with resectable non-small cell lung cancer (NSCLC) [1]. However, many lung cancer patients are also smokers who have associated cardiorespiratory comorbidities that increase perioperative and long-term pulmonary morbidity as well as mortality. Attempts have been made to define the physiologic limits for safe lung resection [2–5], but application of such limits may have hitherto excluded a significant number of patients from curative surgery.

Some investigators have found that operative risk is related to the absolute value of the predicted postoperative forced expiratory volume in 1 second (ppoFEV₁) [6], with a forced expiratory volume in 1 second (FEV₁) of less than 0.8L conventionally used as the cut-off for surgery. Others have found the percentage of the predicted FEV₁ based on sex, age, height, and body weight (FEV₁%) to be more useful. A preoperative FEV₁% of greater than 50%, or a predicted postoperative value (ppoFEV₁%) of greater than 40% has been recommended for patients receiving lung resection [3, 7]. However, in patients with a preoperative FEV₁% of less than 70%, the ppoFEV₁ may be an unreliable predictor of postoperative morbidity [8]. Another predictor of the likelihood of pulmonary complications after major lung resection is the preoperative diffuse capacity for carbon monoxide, although its routine use for preoperative assessment and ability to predict surgical outcome remains controversial, and it is not often performed [5]. Measuring oxygen uptake has evolved as a useful objective tool in the evaluation of patients with poor pulmonary function, but again is not always readily available in many centers. However, with modern advances in surgery, anesthesia, and perioperative care, the definitions of prohibitive risk based on these tests may have to be revised [3, 4, 9, 10]. Recently, for example, it has been suggested that patients with FEV₁% values considerably lower than the currently accepted level of greater than 50% can receive surgical intervention for lung cancer without significantly increased mortality [10].

Experience from lung volume reduction surgery, for example, has shown that some patients with poor lung function due to emphysematous change can safely undergo concurrent lung resection for both their lung cancer and lung volume reduction surgery within the same procedure at an acceptable level of risk, and even with improvement of their pulmonary status [11, 12]. Postoperatively, advances in pain management, the increasing early use of minitracheostomy for airway secretions, and incentive spirometry have aided the reduction in respiratory complications. The addition of structured postoperative pulmonary rehabilitation by specialist units has been responsible for shifting many patients from the physiologically unresectable category to the resectable [12].

The development of video-assisted thoracic surgery (VATS) has proven to be an attractive alternative approach for selected patients with normal or near-normal lung function, offering reduced pain and morbidity compared with open surgery [13]. By minimizing chest wall trauma and the potentially consequent effects on postoperative pulmonary impairment, VATS may even allow patients with very poor lung function to be surgical candidates. However, data regarding outcome in terms of postoperative complications, recurrence, survival, and quality or life are limited in such patients with poor lung function undergoing VATS for lung cancer. We retrospectively review our experience of VATS lung resection for poor lung function patients with NSCLC over a 5-year period.

	Material and Methods

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We reviewed retrospectively the records of our patients with NSCLC operated on in two University-affiliated teaching hospitals under one surgical team from January 2000 to January 2005. Ethical approval was given by the Research Ethics Committee of the Chinese University of Hong Kong, and informed consents for the study were obtained from the patients.

Of 626 major pulmonary resections performed for lung cancer during this time, we identified 25 patients (4%) with poor lung function who underwent VATS pulmonary resection. Video-assisted thoracic surgery is the standard approach for resection of lung cancer in our institute. Tumors larger than 5 cm are usually resected by open thoracotomy, and distance of tumor from the pleura (unless there is suspicion of chest wall involvement) is not contraindication for VATS in this center. Bronchoplastic procedures are performed by the open approach.

Inclusion criteria included diagnosis of NSCLC, VATS lung resection, and patients with poor lung function preoperatively. Poor lung function was defined as a forced expiratory volume in 1 second (FEV₁) less than 0.8 L or the percentage of the predicted value for FEV₁ less than 50%. Predicted postoperative FEV₁ (ppoFEV₁) values were calculated by multiplying preoperative FEV₁ by number of segments remaining divided by total number of segments. The wedge resections are considered to be equivalent to 1.5 segments and the ppoFEV₁ calculated accordingly. The location of tumor, degree of upper dominance emphysema, and degree of restrictive lung disease are not absolute determinants for operability in this group of patients.

The choice between lobectomy and wedge resection depends on a number of factors. We aim for VATS lobectomy in all our poor lung function cancer patients. However, in general, those with exercise tolerance of one flight of stairs or less will undergo VATS wedge resection. An additional consideration is that the location and size of tumor should allow wedge resection to be performed without resecting more than 1.5 pulmonary segments. Furthermore, the patient's general health, cardiac reserve, as well as available family and social support, are also considered. In our experience, exercise tolerance in terms of flights of stairs is more important. Patients with CO₂ retention (PaCO₂ > 6 kPa) or known pulmonary hypertension (although we do not routinely perform a preoperative echocardiogram) are usually excluded. Preoperative staging included chest reontgenogram, thoracic and abdominal computed tomography (CT) scan, flexible bronchoscopy, and positron emission tomography (PET)-CT scan when suspicious images of mediastinal lymph node enlargement were seen in thoracic CT scan. Our technique of VATS pulmonary resection for lung cancer has been previously described [13]. Sampling of the hilar, subcarinal, paratracheal, prevascular, aortopulmonary, and paraesophageal mediastinal lymph nodes was routinely performed.

Demographics, risk factors, smoking history, pulmonary function tests, and clinical course including respiratory and nonrespiratory complications were documented. In an attempt to quantify more objectively from the patients' perspective their pulmonary performance after pulmonary resection, we evaluated the pulmonary changes using the Eastern Cooperative Oncology Group (ECOG) score [5] (Appendix) at 1 month postoperatively, which was done by the hospital occupational therapist, as well as record the oxygen requirements during the postoperative period [14]. Follow-up data including respiratory status, recurrence, and survival data were recorded in outpatient clinic follow-up and by telephone contact. Full follow-up data were obtained from all patients.

Patents with stage IB or above tumors receive an oncology consultation postoperatively based on recommendations from the Southwest Oncology Group JBR10 and Cancer and Leukemia Group B 9633 trials. Nevertheless, for this poor risk group of patients, only 2 patients received adjuvant chemotherapy after balancing the pros and cons.

Statistical analysis using the two-sided ² test and Fisher's exact test was performed to determine association between respiratory complications and each independent variable when appropriate. The log-rank test was used to identify significant risk factors affecting survival at 2-year follow-up. Data analysis was performed using SPSS Version 11.5 (SPSS, Chicago, Illinois). A two sided p value of less than 0.05 was considered significant.

	Results

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Demographic and Clinical Data
A total of 25 patients during the study period fit the inclusion criteria for this retrospective review. Based on the exclusion criteria, 11 patients were not suitable for the study. The ages of the patients ranged from 69 to 80 years, with a mean of 75 years. Seventeen (68%) were male and 8 (32%) were female. Seventeen patients (68%) were smokers, and Brinkman's index among smokers ranged between 10 and 50 pack-years, with a mean of 33 pack-years. Seventeen (68%) had FEV₁ less than 0.8 L, 21 (84%) had FEV₁% less than 50% predicted, and 13 (52%) had both.

Surgical procedures were 13 lobectomies (52% [right upper lobe 3, right middle lobe 1, right lower lobe 5, left upper lobe 2, left lower lobe 2]) and 12 limited (wedge) resections (48%). Four of the 5 upper lobectomy patients have chronic obstructive pulmonary disease. Mean operative time was 2 hours and 3 minutes (range, 45 to 220 minutes). None of the patients required conversion from VATS to thoracotomy. All surgical margins were clear, and the most frequent histological subtype was adenocarcinoma seen in 19 patients (76%). The patients with clinical stage IIIa (T3N1) disease preoperatively had local invasion of pericardium and diaphragm. The additional patient with stage IIIa postoperatively had pathologic N2 disease found after surgery. The stage IIIB patient diagnosed after surgery was found to have metastasis within the same resected lobe (T4). The preoperative and pathologic TNM stage was given according to the criteria of the American Joint Committee on Cancer (Table 1).

Survival on Midterm Follow-Up
After a median follow-up time of 15.1 months (range, 1 to 24), 5 patients had died. Follow-up at 1 and 2 years was complete for 20 and 16 patients, respectively. Actuarial survival rates were 80% at 1 year after surgery and 69% at 2 years. Four deaths were related to lung cancer. Two patients had local disease progression within 6 months of surgery and died 3 and 4 months, respectively, after discovery of recurrence. Another 2 patients were found to have distant metastasis within 1 year of surgery (1 patient with brain metastases and 1 patient with both hepatic and bone metastases), and they died at 6 and 18 months after surgery, respectively. These 4 patients all received limited resections. Statistical analysis of all demographic and clinical factors revealed that limited resection was the only one significantly associated with poorer survival after 2 years of follow-up (p = 0.01; Tables 2 and 4).

	Comment

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Poor preoperative pulmonary function is a well-recognized predictor for morbidity and mortality after lung cancer surgery [3, 16]. However, with advancements in surgical technology and strategies, the guidelines for offering surgery to patients with poor lung function have evolved accordingly, allowing curative resection to be offered to many patients who would have been previously considered inoperable [7]. In particular, the minimally invasive nature of VATS may broaden the applicability of lung resection surgery for lung cancer patients with poor lung function [17]. For early-stage lung cancer resection, this approach is now widely accepted, and its advantages in terms of reduced postoperative morbidity, shorter hospital stays, and reduced functional and immunologic impairment have been demonstrated by many groups as well as the adequacy of resection, which has also been recently addressed [18–21].

In this study, we have demonstrated that the perioperative morbidity and mortality for patients with poor lung function undergoing VATS lung resection for lung cancer is very acceptable. Our patients had no surgical mortality and an overall morbidity rate of 29%. These figures are comparable with open major lung resection surgery [9, 12, 22–25] (Table 5). In one study, Cerfolio and colleagues [22] reported mortality of 2.4% and morbidity of 49% in 85 patients with poor lung function defined as FEV₁ less than 1.2 L. Another more recent study by Magdeleinat and colleagues [23], reported high operative morbidity (70%) and mortality (8.5%) seen in a group of 106 patients with poor lung function who underwent open lung resection; however, long-term survival and respiratory function were acceptable. In particular, VATS causes less postoperative pain and may offer faster recovery for the frail or high-risk patient with poor lung function [17].

Statistical analysis revealed that the only preoperative demographic or clinical factor associated with improved survival at 2 years was anatomical resection (lobectomy) with curative intention (p = 0.01). This conclusion has been reached by several other studies [24, 25]. However, selection bias may have accounted for survival differences between the wedge and lobectomy patients. The survival data should also be interpreted with caution because of the modest patient numbers and short follow-up, and hence limited power of the current study. Nevertheless, our results suggest that VATS lobectomy can be performed in patients with poor lung function, achieving satisfactory outcomes in terms of survival at 2 years. Limited resection for lung cancer is also an acceptable option for selected patients. Our data confirmed that limited resection using VATS in patients with very poor lung function results in acceptably low rate of surgery-related respiratory complications.

Some studies have found that surgical morbidity may be associated with ppoFEV₁ less than 40% [3, 6, 7], preoperative FEV₁ of less than 0.8 L, and FEV₁% of less than 50% [3, 7]. However, it should be noted that the ppoFEV₁ becomes less reliable as a predictor of postoperative morbidity when the patient's preoperative FEV₁% is less than 70% [8]. We found that the ppoFEV₁ (mean ppoFEV₁% 36.4%) in our poor lung function patients undergoing VATS major lung resection did not significantly predict morbidity or survival at 2 years, which is concurrent with recent large series [5]. The preoperative functional status of the patient may be a more important predictor [5]. Of course, failure to show ppoFEV₁% is associated with outcome is by no means the same as establishing that it is not associated with outcome.

Postoperative functional status of the patients, rather than survival per se, has become an increasingly important issue in assessing the benefits of lung surgery [16, 27]. Palliation of tumor-related symptoms needs to be carefully balanced against the morbidity caused by surgery. Prospective studies analyzing long-term quality of life after lung resection surgery are not available, but retrospective data from previous studies suggest that long-term survivors after lung cancer surgery enjoy good quality of life [16].

The postoperative functional status (as assessed by the ECOG score) and the requirement for postoperative oxygen have given us some indication of the pulmonary status in the postoperative period. Although 28% of the patients noted an elevation in their ECOG scores at 1 month, only 1 patient had ECOG score greater than 2. Patients with persistent functional deficit appear to drop rapidly, to just 11% after 6 months. Furthermore, only 2 patients required home oxygen supplements on discharge after surgery, including 1 who had pneumonia that would subsequently prove fatal. The limitation of using ECOG in patients after major lung resection is that pain and psychological effects may be additional factors affecting this performance. Future prospective studies assessing the postoperative functional status may be improved by using European Organization for Research and Treatment of Cancer Quality of Life Questionnaires–C30 and LC-13, which would have been difficult to complete in the present retrospective study.

In this study, we have not identified any preoperative demographic or clinical factors that are significantly related to postoperative respiratory morbidity in these patients. Nevertheless, we would advice that potential surgical candidates be meticulously prepared for surgery, with preoperative chest physiotherapy, strict smoking cessation, and optimization of medical therapy for preexisting pulmonary and airways diseases. Postoperatively, these patients should undergo vigorous chest physiotherapy and early mobilization. A formal postoperative rehabilitation program should be available for select patients with especially poor pulmonary function after surgery. Early and aggressive intervention for chest infections, including bronchoscopic toileting and minitracheostomy for suctioning, may be required to avoid pneumonia, which can be fatal in these patients.

We conclude that VATS pulmonary resection for lung cancer in patients with poor lung function can achieve morbidity and survival rates comparable to those of patients with adequate pulmonary function without resulting in long-term respiratory impairment. In addition to other nonsurgical factors, the benefits of a minimal access technique may play a role in improving outcomes in this high-risk group.

	Appendix

 
Eastern Cooperative Oncology Group Score (ECOG)

	Acknowledgments

Top Abstract Introduction Material and Methods Results Comment Acknowledgments References

 
The authors would like to thank Tse Yee-Kit of the Centre of Epidemiology and Biostatistics, the Chinese University of Hong Kong, for his kind assistance with the statistical analysis.

	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): Juan C. Garzon Calvin S.H. Ng Alan D.L. Sihoe Anthony V. Manlulu Randolph H.L. Wong Anthony P.C. Yim Permission Requests Citing Articles Citing Articles via HighWire Citing Articles via Google Scholar Google Scholar Articles by Garzon, J. C. Articles by Yim, A. P.C. Search for Related Content PubMed PubMed Citation Articles by Garzon, J. C. Articles by Yim, A. P.C. Related Collections Lung - cancer