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(Chest. 2005;128:1571-1579.)
© 2005 American College of Chest Physicians

Bronchial Colonization and Postoperative Respiratory Infections in Patients Undergoing Lung Cancer Surgery*

Jose Belda, MD, PhD; Manuela Cavalcanti, MD; Miquel Ferrer, MD, PhD; Mireia Serra, MD; Jorge Puig de la Bellacasa, MD; Emilio Canalis, MD, PhD, FCCP and Antoni Torres, MD, PhD, FCCP

* From the Institut Clínic de Pneumologia i Cirurgia Toràcica (Drs. Belda, Cavalcanti, Ferrer, Serra, Canalis, and Torres), and Servei de Microbiologia (Dr. Puig de la Bellacasa), Hospital Clínic, and Institut d’Investigacions Biomèdiques August Pi i Sunyer, Universitat de Barcelona, Barcelona, Spain.

Correspondence to: Antoni Torres, MD, PhD, FCCP, Servei de Pneumologia, Hospital Clínic, Villarroel 170. 08036 Barcelona, Spain; e-mail: atorres{at}ub.edu


   Abstract
TOP
 Abstract
Introduction
 Materials and Methods
 Results
 Discussion
 Conclusion
 References
 
Study objectives: To evaluate the risk factors associated with postoperative respiratory infection in patients undergoing lung cancer surgery, with special emphasis on the perioperative pattern of airway colonization.

Design: Prospective cohort study.

Setting: Department of Pneumology and Thoracic Surgery of a tertiary hospital.

Patients: Seventy-eight consecutive patients undergoing lung cancer surgery were evaluated. Patients were followed up until hospital discharge or death.

Interventions: Fiberoptic bronchoscopies with bilateral protected specimen brush or bronchial aspirates were performed during anesthesia prior to the initiation of the surgical procedure.

Results: Sixty-five patients (83%) had perioperative bronchial colonization by either potentially pathogenic microorganisms (PPMs) [28 patients, 36%] or nonpotentially pathogenic microorganisms (56 patients, 72%). The 24 patients (31%) with a postoperative respiratory infection (pneumonia, purulent tracheobronchitis, or pleural empyema) had significantly higher perioperative bronchial colonization by PPMs (15 patients [63%] vs 13 patients [24%], p = 0.003) and a higher bacterial index (mean ± SD, 3.6 ± 3.3 vs 0.9 ± 1.4; p = 0.003), compared to patients without infection. The agreement between pathogens found in perioperative evaluation and during postoperative infection was total in 5 patients (21%), partial in 5 patients (21%), and no concordance in 14 patients (58%). In the multivariate analysis, the presence of perioperative airway colonization by a PPM (odds ratio [OR], 6.9; p = 0.001) and a higher postoperative pain score (OR, 4.1; p = 0.014) were independent predictors of postoperative respiratory infection.

Conclusion: Adequate control of postoperative pain, as well as the conditions that potentially cause airway colonization by PPMs, could be beneficial in preventing postoperative respiratory infections after lung cancer surgery.

Key Words: bronchial colonization • lung cancer • nosocomial pneumonia • postoperative respiratory infection


   Introduction
TOP
 Abstract
 Introduction
Materials and Methods
 Results
 Discussion
 Conclusion
 References
 
Patients submitted to lung cancer resection are at special risk for postoperative respiratory infections, with an incidence among these patients ranging from 2 to 20%.1234 Moreover, the mortality of these patients remains high, ranging from 22 to 67%, especially with the presence of postoperative pneumonia.45 The different definitions of postoperative respiratory infection and the different percentage of pneumonectomies in the published studies may explain this wide variation in the incidence of pneumonia and its attributed mortality.

To our knowledge, no study has specifically evaluated the risk factors associated with the development of postoperative respiratory infections among patients with lung cancer submitted to surgery. Prior airway colonization could be a potential risk factor for postoperative infections. Previous studies67 have found rates of airway bacterial colonization in patients with lung cancer at approximately 40%. However, an association between previous bacterial colonization and the incidence of postoperative respiratory infections could not be demonstrated by Ioanas and co-workers,7 probably due to small sample size.

We hypothesized that patients with colonization of the airways by potentially pathogenic microorganisms (PPMs) are at increased risk for postoperative respiratory infections due to the potential spread of colonizing PPMs during surgery. The aim of the present study was to identify risk factors for postoperative respiratory infections in patients submitted to pulmonary resection for lung cancer, with special emphasis on perioperative bronchial colonization.


   Materials and Methods
TOP
 Abstract
 Introduction
 Materials and Methods
Results
 Discussion
 Conclusion
 References
 
Patients
This study prospectively enrolled all consecutive patients with histologic diagnosis of lung cancer and suitability for resection using the TMN classification89 and treated in our institution during a 1-year period. Patients who used of antibiotics within the previous month, those hospitalized for > 48 h within 14 days prior to surgery, and those allergic to cefazolin were excluded. The Ethics Committee of the Hospital Clínic approved the study protocol. Informed consent was obtained from all patients.

Procedures and Data Collection
Perioperative bronchoscopy was performed in all patients during anesthesia and endotracheal intubation immediately before the surgical procedure. Bronchoscopic respiratory sampling consisted of bilateral protected specimen brush (PSB) or bronchial aspirate (BAS) in the distal part of the two main bronchi, or proximal to the tumor in those occluding the airway. Samples were quantitatively cultured according to standard procedures.101112 After bronchoscopy, each patient received cefazolin (1 g q8h) for 24 h, according to our current hospital policy for prophylaxis of surgical wound infection. Control chest radiographs were systematically obtained during the postoperative period and if respiratory infections were clinically suspected. In this case, blood, respiratory secretions (sputum, endotracheal aspirates, or bronchoscopic samples), and pleural fluid, if puncture was indicated, were cultured. Susceptibility tests were carried out in case of positive growth.

Pain was controlled by inserting an epidural thoracic catheter for administration of analgesia from 3 to 4 days; this was achieved in 95% patients. In the remaining 5% of patients, this catheter could not be inserted, so we used subcutaneous opioids. In all patients, we administered nonsteroidal anti-inflammatory drugs as well as IV paracetamol. In all cases, patients tried to sit up 1 day after surgery if clinically feasible, and ambulation was attempted as soon as possible. In addition, there is a specific physiotherapy protocol applied in all patients.

All relevant data from patients were recorded before and after surgery, and patients were followed up until hospital discharge. COPD was defined, and the degree of severity was stratified according to the Global Initiative for Chronic Obstructive Lung Disease strategy.13 Body mass index (BMI [weight in kilograms/height in meters]2) was calculated. Lung function tests (FVC, FEV1, diffusing capacity of the lung for carbon monoxide [DLCO]) had been performed preoperatively, and predicted postoperative lung function was calculated according to the number of resected segments and perfusion lung scan.14 The subjective postoperative pain score was evaluated by a linear visual analog scale (VAS) [0 = no pain, 10 = maximal imaginable pain], performed by the attending nursing staff every 8 h during the initial 48 h after surgery. The reported values are the average of these determinations.

Definitions
For the purpose of this study, a cut-off ≥ 102 cfu/mL was used to define perioperative colonization using PSB, and ≥ 104 cfu/mL for BAS.615 Patients were considered to have colonization whenever a microorganism was isolated above these thresholds.

Isolated bacteria were classified as PPMs or non-PPMs. The PPM group included the microorganisms usually implicated in respiratory infections in nonimmunosuppressed hosts (eg, Haemophilus influenzae, Staphylococcus aureus, Streptococcus pneumoniae, Moraxella catarrhalis, Pseudomonas aeruginosa, Klebsiella pneumoniae, among others).6 Non-PPMs included microorganisms not responsible for respiratory infections in nonimmunosuppressed hosts (eg, Streptococcus viridans, Neisseria spp, Corynebacterium spp, Candida spp, coagulase-negative Staphylococcus, among others).6 The bacterial index, obtained as the sum of the logarithmic concentrations of individual species of PPM,16 was calculated only in patients with PSB sampling.

Pneumonia was defined by the presence of a new pulmonary infiltrate, together with two of the following: fever or hypothermia, leukocytosis or leukopenia, and purulent respiratory secretions.17 Purulent tracheobronchitis was defined when these same clinical signs were present, in the absence of pulmonary infiltrate.18 Pleural empyema was defined as the presence of purulent aspirate from the pleural cavity (with or without pathogens). Microbiological confirmation was made by the presence of at least one PPM in respiratory samples above predefined thresholds (≥ 103 cfu/mL using PSB, ≥ 104 cfu/mL using BAL, and ≥ 105 cfu/mL using sputum or BAS)1920 or positive culture results of blood and/or pleural fluid. Agreement (total, partial, or no agreement) between perioperative lung microbiology and postoperative respiratory infections was evaluated only with isolated PPMs.

Statistical Analysis
Results are expressed as percentage and mean ± SD. Categorical variables were contrasted by {chi}2 test or Fisher Exact Test. The quantitative continuous variables were compared using the Student t test or Mann-Whitney U test. Univariate analyses of risk factors for postoperative respiratory infection were performed, and the quantitative continuous variables significantly associated with postoperative infection were categorized by the optimal cut-off values using receiver operator characteristic curve analyses. Lastly, a multivariate analysis using logistic regression with a conditional stepwise forward model (Pin < 0.05) was performed. Results are expressed as odds ratio (OR) and 95% confidence interval. The level of significance was set at 0.05, all two tailed.


   Results
TOP
 Abstract
 Introduction
 Materials and Methods
 Results
Discussion
 Conclusion
 References
 
One hundred four patients underwent lung cancer surgery during the study period; 26 patients had exclusion criteria, and 78 patients were included in this study. The main characteristics of patients with and without postoperative respiratory infections are summarized in Tables 1and 2 .


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  		Table 1. Baseline Characteristics of Patients Undergoing Lung Cancer Surgery*

 

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  		Table 2. Tumor Histology, Perioperative Surgical Data, and Postoperative Complications*

 
Perioperative Airway Colonization
Bilateral PSB was performed in 65 patients, and BAS was performed in 13 patients. The pattern of airway colonization in the two groups is summarized in Table 3 . Thirty-seven PPMs were isolated from 28 patients, most frequently H influenzae, S pneumoniae, P aeruginosa, and S aureus; and 103 non-PPMs were isolated from 56 patients, predominantly S viridans. There were 13 patients (17%) who showed no airway colonization. However, there were 65 patients (83%) with bronchial colonization, either by PPMs or non-PPMs; 19 patients had colonization by one microorganism, 23 patients by two microorganisms, 16 patients by three microorganisms, and 7 patients by four microorganisms. Fifteen patients (19%) had bronchial colonization only on the side of the tumor, 5 patients (6%) had bronchial colonization only on the contralateral lung, and 45 patients (58%) had bilateral bronchial colonization. In patients with bilateral bronchial colonization, the concordance between microorganisms isolated on both sides was partial in 22 patients (49%) and total in 23 patients (51%).


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  		Table 3. Pattern of Perioperative Airway Colonization Among Patients Undergoing Lung Cancer Surgery With or Without Postoperative Respiratory Infection*

 
The proportion of patients with bronchial colonization either by PPMs or non-PPMs was not different among patients with and without postoperative respiratory infection. However, the proportion of patients with PPM colonization was higher among those with subsequent postoperative respiratory infections (13 patients [24%] vs 15 patients [63%], p = 0.003). Patients with postoperative respiratory infections also had a significantly higher bacterial index (3.6 ± 3.3 vs 0.9 ± 1.4, p = 0.003) than those without postoperative respiratory infections (Fig 1 ).



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  		Figure 1. Rate of colonization by PPMs (panel A), and bacterial index (panel B) in patients with and without a respiratory infection. Error bars in plot B correspond to the SEM.

 
Patients with COPD more frequently had PPM colonization (24 patients [57%] vs 5 patients [14%], p < 0.001), compared to those without COPD. Patients with COPD were not hospitalized in the last 6 months prior to surgery.

Antimicrobial Susceptibility of the Most Frequently Isolated PPMs
Among the six isolated strains of S pneumoniae, four presented intermediate and one presented high penicillin resistance, four presented macrolide resistance, and one presented intermediate third-generation cephalosporin resistance. There were one ß-lactamase–positive H influenzae and one methicillin-resistant S aureus. The remaining PPMs were susceptible to their ordinarily tested antibiotics.

Postoperative Respiratory Infection
Twenty-four patients (31%) had at least one postoperative respiratory infection. There were 9 cases (12%) of pneumonia, 19 cases (24%) of purulent tracheobronchitis, and 5 cases (6%) of pleural empyema. In 17 patients, one single infection was diagnosed, while 5 patients had two different infections and 2 patients had three different infections. Purulent tracheobronchitis preceded pneumonia in the four patients with both infections. The microbiological findings of these patients are summarized in Table 4 .


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  		Table 4. Perioperative and Postoperative Microbiological Characteristics of Patients With Respiratory Infections

 
Among the 24 patients with postoperative respiratory infection, 21 patients (88%) had perioperative colonization by PPMs. Specifically in the case of pneumonia, 6 patients (67%) had perioperative colonization by PPM. Among the three cases of postoperative respiratory infection without perioperative colonization by any microorganism, all of them had purulent tracheobronchitis.

An etiologic diagnosis based on the isolation of at least one PPM was obtained in 17 patients (71%) with a postoperative respiratory infection. Comparing the PPMs isolated during the perioperative examination and those isolated at the onset of infection, total concordance of PPMs was obtained in 5 patients (21%) [in two cases with and in three cases without etiologic diagnosis], partial concordance was obtained in 5 patients (21%), and no concordance occurred in 14 patients (58%). With regard to the location of the pulmonary infection (pneumonia or empyema plus pneumonia) in relation to the lung side operated, it was contralateral in four cases, ipsilateral in four cases, and bilateral in the remaining three.

Risk Factors for Postoperative Respiratory Infection
The variables associated with an increased risk for postoperative respiratory infection in the univariate analysis were the presence of moderate-to-severe COPD, perioperative airway colonization by a PPM, and a higher postoperative pain score, as shown in Table 5 . In the multivariate analysis, the presence of perioperative airway colonization by a PPM (p = 0.001) and a higher postoperative pain score (p = 0.014) were the only independent predictors of postoperative respiratory infection.


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  		Table 5. Predictive Factors for the Development of Postoperative Respiratory Infection

 
The following variables were not associated with postoperative infectious complications: age, gender, tobacco consumption, renal or cardiac morbidity, BMI, nutritional parameters, lung function tests (except FEV1, which was lower in patients with COPD), airway colonization by non-PPMs, tumor characteristics (location, histopathology, TNM stage), surgical data (type of resection, duration, side of intervention), and postoperative data (transfusion of blood derivates, air leak, reintervention, prolonged mechanical ventilation).

Length of Stay and Hospital Mortality
Length of stay and outcome variables are shown in Table 6 . Patients with postoperative respiratory infections had a significantly higher length of respiratory intensive and intermediate care unit (RIICU) and hospital stay when compared with those without a postoperative infectious complication. When considering pneumonia, purulent bronchitis, and pleural empyema together, we found a nonsignificant trend of higher hospital mortality rate among patients with a postoperative respiratory infection (p = 0.116). However, only postoperative pneumonia was associated with a significantly higher mortality when compared to those patients without this specific postoperative infection (two patients [3%] vs three patients [33%], p = 0.010).


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  		Table 6. Lengths of Stay and Mortality in Patients With and Without Postoperative Respiratory Infection*

 

   Discussion
TOP
 Abstract
 Introduction
 Materials and Methods
 Results
 Discussion
Conclusion
 References
 
Summary of Results
This study shows that the presence of perioperative airway colonization by a PPM and greater postoperative pain are independent predictors of postoperative respiratory infection.

Microbial Airway Colonization
The bronchial tree is normally sterile in healthy people. However, among patients with impaired local defenses to infection, such as stable COPD, bronchiectasis, and patients with tracheotomy, the bronchial tree is frequently colonized either by PPMs and non-PPMs.612212223 In our study, we found that in patients undergoing lung cancer surgery, the rates of perioperative colonization were 37% for PPMs, 71% for non-PPMs, and 83% for the presence of any microorganism. Only two previous studies67 have addressed this issue in a similar population, and both found lower rates of colonization compared with the present study, approximately 40%. The explanation for these discrepancies is probably that we used bilateral sampling of respiratory secretions, as compared with Cabello and coworkers,6 who performed unilateral sampling. Most of the patients studied in the previous investigations and in the present study had COPD, and our findings on colonization might merely reflect what is happening in this population.

The pathogenesis of lower airway colonization in patients with stable COPD and lung cancer is still not well understood. The knowledge of risk factors for colonization in these populations may help the clinicians to detect those patients with the potential for colonization. In stable COPD patients, current smoking and lower pulmonary function were risk factors associated with bacterial colonization.2223 In patients with lung resection for bronchial carcinoma, a high BMI and the central location of the tumor were the variables related to colonization.7 A potential pitfall of all these studies is that the risk for colonization was investigated pooling together PPMs and non-PPMs. The role of non-PPMs in relation to local bronchial damage or in the potential development of infections is probably less important.24 Several studies have demonstrated an increased local inflammatory response in patients with stable COPD2425 or bronchiectasis,12 especially in the presence of colonization by PPMs and a high bacterial load.24

Postoperative Respiratory Infections
Several studies24262728 have reported an incidence of postoperative pneumonia ranging from 5 to 22%, similar to the present study. This variability may be explained by differences in the type of populations undergoing lung surgery and in the definitions of pneumonia.

Previous studies have evaluated the risk factors for pulmonary complications among patients submitted to lung cancer resection, but unfortunately these studies have considered infectious and noninfectious complications together. Preoperative length of hospital stay, poor nutritional status, COPD, arterial hypertension, smoking habits, advanced age, poor lung function, operating time, extended resection, the side of surgical intervention, postoperative mechanical ventilation, and increased anesthetic risk were associated with a higher risk of postoperative complications in different studies.2627293031323334 However, the specific risk factors for the development of respiratory infections after lung resection have not been studied.

In our study, the multivariate analysis showed that a higher postoperative pain score (OR, 4.1) and the presence of perioperative colonization by PPMs in the lower airways (OR, 6.9) were the main factors related with postoperative respiratory infections. In regard to the higher pain score, this was no surprise since we can expect that greater postoperative pain decreased the effectiveness of cough and removal of respiratory secretions. Conversely, the development of postoperative respiratory infection may also cause worsening of pain. This factor can be potentially modified by medical intervention. Regarding the prior colonization by PPMs, there are two potential explanations for this finding. First, the microorganisms colonizing the airways could be spread out throughout the lungs during the surgical procedure. However, we have to admit that the relationship between perioperative colonization and postoperative microbiology of respiratory infections is relatively weak, showing partial or total coincidence in 42% cases of infection. Moreover, patients without perioperative colonization by PPM are still at risk for postoperative respiratory infection, since in nine cases no PPM was isolated. Another study,28 looking at preoperative microbiology, found only a coincidence of 18% with microorganisms causing postoperative infection after lung cancer resection. Secondly, the development of complications could be related to the likely higher baseline inflammation of the lower airway in patients with PPM colonization. The relationship of colonization by PPMs and bronchial inflammation is described in patients with both stable2435 and exacerbated36 COPD; indeed, the presence of moderate-to-severe COPD was associated with an increased risk of both colonization and postoperative respiratory infections in our study. A new injury, such as surgery, in a previously damaged lung may potentially lead to the development of new infections. However, our study was designed to assess colonization but not inflammation of the lower airways, and therefore this hypothesis remains to be demonstrated.

In our series, we found that not only the presence of airway colonization by a PPM was significantly higher among patients with a postoperative respiratory infection, but the bacterial index was also higher. When evaluating only patients in whom PSB was performed, the bacterial index of the patients with postoperative respiratory infection was significantly higher than in those without a postoperative respiratory infection. However, this variable was not entered into the prediction model because PSB was performed only in 65 patients (83%), and bacterial indexes cannot be compared among PSB and BAS samples.

The development of postoperative respiratory infection was associated with a significantly higher length of RIICU and hospital stays. Furthermore, higher mortality could be demonstrated only among the patients with postoperative pneumonia, confirming the results found by other authors.45

These results open some light for future prophylactic strategies for postoperative infections after lung surgery. The administration of prophylactic antibiotics in patients with colonization before surgery, with the aim to eradicate microorganisms or decrease lung bacterial burden and decrease bronchial inflammation, deserves future investigation. However, the potential efficacy of such a measure in preventing postoperative infection is uncertain since little relation was found among PPMs isolated perioperatively and those causing postoperative infection. Decreasing inflammation with anti-inflammatory drugs could also be another potential prophylactic strategy. Indeed, a recent investigation37 from our group found the use of corticosteroids to be related with better response to treatment in patients with ICU-acquired pneumonia.

Our study has several limitations. First, we did not measure inflammatory markers in respiratory samples; consequently, we have speculated on this, taking the information from previous investigations.2425 Second, our study was not designed to systematically investigate the microbiological diagnosis of postoperative respiratory infections with invasive techniques. This could be a bias when comparing bronchoscopic perioperative colonization with postoperative infection. However, this limitation is inherent of these clinical studies in patients with postoperative infection and acute respiratory failure in whom the risks derived from performing bronchoscopy have to be taken into account. Finally, the study was not designed to establish a relationship between prior colonization and mortality. For this particular purpose, the sample size should be much higher.


   Conclusion
TOP
 Abstract
 Introduction
 Materials and Methods
 Results
 Discussion
 Conclusion
References
 
Adequate control of postoperative pain without interfering with secretion clearance and cough reflex, as well as the conditions that potentially cause airway colonization by PPM, could be beneficial in preventing postoperative respiratory infections after lung cancer surgery. The relationship between prior colonization, postoperative infection, and potential prophylactic measures needs to be studied in more detail.


   Footnotes
 
Abbreviations: BAS = bronchial aspirate; BMI = body mass index; DLCO = diffusing capacity of the lung for carbon monoxide; OR = odds ratio; PPM = potentially pathogenic microorganism; PSB = protected specimen brush; RIICU = respiratory intensive and intermediate care unit; VAS = visual analog scale

Dr. Cavalcanti is a Research Fellow from Pavilhao Pereira Filho, PPG Pneumologia-UFRGS, Brazil, supported by an European Respiratory Society Research Fellowship.

Supported by Red GIRA FIS-ISCIII-03/063, Red Respira FIS-ISCIII-RTIC-03/11, Grant 1999SGR00228, and IDIBAPS.

Received for publication March 30, 2004. Accepted for publication March 10, 2005.


   References
TOP
 Abstract
 Introduction
 Materials and Methods
 Results
 Discussion
 Conclusion
 References
 

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