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Ann Thorac Surg 2008;85:1158-1165. doi:10.1016/j.athoracsur.2007.12.071
© 2008 The Society of Thoracic Surgeons
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Original Articles: General Thoracic

Diffusing Capacity Predicts Morbidity After Lung Resection in Patients Without Obstructive Lung Disease

Mark K. Ferguson, MD*, Wickii T. Vigneswaran, MD

Department of Surgery, The University of Chicago, Chicago, Illinois

Accepted for publication December 19, 2007.

* Address correspondence to Dr Ferguson, Department of Surgery, The University of Chicago, 5841 S. Maryland Ave MC5035, Chicago, IL 60637 (Email: mferguso{at}surgery.bsd.uchicago.edu).

Presented at the Fifty-fourth Annual Meeting of the Southern Thoracic Surgical Association, Bonita Springs, FL, Nov 7–10, 2007.


General thoracic surgery: The Annals of Thoracic Surgery CME Program is located online at http://cme.ctsnetjournals.org. To take the CME activity related to this article, you must have either an STS member or an individual non-member subscription to the journal.

 

   Abstract
Top
 Abstract
Introduction
 Patients and Methods
 Results
 Comment
 Discussion
 References
 
Background: Diffusing capacity (DLCO), an independent predictor of morbidity after major lung resection, is not used routinely in preoperative evaluation because of a perceived lack of value in patients with normal spirometry. We evaluated the potential utility of measuring DLCO for assessment of operative risk in lung resection patients with normal spirometry.

Methods: A retrospective review was conducted for patients undergoing lung resection from 1980 through 2006 to identify predictors of postoperative morbidity. Patients were divided into groups with or without chronic obstructive lung disease (COPD), defined as a ratio of forced expiratory volume in the first second to forced vital capacity of less than 0.7 or a ratio of 0.7 or greater, respectively. Analyses for each group identified covariates for three outcomes: operative mortality, pulmonary morbidity, and overall morbidity.

Results: Of 1,046 patients in the database, 1,008 (545 men; mean age, 61.8 ± 0.35 years) had data permitting determination of COPD status: 450 (45%) with COPD, 558 (55%) without COPD. Operations included lobectomy (752; 75%), bilobectomy (83; 8%), and pneumonectomy (173; 17%). Overall mortality, pulmonary morbidity, and overall morbidity incidences were 59 (5.8%), 140 (14.0%), and 311 (31.4%), respectively. Pulmonary morbidity and operative mortality were related to postoperative predicted DLCO, age, and performance status in patients with and without COPD. The postoperative predicted DLCO was the single strongest predictor of pulmonary morbidity and operative mortality in both patient groups. Overall complications were related to postoperative predicted DLCO only in the COPD group.

Conclusions: Diffusing capacity is an important predictor of postoperative morbidity after lung resection even in patients with normal spirometry. Routine measurement of DLCO, regardless of spirometric findings, can help predict risk in candidates for major lung resection.

Complications after major lung resection are common, are associated with an increase in the incidence of operative mortality, and use costly resources. Diffusing capacity of the lung for carbon monoxide (DLCO) was first shown in the late 1980s to be a strong independent predictor of pulmonary complications and operative mortality after major lung resection [1, 2]. Its use in the preoperative evaluation of patients undergoing lung resection has not been routine [3], however, possibly because physicians believe that patients with normal spirometry do not require the additional measurement of DLCO.

A recent evaluation demonstrated that even in patients with normal spirometry, DLCO is a strong predictor of postoperative complications after major lung resection [4]. A limiting value for forced expiratory volume in the first second (FEV1) was used in that study for identifying patients with impaired spirometry, but such an approach does not specifically address the appropriate assessment of patients with chronic obstructive lung disease (COPD). In this study we evaluated patients without COPD undergoing major lung resection and explored the utility of DLCO in assessing operative risk in this group. We hypothesized that DLCO is a predictor of operative risk even in patients without COPD.


   Patients and Methods
Top
 Abstract
 Introduction
 Patients and Methods
Results
 Comment
 Discussion
 References
 
We retrospectively reviewed information from our database for all patients undergoing major lung resection (anatomic lobectomy, bilobectomy, pneumonectomy, or completion pneumonectomy) from 1980 through 2006. This protocol was approved by our internal review board, and an exemption was granted for specific patient consent.

Abstracted data included patient demographics; preoperative pulmonary function test results (FEV1 [forced expiratory volume in the first second] expressed as a percent of predicted [FEV1%] and single-breath diffusing capacity for carbon monoxide expressed as a percent of predicted [DLCO%]); the presence of comorbid factors including hypertension, diabetes, coronary artery disease, and renal insufficiency; performance status [5]; tobacco use within 6 weeks of operation; and the use of induction therapy (chemotherapy or radiation therapy, or both).

The extent of the operation (lobe[s] and number of segments removed) was recorded. Postoperative predicted FEV1% (ppoFEV1%) and DLCO% (ppoDLCLO%) were calculated using the remaining functional segment technique or, when available, using results of quantitative perfusion scans (133 patients). Postoperative complications were classified as pulmonary (pneumonia, need for prolonged initial intubation or reintubation, lobar collapse), operative mortality (death during the hospitalization during which the operation was performed or within 30 days of the operation), and overall complications (including cardiovascular complications, infectious complications, and any other complications). Surgical staging was performed using the 2002 American Joint Committee on Cancer guidelines [6].

Data were assessed in aggregate and according to COPD status, with COPD defined as an FEV1/FVC (forced vital capacity) ratio less than 0.7 [7]. Comparisons between groups with and without COPD were performed using two-sample Student’s t tests for continuous variables and {chi}2 analysis for categorical variables. Patient characteristics associated with complication categories were identified using univariate analysis for each patient group. Variables identified as having a possible relationship to outcomes (p < 0.1; lower cutoff values were used when the analyses were constrained by the number of events) were entered into a backward stepwise multivariable logistic regression analysis. Continuous data are expressed as mean ± standard error of the mean.


   Results
Top
 Abstract
 Introduction
 Patients and Methods
 Results
Comment
 Discussion
 References
 
During the 1980 to 2006 interval, 1,046 patients underwent major lung resection. Of these, 1,008 had information sufficient to permit assignment to COPD category and form the basis of this study. Patients with COPD were older, had a lower incidence of diabetes mellitus but a higher frequency of prior myocardial infarction, had a higher incidence of unfavorable performance status but less frequently underwent induction therapy, and had substantially worse spirometry and diffusing capacity (Table 1).


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  		Table 1 Patient Characteristics a
 
Patients with COPD underwent lobectomy rather than bilobectomy or pneumonectomy more often than did patients without COPD and had a higher percentage of earlier cancer stage. Postoperative predicted spirometry and diffusing capacity paralleled preoperative values for both groups, reflecting much worse postoperative lung function in patients with COPD than in those without COPD. This poorer function was associated with a higher incidence of pulmonary complications and overall morbidity in the COPD group, resulting in a longer length of hospital stay in this group (Table 2). Interestingly, the distribution of DLCO% remained broad, and DLCO% held fairly constant even as FEV1/FVC ratio declined, findings that indicate of the lack of a close relationship between spirometry and DLCO (Fig 1; correlation coefficient 0.238). The correlation coefficient between FEV1% and DLCO% for the entire dataset was 0.275, whereas the correlation coefficient between FEV1% and FEV1/FVC ratio was 0.493 for the entire group.


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  		Table 2 Perioperative Data a
 

Figure 1
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  		Fig 1. The relationship of predicted diffusing capacity for carbon monoxide (DLCO%) to the ratio of forced expiratory volume in the first second to forced vital capacity (FEV1/FVC) among patients undergoing major lung resection. The solid line is the regression line for relating predicted diffusing capacity for carbon monoxide to the ratio of forced expiratory volume in the first second to forced vital capacity, and the dashed lines indicate the 95% confidence limits for this equation.

 
Univariate analyses identified variables for entry into logistic regression analyses for the three complication categories. The COPD and non-COPD groups shared only prior myocardial infarction and ppoDLCO% as possible predictors of pulmonary morbidity, and only poor performance status and ppoDLCO% were shared as potential predictors of both operative mortality and overall morbidity (Tables 3, 4, 5). Go Go The extent of the operation was related to the incidence of complications: COPD patients with complications were more likely to have undergone bilobectomy than their complication-free counterparts, whereas patients without COPD who suffered complications were more likely to have undergone either bilobectomy or pneumonectomy than their complication-free counterparts. The extent of surgery was not entered into the logistic regression modeling because this factor was used to calculate ppoDLCO%, making the two variables mathematically linked. The logistic regression models demonstrated ppoDLCO% to be an independent and important predictor of pulmonary complications and operative mortality for patients with and those without COPD (Table 6). The odds ratios for ppoDLCO% were similar in patients without COPD and in those with COPD.


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  		Table 3 Univariate Analyses of Pulmonary Complications a
 

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  		Table 4 Univariate Analyses of Operative Mortality a
 

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  		Table 5 Univariate Analyses of Overall Complications a
 

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  		Table 6 Results of Logistic Regression Analyses for Outcomes
 
We also evaluated a subgroup of 368 patients, or 37% of the entire group, which possessed the most favorable spirometric values (FEV1/FVC ratio ≥ 0.7 and FEV1% ≥ 80). Logistic regression analysis demonstrated pulmonary complications to be related to age (odds ratio, 1.780 for each 10-year increase; 95% confidence interval, 1.174 to 2.699; p = 0.007) and ppoDLCO% (odds ratio, 0.728 for each 10-point increase; 95% confidence interval, 0.565 to 0.939; p = 0.015). Overall complications were related to age (odds ratio, 1.305 for each 10-year increase; 95% confidence interval, 1.018 to 1.673; p = 0.036) and ppoDLCO% (odds ratio, 0.772 for each 10-point increase; 95% confidence interval, 0.654 to 0.911; p = 0.002). There were too few operative deaths in this subgroup to permit analysis of predictive factors.

The risk of complications in the COPD and non-COPD groups was related to the degree of impairment of diffusing capacity (Fig 2). Pulmonary complication risk levels were somewhat higher for patients with COPD than for those without COPD for each ppoDLCO% value. Risks of pulmonary complications in patients without COPD but with low diffusing capacity were substantial. Mortality risks were similar between the COPD and non-COPD groups, and were similarly substantial when ppoDLCO% was low. Regression equations were not determined for overall complications because ppoDLCO% was not an independent predictor of such complications.


Figure 2
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  		Fig 2. Regression lines for risk of pulmonary or fatal complications relative to predicted postoperative diffusing capacity expressed as a percent of predicted (ppoDLCO%) for patients with (solid lines) and without (dashed lines) chronic obstructive pulmonary disease (COPD).

 

   Comment
Top
 Abstract
 Introduction
 Patients and Methods
 Results
 Comment
Discussion
 References
 
Diffusing capacity of the lung for carbon monoxide was initially investigated in the 1950s and 1960s as a correlate to anatomic changes in the interalveolar septae. Substantially impaired diffusing capacity in patients with emphysema was associated with poor long-term survival [8]. Diffusing capacity subsequently was found to decrease after major lung resection [9–12], and low DLCO was anecdotally related to an increased risk of operative mortality [13]. In the late 1980s DLCO was identified as an independent predictor of operative mortality and postoperative pulmonary complications [1, 2]. Subsequent reports confirmed the relationship of DLCO to postoperative morbidity and mortality [14–16].

Despite the utility of DLCO in assessing risk of postoperative complications and mortality after major lung resection, its use for this purpose does not appear to be widespread in the United States and Europe. In the European Thoracic Society database fewer than 25% of patients undergoing major lung resection had DLCO measured as part of the preoperative assessment [3]. It is likely that in the United States a similarly low percentage of surgeons takes advantage of this information. The practice of not routinely measuring DLCO is supported by algorithms published by respected organizations interested in assessing cardiopulmonary function as risk factors for lung surgery. Guidelines published in 2002 for assessing pulmonary resection candidates suggest that DLCO generally should be measured when there is a clear impairment of ventilatory capacity based on spirometry, identified as an FEV1 less than 80% of predicted [17]. This admonition was repeated in the most recent set of guidelines published by this group [18]. Others have recommended guidelines with similar restrictions on the measurement of DLCO [19].

There are a number of potential explanations for this, including lack of access, necessitating reliance on office spirometry rather than formal pulmonary function tests that often must be performed in a hospital setting; increased cost; the use of other screening tests, such as exercise capacity, to assess risk; lack of knowledge about the utility of this test; perceived lack of utility in a setting of normal spirometry; and perceived lack of impact on clinical recommendations. Not all of these possible factors can be addressed in a single study fostering an understanding of current practice patterns among thoracic surgeons. The current study was designed to provide data relevant to the latter three points, particularly the perceived lack of utility of measuring DLCO in the setting of normal spirometry.

Our investigation was stimulated by a report of Brunelli and others [4], who described the utility of DLCO in predicting complications in patients with and without abnormal spirometry, defined as an FEV1 less than 80% of predicted They found that almost 45% of patients with normal spirometry had a DLCO less than 80% of predicted. They demonstrated that in patients with a normal FEV1%, a ppoDLCO% less than 40 was an independent and important predictor of postoperative cardiopulmonary complications. Rather than replicate this study using raw spirometric values to identify impaired lung function, we chose to classify our patients according to COPD status as defined by the American Thoracic Society as an FEV1/FVC ratio of less than 0.70 [7]. This definition resulted in a similar percentage of patients identified as having normal spirometry relative to the study by Brunelli and associates [4] (55% in the current study versus 58% in the prior study), although the patient groups were otherwise not strictly comparable because of the different definitions used. Use of this definition permitted us to validate the findings of Brunelli and coworkers [4] with a different dataset, albeit one that was dichotomized differently, while using standard definitions of respiratory impairment to permit generalization of our findings to groups of patients on the basis of COPD status.

Our findings were similar to those of Brunelli and coauthors [4], and demonstrated that even in patients without COPD, DLCO% is an independent and important determinant of postoperative pulmonary complications and operative mortality. In fact, the odds ratios associated with these risks were similar between groups with and without COPD, indicating that COPD status did not influence the relative risk related to DLCO status. In contrast to the analyses reported by Brunelli and others [4] that used a cutoff value of 40% for ppoDLCO% to distinguish increased risk levels, our results identified a direct relationship between decreasing DLCO% and an increasing risk of complications. This relationship, which recapitulates our previously published findings in this regard, characterizes risk as a continuous rather than a dichotomous function of DLCO, and can aid clinicians in providing information to lung resection candidates regarding relative risk [1, 15].

There are a number of potential shortcomings of this study. During the long time frame over which data were collected substantial changes in surgical and anesthetic practices took place, many of which may have influenced outcomes. Some of these factors have recently been reported in a separate analysis of this dataset focusing on changes in patient presentation and practice patterns with time [20]. In particular, changes in patient selection and management with time may lessen the relative importance of DLCO in assessing risk in the current era. The data analyzed in this study originated from a single institution with a limited number of surgeons involved in the clinical care of these patients. Whether these findings can be extrapolated to the other institutions and surgical practices remains to be seen.

In summary, in this retrospective study we have demonstrated that regardless of COPD status, DLCO is an independent and important determinant of pulmonary complications and operative mortality in patients undergoing lung resection. We recommend that DLCO be assessed routinely in patients who are candidates for major pulmonary surgery regardless of findings on spirometry, and that this value be taken into account when assessing operative risk and in obtaining informed consent from patients. Although our findings are robust, we acknowledge the obvious shortcomings of a single institution study involving patients from different surgical eras. Thus, our findings and recommendations require confirmation through analysis of a larger contemporary multiinstitutional database.


   Discussion
Top
 Abstract
 Introduction
 Patients and Methods
 Results
 Comment
 Discussion
References
 
DR JEMI OLAK (Bakersfield, CA): I would like to thank the Association for asking me to discuss this well-presented paper and thank Mark for providing me with a draft of the manuscript last week.

Due to the lateness of the day, I will limit my discussion to two questions. Number one, I have been under the impression that the measurement of DLCO (diffusing capacity for carbon monoxide) can vary significantly from one laboratory to another and wondered what percentage of patients in your cohort had their DLCO determined at the University of Chicago PFT (pulmonary function testing) lab versus other labs in the city or wherever they came from?

DR FERGUSON: Most of our patients are referred from outside and come with pulmonary function testing, and so we accept the diffusing capacity measurement from those labs. Compared to spirometry, diffusing capacity is much less error prone in terms of measurement. Its measurement is not effort related, as long as the patient can breathhold for a sufficiently long period of time. Having said that, if there is a worrisome level for the diffusing capacity, we will repeat the study, usually at our own institution. It is true, there are some patients who improve substantially on repeat measurement. Sometimes that is because they have been identified as potential cancer patients because of pneumonia or things like that and they have time to recover during the interval before we repeat the test. I am not sure about any other cause for inaccuracy in the measurement in the outside institutions.

DR OLAK: And my second question is a two-part question. What cutoff of postoperative predictive DLCO do you use in this subset of patients with near normal spirometry below which you would deny them surgery as a component of their care? And the second part is, is there any literature on the effect of induction chemotherapy and radiation or, indeed, definitive chemoradiation on the measurement of DLCO?

DR FERGUSON: We don’t have a definitive cutoff, which I think is probably a good thing. We use clinical judgment in these patients. Forty percent has been touted as differentiating between sort of normal risk patients and high-risk patients, but it doesn’t differentiate between high risk and excessive risk. So we will go down maybe in the high 20s or low 30s now. There was a time in the early to mid 1990s when I was much more conservative in the use of diffusing capacity, but I think I have gotten a little bolder in my old age.

The other issue is that there are a couple of well-documented reports now on the decrease in diffusing capacity resulting from induction chemotherapy, and we are very careful to remeasure those patients prior to taking them to surgery. We are applying this to our esophagectomy patients as well. Sometimes we have to wait for a month or even 2 or 3 months for the DLCO to get back up to normal and make them operable.

DR JOSEPH I. MILLER (Atlanta, GA): I guess it reflects age and how long you have been doing this, but, Mark, a couple of comments. Mark has done more than any general thoracic surgeon in the last 25 years to promote the importance of diffusion capacity, not only in pulmonary resection but lung volume reduction. He has got a trilogy of papers, all of which I had the opportunity to be the principal discussant of at the AATS and then the primary reviewer for his third. Basically, in 1994 when lung volume reduction came on, we turned mainly to Mark’s papers to look to see the importance of the diffusion capacity, and what I would say, if you are still doing lung volume, you know the two principal things other than the arterial blood gases are the FEV1 (forced expiratory volume in the first second) and the diffusion capacity. I think what he has presented today is an outstanding work.

And as we tell the residents, if you could only have one test, you would like to have the diffusion capacity, and then to be able to use a quantitative scan to look at the predicted postoperative diffusion capacity. That probably represents the highest risk assessment, because we all know that patients who have good PFTs in terms of FEV1 but a low diffusion capacity, 30% or below, you are going to have trouble with the lung and you may use bovine pericardium and other technical aids.

So I rise only to compliment you but to stress the importance of getting a diffusion capacity, and probably if you can only get a couple of things, diffusion is one that you need to get along with blood gases and FEV1.

Thank you.

DR JOSEPH B. ZWISCHENBERGER (Lexington, KY): As you know, all of us live and die by our preoperative assessment of risk/benefit regarding pulmonary resection. If you had only one preoperative test, you would want to know exercise tolerance during stair walking. How does exercise tolerance relate to your study on diffusing capacity?

DR FERGUSON: Well, I actually agree with you. If we are going to do one single test, it would be some test of exercise capacity, and a good screening test would be stair climbing. We are actually putting together our own protocol for starting that up next month as a result of Alex Brunelli’s work.

DR DOUGLAS E. WOOD (Seattle, WA): Mark, at the end of the day, does it make a difference when we are talking with a patient and assessing whether they have a greater risk of having surgery or a greater risk of not having surgery? This is very helpful to us in educating the patient about what to expect, but ultimately, most of the time the patient has more at risk from not having surgery than from having surgery. We are mostly talking about lung cancer and mostly patients that don’t have an alternative that offers a significant chance for cure other than surgery. So how do you weigh that in your decision-making? I think even a patient that has a fourfold, fivefold, sixfold greater risk than normal still most of the time deserves an operation.

DR FERGUSON: I think there is a lot of utility in assessing potential risks for patients. One is discussing risk with them, providing informed consent, another is to stratify patients into risk categories so you know which patients are most likely to have difficulties postoperatively, which patient we should keep in the ICU (intensive care unit) longer, which patient can go straight to the floor, et cetera. In the very high-risk patients, sometimes more time, cardiopulmonary rehab, or other measures can reduce the risk, and actually improve the diffusing capacity. And finally, you can change the operation you are going to do. It doesn’t mean that you are not going to operate on the patient. Maybe you are going to do a minimally invasive approach, maybe you are going to do a segmental resection as opposed to a formal lobectomy. So there is a lot of potential impact as a result of knowing what the risk is for the patient.

DR THORALF SUNDT (Rochester, MN): Real quickly, and this might challenge Doug’s question a little bit. As a cardiac surgeon, we see somebody who is of advanced age, has lung disease and aortic valve disease, and their chief complaint is dyspnea. For us it really does become a critical question, what is their operative risk and how much is their shortness of breath from their valve and from their lungs? How do you think we as cardiac surgeons should use the diffusing capacity in evaluating the preoperative risk of a valve patient, for example?

DR FERGUSON: It is a good question. I don’t know the answer to it.


   References
Top
 Abstract
 Introduction
 Patients and Methods
 Results
 Comment
 Discussion
 References
 

  1. Ferguson MK, Little L, Rizzo L, et al. Diffusing capacity predicts morbidity and mortality following pulmonary resection J Thorac Cardiovasc Surg 1988;96:894-900.[Abstract]
  2. Markos J, Mullan BP, Hillman DR, et al. Preoperative assessment as a predictor of mortality and morbidity after lung resection Am Rev Respir Dis 1989;139:902-910.[Medline]
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  4. Brunelli A, Refai MA, Salati M, Sabbatini A, Morgan-Hughes NJ, Rocco G. Carbon monoxide lung diffusion capacity improves risk stratification in patients without airflow limitation: evidence for systematic measurement before lung resection Eur J Cardiothorac Surg 2006;29:567-570.[Abstract/Free Full Text]
  5. Oken MM, Creech RH, Tormey DC, et al. Toxicity and response criteria of the Eastern Cooperative Oncology Group Am J Clin Oncol 1982;5:649-655.[Medline]
  6. American Joint Committee on Cancer AJCC Staging Manual6th ed.. New York: Springer; 2002.
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  8. Bates DV, Knott JM, Christie RV. Respiratory function in emphysema in relation to prognosis Q J Med 1956;25:137-157.[Medline]
  9. Bates DV, McIlroy MB. Respiratory function after pneumonectomy Thorax 1956;11:303-311.[Medline]
  10. Curtis JK, Bauer H, Loomans S, Rasmussen HK. Pulmonary diffusion capacity studies. II. Clinical results using a modified carbon monoxide breathholding technique. Am J Med Sci 1958;236:57-64.[Medline]
  11. Burrows B, Harrison RW, Adams WE, Humphreys EM, Long ET, Reimann AF. The postpneumonectomy state: clinical and physiologic observations in thirty-six cases Am J Med 1960;28:281-297.[Medline]
  12. Dietiker F, Lester W, Burrows B. The effects of thoracic surgery on the pulmonary diffusing capacity Am Rev Respir Dis 1960;81:830-838.[Medline]
  13. Boushy SF, Helgason AH, Billig DM, Gyorky FG. Clinical, physiologic, and morphologic examination of the lung in patients with bronchogenic carcinoma and the relation of the findings to postoperative deaths Am Rev Respir Dis 1970;101:685-695.[Medline]
  14. Pierce RJ, Copland JM, Sharpe K, Barter CE. Preoperative risk evaluation for lung cancer resection: predicted postoperative product as a predictor of surgical mortality Am J Respir Crit Care Med 1994;150:947-955.[Abstract]
  15. Ferguson MK, Reeder LB, Mick R. Optimizing selection of patients for major lung resection J Thorac Cardiovasc Surg 1995;109:275-283.[Abstract/Free Full Text]
  16. Alam N, Park BJ, Wilton A, et al. Incidence and risk factors for lung injury after lung cancer resection Ann Thorac Surg 2007;84:1085-1091.[Abstract/Free Full Text]
  17. Beckles MA, Spiro SG, Colice GL, Rudd RM. The physiologic evaluation of patients with lung cancer being considered for resectional surgery Chest 2003;123:105-114.
  18. Colice GL, Shafazand S, Griffin JP, Keenan R, Bolliger CT. Physiologic evaluation of the patient with lung cancer being considered for resectional surgery. ACCP Evidenced-Based Clinical Practice Guidelines (2nd edition). Chest 2007;132(Suppl):161-177S.
  19. Loewen GM, Watson D, Kohman L, et al. Preoperative exercise VO2 measurement for lung resection candidates: results of Cancer and Leukemia Group B protocol 9238 J Thorac Oncol 2007;2:619-625.[Medline]
  20. Ferguson MK, Vigneswaran WT. Changes in patient presentation and outcomes for major lung resection over three decades. Eur J Cardiothorac Surg. In press.



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