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Ann Thorac Surg 1996;62:968-974
© 1996 The Society of Thoracic Surgeons

Original Articles: General Thoracic

Early and Late Morbidity in Patients Undergoing Pulmonary Resection With Low Diffusion Capacity

Michael Bousamra, II, MD, Kenneth W. Presberg, MD, Joseph H. Chammas, MD, James S. Tweddell, MD, Barry L. Winton, MD, Mark R. Bielefeld, MD, George B. Haasler, MD

Department of Cardiothoracic Surgery and Divisions of Pulmonary and Critical Care Medicine and Surgery, Medical College of Wisconsin, Milwaukee, Wisconsin


   Abstract
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 Footnotes
 Abstract
Introduction
 Material and Methods
 Results
 Comment
 References
 
Background. We sought to determine whether low diffiusion capacity of the lung to carbon monoxide (DLCO) is a predictor of high postoperative mortality and morbidity after major pulmonary resection and whether major pulmonary resection in patients with low DLCO results in substantial long-term morbidity.

Methods. Sixty-two major pulmonary resections were performed in 61 patients with low DLCO (DLCO <=60% predicted for pneumonectomy or bilobectomy; <=50% predicted for lobectomy). Contemporaneously, 262 other patients underwent 263 major pulmonary resections (group II). Long-term morbidity was assessed in subsets of patients with low (n = 24) and high (n = 22; DLCO >60% predicted) DLCO.

Results. The hospital mortality rates were equivalent (4.8% low DLCO versus 4.9% group II), whereas respiratory complications were more frequent in patients with low DLCO (18% versus 9.5%; p = 0.05). In the subgroup analyses, patients with low DLCO had more hospitalizations for respiratory compromise and worse median dyspnea scores. Analysis of patients with substantial dyspnea revealed an association with extended pulmonary resection and postoperative radiation therapy in patients with low DLCO.

Conclusions. Patients with low DLCO underwent major pulmonary resection with a low mortality rate and an acceptable, but increased, respiratory complication rate. Long-term respiratory morbidity was increased in patients with low DLCO; however, the extent of pulmonary resection and the use of postoperative radiation therapy may have contributed to the development of dyspnea in these patients.


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 Abstract
 Introduction
Material and Methods
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 References
 
See also page 974.

Over the past 40 years, progressive refinement in patient selection strategies has reduced the morbidity and mortality of major pulmonary resection [1, 2]. A minimum forced expiratory volume in 1 second (FEV1) of 1 L for lobectomy and a predicted postoperative FEV1 of 0.8 L after pneumonectomy are frequently quoted cutoff points for pulmonary resection [3, 4]. Pulmonary reserve also has been assessed by maximal voluntary ventilation [5, 6], maximal oxygen consumption [7, 8], and exercise desaturation studies [9], with improvement in the prediction of adverse outcomes after major pulmonary resection. Recent experience with lung volume reduction underscores the need to assess further the functional capacity of the involved lung, as removal of severely emphysematous tissue may be well tolerated in patients with advanced chronic obstructive pulmonary disease [10].

Less well studied, but also of importance, are the long-term morbidities related to pulmonary resection and the preoperative factors associated with their development. Chronic dyspnea is one such disabling symptom, which can result from pulmonary resection in marginal patients. In several pulmonary diseases, reduction in the diffusion capacity of the lung to carbon monoxide (DLCO) has been associated with exertional dyspnea, pulmonary hypertension, and shorter life expectancy [11–14]. The DLCO has also been reported to be an independent predictor of postoperative morbidity and mortality after major pulmonary resection [15]. In this retrospective study, we sought to determine whether patients with low DLCO were at increased risk of morbidity and mortality in both the perioperative period and during long-term follow-up after major pulmonary resection.


   Material and Methods
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 Introduction
 Material and Methods
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We reviewed all adult patients at the Zablocki Veterans Administration Hospital and the Milwaukee County Medical Center who underwent standard lobectomy, bilobectomy, or pneumonectomy for nontraumatic diagnoses from January 1, 1991 to July 31, 1995. Case information spanning 26 perioperative variables was entered into a continually updated data base (Table 1Go). These data were supplemented by chart review as necessary.


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  		Table 1. . Comparison of Perioperative Factors Between Patients With Low Diffusion Capacity of the Lung to Carbon Monoxide and Group II Patientsa
 
The single-breath DLCO was measured according to the method of Gaensler and Wright [16] and adjusted to correct for anemia, as described previously [17]. The forced vital capacity and the FEV1 were measured by a Collins DS Plus Spirometer System (W.E. Collins Inc, Braintree, MA). Patients were divided into two groups related to their DLCO: Patients with low DLCO were defined as having a DLCO of 60% or less predicted if undergoing pneumonectomy or bilobectomy and 50% or less predicted if undergoing lobectomy; the remaining patients had a higher or undetermined DLCO value (group II). Predicted postoperative values for the percentage of predicted DLCO, FEV1, percentage of predicted FEV1, forced vital capacity, and percentage of predicted forced vital capacity were calculated by multiplying the index by the fraction of functional lung segments remaining after resection. The number of lung segments was assigned as described previously [5, 18]: right upper lobe = 3; right middle lobe = 2; right lower lobe = 5; left upper lobe = 5; left lower lobe = 4. Performance status was assessed by the Karnofsky score [19].

Postoperative events are listed for patients with low DLCO and group II patients in Table 2Go. Respiratory complications included atelectasis, pneumonia, and adult respiratory distress syndrome. Atelectasis was considered substantial if it was lobar or if it prompted reintubation, bronchoscopy, transfer to the intensive care unit, or prolongation of the intensive care unit stay. Pneumonia was defined as the presence of a focal or diffuse infiltrate associated with pathologic organisms on sputum culture. The diagnosis of adult respiratory distress syndrome was reserved for cases with respiratory compromise associated with diffuse infiltrates, without identification of causative bacteria and in the absence of congestive heart failure. Prolonged air leak was defined as lasting for more than 10 days. Cardiac complications included cardiac failure requiring inotropic support, myocardial infarction confirmed by enzymatic and electrocardiographic evidence, and arrhythmias resulting in hemodynamic compromise. Pulmonary embolism was documented by high-probability scan, pulmonary arteriogram, or autopsy. Miscellaneous complications included renal insufficiency requiring dialysis, stroke, prolonged ileus, intestinal ischemia, wound infection, and sepsis. Each of these complications individually occurred in less than 2% of patients.


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  		Table 2. . Mortality and Complications in Patients With Low Diffusion Capacity of the Lung to Carbon Monoxide and Group II Patientsa
 
All available patients with low DLCO (n = 24) and a cohort of 22 group II patients with known DLCO greater than 60% of that predicted (high DLCO) were interviewed 6 months or more after major pulmonary resection to assess long-term respiratory morbidity. This cohort of group II patients was preselected to have age and spirometry data similar to those of their low-DLCO counterparts. All patients were free of recurrent cancer. Dyspnea was graded by the Modified Medical Research Council of Great Britain dyspnea scale [20] (Appendix 1) and by the baseline dyspnea scale [21] (Appendix 2). The change in dyspnea related to major pulmonary resection was graded by the transitional dyspnea index [20] (see Appendix 2). Negative changes in the transitional dyspnea index were assigned the modifiers "mild" (-1), "moderate" (-2), and "major" (-3) to describe the deterioration in dyspnea. Patients were also questioned regarding their level of dyspnea before operation to obtain a retrospective baseline dyspnea score, which was compared with the current score. Hospitalization for respiratory compromise was assessed by patient interview and confirmed by chart review. Continued supplemental oxygen use 1 month after discharge was noted.

Survival comparison for lung cancer patients was made between group I (low DLCO) and group II patients using a Kaplan-Meier method of analysis. There were 41 group I patients and 172 group II patients with current data permitting analysis of survival and disease status.

Comparisons between patients with low DLCO and group II patients were made by an unpaired Student's t test for continuous variables and by {chi}2 analysis for indicator variables. Dyspnea scores within groups were compared by the Wilcoxon signed rank test; scores between groups were compared by the Wilcoxon rank sum test. Missing data for individual variables were not included in the total number when calculating percentages.


   Results
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 Footnotes
 Abstract
 Introduction
 Material and Methods
 Results
Comment
 References
 
A total of 325 major pulmonary resections were performed in 323 patients: 243 lobectomies, 16 bilobectomies, and 66 pneumonectomies. Two hundred ninety-two patients had lung cancer, and 33 had either benign disease or metastatic cancer to the lung. The criteria for low-DLCO classification (group I) were met in 62 cases, whereas the remainder (n = 263) were classified as group II cases.

Preoperative variables were compared between patients with low DLCO and group II patients (see Table 1Go). Patients with low DLCO were older, had a more extensive smoking history, were more likely to have had preoperative dyspnea, and had worse general health. Both measured and fractional spirometric values were lower in patients with low DLCO. Mean DLCO values were 44% ± 9% in patients with low DLCO and 79% ± 16% in group II patients. Patients with low DLCO underwent pneumonectomy or bilobectomy more frequently than their group II counterparts. Lung cancer was the predominant indication for resection in both groups.

Hospital mortality rates were equivalent between the patient groups. Patients with low DLCO experienced a higher respiratory complication rate (18% versus 10%), and pleural space problems were twice as frequent among these patients (see Table 2Go). Individually and combined, other complication rates were similar between patients with low DLCO and group II patients.

Among lung cancer patients, the stage of disease was more advanced in the low-DLCO group (see Table 1Go). Long-term survival was similar between the groups, although there was a constant trend toward poorer survival in patients with low DLCO (Fig 1Go). The median survival was 41 months in patients with low DLCO and 45 months in group II patients. Twenty-six percent of the late deaths (19 of 71) were unrelated to cancer in group II, compared with 41% (7 of 17) in the low-DLCO group (p = not significant).



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  		Fig 1. . Survival among patients with low and high diffusion capacity of the lung to carbon monoxide (DLCO) with lung cancer. Median survival was 41 months for low DLCO; 45 months for high DLCO.

 
Twenty-four patients with low DLCO and 22 group II patients with DLCO greater than 60% (high DLCO) were interviewed at least 6 months after resection to assess chronic respiratory compromise (Table 3Go). The subgroups were similar with respect to age and predicted postoperative spirometric values. Predicted postoperative DLCO was 58% in patients with high DLCO and 32% in those with low DLCO (p < 0.01). Hospitalizations for respiratory compromise were significantly more frequent in patients with low DLCO. Three patients with low DLCO required supplemental oxygen after resection, whereas all 22 patients with high DLCO were free of supplemental oxygen. Dyspnea assessed by the Modified Medical Research Council dyspnea scale was worse in patients with low DLCO than in their high-DLCO counterparts (Fig 2aGo). In addition, pulmonary resection resulted in a significant decline in the median baseline dyspnea scores only among patients with low DLCO (Fig 2bGo). The transitional dyspnea index was used to identify patients with clinically significant worsening of dyspnea related to pulmonary resection (index scores of -2, -3) (Table 4Go). Seven patients with low DLCO experienced moderate (n = 4) or major (n = 3) worsening of dyspnea, compared with 2 patients with high DLCO who had moderate declines. These 9 patients with moderate or major worsening of dyspnea underwent more extensive pulmonary resections (bilobectomy, pneumonectomy; n = 4) and were more likely to have received postoperative radiation therapy (n = 4). Analysis by treatment modality showed that 3 of 6 patients with low DLCO and 1 of 7 patients with high DLCO who underwent bilobectomy or pneumonectomy had moderate or major deterioration of dyspnea. Similarly, 3 of 6 patients with low DLCO and 1 of 2 patients with high DLCO who had postoperative radiation therapy reported marked worsening of dyspnea. There was overlap within these subsets, as 3 patients underwent extended resection followed by radiation therapy; all experienced substantial worsening of dyspnea.


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  		Table 3. . Comparison of Patients With Low and High Diffusion Capacity of the Lung to Carbon Monoxide Assessed for Chronic Respiratory Morbiditya
 


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  		Fig 2. . (a) Modified Medical Research Council (MMRC) median dyspnea scores for patients with low and high diffusion capacity of the lung to carbon monoxide (DLCO) after resection: Low DLCO is greater than high DLCO (p < 0.002 by Wilcoxon rank sum test). (b) Preoperative and postoperative median baseline dyspnea scores (BDS) for patients with low and high DLCO. Post-low DLCO is less than pre-low DLCO (p < 0.01 by Wilcoxon signed rank test).

 

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  		Table 4. . Comparison of Patients With and Without Substantial Deterioration in Dyspneaa Related to Major Pulmonary Resectionb
 

   Comment
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 Abstract
 Introduction
 Material and Methods
 Results
 Comment
References
 
The data presented indicate that patients with low DLCO can undergo major pulmonary resection with a low mortality rate and an acceptable, though increased, incidence of respiratory complications. This result is notable in that patients with low DLCO also underwent pneumonectomy more frequently and as a group were older, smoked more, and had more advanced cancer. We accepted the premise forwarded by Ferguson and colleagues [15] that these patients were at higher risk for lobectomy or pneumonectomy. In turn, patients with low DLCO were selected with relatively well-preserved spirometry values (80% predicted forced vital capacity, 74% predicted FEV1). We also maintained a policy of longer observation in an intensive care setting, generally lasting 2 to 3 days. This program was reinforced by the observation in our institution that most fatal complications after major pulmonary resection were respiratory related and that the initial compromising insult usually occurred within the first 3 postoperative days. In addition to preoperative patient selection and prolonged postoperative intensive care, we advocated aggressive pain management using intrathecal or epidural agents. Together these measures may have reduced the incidence of respiratory complications and promoted earlier recognition of their presence, thus normalizing the mortality rate in patients with low DLCO.

We hypothesized that because patients with low DLCO were subjected to greater respiratory morbidity, their survival would also be decreased because of related or comorbid factors. However, long-term survival was equivalent between the patient groups despite a higher stage distribution in patients with low DLCO. The incidence of death from causes other than recurrent cancer tended to be higher in patients with low DLCO, but the small populations prevented firm conclusions in this regard.

Patients with low DLCO experienced greater chronic respiratory morbidity after major pulmonary resection. Specifically, major pulmonary resection led to worsening of the sense of dyspnea only in these patients. Patients with high DLCO, on average, remained stable. Radiation therapy and more extensive pulmonary resection may have had an additive effect on the worsening of dyspnea. Although the small sample size prohibited statistical significance, these patterns of respiratory decline in patients with low DLCO subjected to extensive pulmonary resection with or without chest radiation therapy make intuitive sense and should be considered when counseling patients regarding therapeutic options. The data are also supported by experience in lung cancer patients undergoing primary radiation therapy. Abratt and Willcox [22] recently demonstrated worsening of clinical dyspnea scores in patients after chest radiation therapy for inoperable lung cancer. Associated with this finding was a 14% reduction in DLCO 6 months after radiation therapy. Choi and Kanarek [23], in a similar study of pulmonary function in patients undergoing radiation therapy for inoperable lung cancer, found that pulmonary function scores were reduced by 22% in patients with higher baseline FEV1 values (FEV1 >=50% predicted), whereas half of patients with lower baseline FEV1 values actually had a modest improvement in pulmonary function 6 months after radiation therapy. With regard to the extent of pulmonary resection, Pelletier and associates [24] demonstrated that patients who underwent pneumonectomy were more likely to experience dyspnea and exercise desaturation after resection than were lobectomy patients.

Patients with low DLCO have less functional reserve to tolerate either more extensive pulmonary resection or postoperative radiation therapy, and thus the prevalence of symptoms in this subgroup is not surprising. On the other hand, the majority of these patients did not experience marked worsening of dyspnea after pulmonary resection. In fact, postoperative dyspnea indices were equivalent between the patients with high and low DLCO if patients having radiation therapy and extended resection were excluded.

Our findings confirm those of Ferguson and colleagues [15] that a reduction in DLCO is a predictor of respiratory complications after pulmonary resection. The DLCO may act as an independent variable with respect to other pulmonary function tests. The DLCO reflects the capillary surface area available for gas diffusion across the alveolus and thus indicates the lungs' ability to oxygenate blood. In scleroderma, a reduction in DLCO is associated with pulmonary hypertension, exercise desaturation, and reduced survival [13, 25]. Among patients with chronic obstructive pulmonary disease, Owens and co-workers [14] confirmed the association of exercise desaturation with reduction in DLCO. Because chronic obstructive pulmonary disease is the principal cause of low DLCO among lung cancer patients, major pulmonary resection may exacerbate exercise desaturation, resulting in exertional dyspnea. Likewise, this loss of reserve may lead to complications or death in the perioperative period.

For individuals undergoing major pulmonary resection, particularly lung cancer patients, the struggle remains to provide an "optimal" curative resection against the mounting risk of morbid and fatal postoperative events. The decision-making process is further complicated by the availability of modern radiotherapeutic techniques and parenchyma-conserving pulmonary resections, which offer high-risk patients reasonable alternatives for lung cancer treatment. Thus, the quest to optimally assess perioperative risk continues. The DLCO measurement adds to the surgeon's armamentarium in evaluating patients for pulmonary resection and sheds light on the clinical course of these patients in the perioperative period and during long-term follow-up. Our data show that these patients can undergo major pulmonary resection with an equivalent mortality rate and an increased, but acceptable, respiratory complication rate. Chronic dyspnea and hospitalizations for respiratory decompensation are more common among patients with low DLCO; however, the development of substantial dyspnea in these patients is probably also dependent upon the extent of pulmonary resection and the use of postoperative chest radiation therapy.


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  		Appendix 1. Modified Medical Research Council Dyspnea Scale
 

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  		Appendix 2. Baseline Dyspnea Scale and Transition Dyspnea Index
 

   Footnotes
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 Footnotes
Abstract
 Introduction
 Material and Methods
 Results
 Comment
 References
 
Address reprint requests to Dr Bousamra, Department of Cardiothoracic Surgery, Medical College of Wisconsin, 9200 W Wisconsin Ave, Milwaukee, WI 53226.

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


   References
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 Abstract
 Introduction
 Material and Methods
 Results
 Comment
 References
 

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Discussion
Ann. Thorac. Surg. 1996 62: 974-975. [Extract] [Full Text]



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