Eur J Cardiothorac Surg 2002;22:23-29
© 2002 Elsevier Science NL
Sources of pathogens causing pleuropulmonary infections after lung cancer resection
M. Soka*,
A.Z. Draga
b,
J. Er
ena,
J. Jermana
a Department of Thoracic Surgery, Division of Surgery, University Medical Centre Ljubljana, Zaloka 2, Ljubljana, Slovenia
b Institute of Microbiology, Faculty of Medicine, University of Ljubljana, Zaloka 4, Ljubljana, Slovenia
Received 29 October 2001;
received in revised form 15 February 2002;
accepted 8 April 2002.
* Corresponding author. Tel.: +386-61-317582; fax: +386-1-4316-006
e-mail: miha.sok{at}mf.uni-lj.si
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Abstract
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Objective: The source of pathogens responsible for pleuropulmonary complications after lung resection is not yet completely understood, yet knowing this source is very important for proper perioperative use of antibiotics in lung surgery. We studied prospectively the value of sputum samples – collected 3 days before and 3 days after surgery – and of intraoperative bronchial swabs in the diagnosis of infective pulmonary complications following lung cancer resection. Methods: In a prospective trial, we studied 194 patients (18 women and 176 men, age range 34–79 years, mean 57 years) who were operated on for lung cancer. The infection screen consisted of intraoperative bronchial swabs, and sputum samples obtained prior to and 3 days after surgery. Before the operation, all patients were free of clinical signs of respiratory infection. In patients with postoperative infection, causative pathogens were identified from sputum, tracheal aspirate, thoracic puncture and thoracic drainage fluids. Results: Thirty-four patients suffered from 32 pleuropulmonary infections, and two from wound infection. Pathogenic organisms were isolated from preoperative and postoperative sputum samples and from intraoperative bronchial swabs in 50, 64 and 27% of patients, respectively. Postoperative infective complications were caused by gram-negative bacteria and Candida albicans in 75% of patients. These potential pathogens were recovered from preoperative sputum samples and from intraoperative bronchial swabs in only 18 and 13% of cases, but from postoperative sputum samples in 63% of cases. A strong correlation in identified pathogens was found between the postoperative sputum samples and the samples collected for microbiological diagnosis of subsequent postoperative infective complications (P<0.01). Conclusions: Our results indicate that pathogens that cause pleuropulmonary infective complications are probably acquired postoperatively from the patient's oral cavity, pharynx and hypopharynx. Appropriate antibiotic prophylaxis is discussed.
Key Words: Lung resection • Microbiology • Infection
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1. Introduction
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Patients undergoing elective lung cancer surgery frequently suffer from lower airway and lung infections. In addition to having a life-threatening potential, postoperative infections prolong the hospital stay and increase the cost of treatment. Risk factors for postoperative infections include depressed immune response, lung damage caused by resection, tube and catheter-related contamination of the airway, impaired expectoration, silent aspirations, changed local ventilation parameters and impaired postoperative ventilation due to pain [1,2]. The source of pathogenic organisms responsible for these complications is not yet completely clear. A significant correlation was found between the carriage of Haemophylus influenzae in preoperative oropharyngeal swabs [3], sputum samples [4], and colonization of the trachea at the time of intubation [5]. The culturing of bacterial pathogens from bronchoalveolar lavage samples obtained from the resected lung [6] and from intraoperative aspirates [7] was a significant predictor of postoperative chest infection. Postoperative infections occurred in 12–40% of the patients undergoing lung resection [7].
We studied prospectively the value of sputum samples – collected 3 days before surgery and 3 days postoperatively – and of intraoperative bronchial swabs for the diagnosis of infective pulmonary complications following lung cancer resection.
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2. Patients and methods
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This prospective study included 194 patients (18 women) undergoing lung cancer resection during the 2 years of the study. The age range was 34–79 years, mean 57.3 years. Histological and/or cytological diagnosis of stages I and II lung cancer was made before the operation. No patient received preoperative induction therapy. On postoperative pathological staging, stages I and II cancer was diagnosed in 140 patients, and stage III in 54. Squamous cell carcinoma of the lung was diagnosed in 108 patients, adenocarcinoma in 52, non-small cell carcinoma in 26, and small cell cancer in 8. Resection procedures included 121 lobectomies and bilectomies, 70 pulmonectomies and three sleeve lung resections. The mean length of surgery was 130±45 min. The thoracic wall was closed by rib approximation using non-resorbable sutures; the muscles and subcutaneous tissue were sutured with absorbable sutures, and the skin with silk. The surgical wound was covered; it was checked only when wound infection was suspected. The patients had no preoperative clinical or laboratory evidence of infection. The microbiological survey was carried out from sputum samples obtained 3 days before and 3 days after the operation, and from bronchial swabs collected at operation by passing a cotton swab over the cut bronchus. All microbiological examinations were carried out in one laboratory using standard laboratory methods. The sensitivity of identified pathogens to antimicrobials was determined. In patients with infective complications, causative pathogens were identified from the sputum, tracheal aspirate, thoracic puncture and thoracic drainage fluids.
All patients received antibiotic prophylaxis with perioperative cefuroxime 1.5 mg administered intravenously 1 h before the induction of anaesthesia, and 3 h after surgery. Preoperatively, 85 patients received 750 mg of oral cefuroxime every 8 h for 1–6 days; 109 patients were given no preoperative antibiotics. After the operation, the patients were cared for in the intensive care unit (ICU). Central venous and arterial catheters were placed in all patients. Normal eating was started on the first postoperative day.
During the first 3 postoperative days, blood screens, chest films and, when necessary, arterial blood gas levels were monitored. The patients performed vigorous breathing exercises with the assistance of a physiotherapist several times a day. Postoperative patient-controlled analgesia with morphine and bupivacaine was administered to all patients.
The diagnostic criteria for infection were as follows:
- Co-existing respiratory infection: increased amount of purulent expectorate, body temperature of >38°C of unclear cause , persisting for 3 days; hypoxia, white blood cell (WBC) exceeding 50% of the baseline value, and radiologic evidence of new lung infiltration (with or without pathogens).
- General infection: at least one positive blood culture.
- Pleural empyema: purulent aspirate from the pleural cavity (with or without pathogens).
- Wound sepsis: reddened, painful and indurated wound.
Patients who developed signs of infection were placed on cefuroxime 750 mg, given intravenously every 8 h. Their sputum and other available secretions were collected for identification of the pathogen. Further antibiotic treatment was based on bacteriological findings.
2.1. Statistical analysis
The SPSS/PC+ program was employed for statistical analysis of patient data. Statistical significance was determined by the chi-square test and expressed by P value.
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3. Results
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Postoperative infective complications occurred in 34 patients (17.5%). There were five (2.6%) deaths: two patients died because of cardiovascular complications; three succumbed to chest infection; two had bronchopneumonia and multiple organ failure and one patient with pneumonectomy died because of MRSA (Meticilin resistant Staphylococcus aureus) resistant bronchopneumonia. Other complications included bronchopneumonia in 30 patients, postoperative pleural empyema in two, and operative wound infection in two. Complications appeared 4.3±2.9 days after surgery. Table 1 summarizes clinical variables that may affect postoperative complications. There was only a slight association between the infection rate and the extent of resection (P=0.06). The rate of infection was not correlated to age, presence of associated disease, stage of the lung cancer or time of air leak after resection. Of the total of 194 patients, 124 (64%) had no important co-existing diseases. In the group of 70 patients with associated diseases, 14 (7.2%) suffered from diabetes, nine (4.6%) had cirrhosis, eight (4.1%) second primary cancer, 11 (5.7%) a history of myocardial infarction and nine (4.6%) of excavated tumor; 25 (12.8%) patients were on chronic bronchodilatator therapy for asthma and six (3%) had clinically important pneumonitis with bronchial obstruction. Several patients had more than one associated disease.
Bacteria were recovered from preoperative and postoperative sputum samples in 50 and 64% of patients, respectively, and from bronchial swabs in 27%. Table 2 shows the proportion of gram-negative and gram-positive bacteria, and Table 3 indicates bacterial strains recovered from the samples studied. Normal bacterial flora of the nasopharynx and oropharynx was identified from the sputum collected 3 days preoperatively in 82% of cases. Gram-negative bacteria were recovered in only 19%. Gram-negative bacteria and Candida were isolated from the sputum samples collected 3 days after surgery in 63% of cases; Candida being identified in 12%.
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Table 2. Percentage of positive bacterial cultures in the three samples studied, and percentage of gram-positive and gram-negative bacteria in each sample
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Table 3. Pathogenic organisms identified from preoperative sputum, postoperative sputum and bronchial swab samples
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Table 4 shows the association between the complication rate and microbiology of the three samples. Patients with bacteria identified from the sputum and bronchial swabs prior to surgery showed no increase in postoperative complication rates. The rate of postoperative infections, however, was statistically significantly higher in patients who had pathogens isolated from the sputum 3 days after surgery (P<0.01).
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Table 4. Chest infection rates and microbiology of preoperative and postoperative sputum samples and intraoperative bronchial swabs
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In 32 of 34 patients, presumed causative pathogens were identified from the tracheal aspirate, bronchial aspirate, and thoracic puncture and thoracic drainage fluids. Table 5 shows bacterial flora identified on the 3rd postoperative day from the sputum of all 194 patients and separately from the 3rd postoperative day sputum of 34 patients with infective complications, and pathogens responsible for the infection identified on the onset of infection. In 63% of cases, chest infections were caused by gram-negative bacteria and in 9% by Candida albicans. On the third postoperative day, gram-negative bacteria and C. albicans were recovered from the sputum in 66 and 6% of these patients, respectively.
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Table 5. Pathogens identified on the 3rd postoperative day from the sputum of 194 patients, and from the sputum of 32 patients with postoperative infection, and causative pathogens identified in 32 patients on the onset of infection
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4. Discussion
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Many risk factors seem to be involved in postoperative infection complications. Sex, age, extent of resection, p-stage of lung cancer, associated diseases and time of air leak were not identified as significant risk factors. Other factors, such as performance status, duration of operation, length of hospital stay and surgical technique were not studied, yet they seem to play an important role. The purpose of this study was to identify possible sources of causative pathogens and not to investigate risk factors for infection. We hypothesized that these common sources, with some exceptions, are independent of risk factors.
Collecting bronchial swabs at operation is the cleanest method of obtaining samples from the lung. Bacteria – mostly individual strains – were isolated from the bronchial swabs in 21% of cases in our series, which agrees with the results reported by Corell et al. [8]. The high frequency of Staphylococcus epidermidis isolated from intraoperative bronchial swabs (25%) seems to be due to bronchial manipulation during the operation.
Postoperative infective complications were caused by gram-negative bacteria and C. albicans in 75% of the cases. These potential pathogens were identified from preoperative sputum samples in 18% of cases, from intraoperative bronchial swabs in 18%, and from postoperative sputum samples in 63% (Table 3). This study has confirmed the high percentage of gram-negative bacteria and C. albicans in postoperative chest infections, reported by other authors [9,10]. A negative postoperative sputum in our study is prognostically interesting: only one of the 55 patients with a negative sputum developed postoperative infection (P<0.1) (Table 4).
Similar strains and a similar distribution of pathogens were found in the postoperative sputum and in samples collected to identify the causative agent of postoperative complications (Table 5). In the three columns, very similar pathogenic agents are presenting indicating and suggesting a common source of bacteria responsible for chest infections. This suggests that the mechanism of airway contamination does not occur during anaesthesia but rather in the early postoperative period secondary to silent aspiration, reflux, overspill and manipulation in the ICU. The strong correlation between the postoperative sputum microbiology and the subsequent postoperative infective complications indicates that the oral cavity, pharynx and hypopharynx rather than the lung itself are the sources of pathogens. It has been stressed, however, that in oesophageal surgery the most obvious route for infection to reach the upper airway is inoculation with a pathogen load during its manipulation under anaesthesia [11].
Our study suggests that antibiotic prophylaxis covering gram-negative organisms and C. albicans should not be given intraoperatively, but later on when the patient is at increased risk of developing nosocomial respiratory infection. The basic principle of perioperative antibiotic prophylaxis – to provide an optimal amount of antimicrobials in the surgical field at the time of surgery – does not seem to apply to patients undergoing pulmonary surgery. What appears to be more important in these patients is to prevent oropharyngeal colonization by strict oral hygiene and thorough disinfection of oral cavity prior to and after the operation, or/and by administering appropriate antibiotics during the first critical postoperative days. Bernard et al. [12] showed that a 48-h postoperative antibiotic prophylaxis regimen with second-generation cephalosporins decreases the rate of deep infections and empyemas compared to flash cefuroxime. Inappropriate timing of antibiotic prophylaxis seems to explain why there is no difference in the efficacy between various protocols of perioperative antimicrobial prophylaxis [13]. It may be that perioperative antibiotics, administered a few hours before surgery and a few hours after it, are effective against an insignificant source of infection. Further investigations will be necessary to determine whether oral disinfectants, given preoperatively and for several days after the operation, have any effect on the incidence of respiratory infections, and whether respiratory infection rate can be reduced by instituting a proper antibiotic and ensuring optimal levels of the antibiotic a few days after the operation, when the influence of nosocomial factors is strongest.
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5. Conclusion
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We conclude therefore that pleuropulmonary infection is probably acquired postoperatively from the microorganisms present in the patient's oral cavity, pharynx and hypopharynx. In patients undergoing lung cancer resection, appropriate antibiotic prophylaxis regime should therefore be prolonged in the postoperative period.
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Appendix A. Editorial Comment
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In this issue of the journal Sok et al. [1] report on a study undertaken with the objective of identifying the source of pathogens responsible for postoperative infection in patients undergoing pulmonary resection.
The identification of the source of pathogens in infective complications is an important issue which has much practical relevance related to prophylaxis and treatment of these complications. It also makes prophylaxis a target-oriented objective rather than an assumption-based exercise. Furthermore, it provides evidence-based patient management concerning admission to hospital and the need for preoperative microbiological screening.
Historically, patients intended for pulmonary resection were admitted a few days pre operatively for investigations which included identification of sputum micro-organisms. With the advent of minimalism in surgery and the ever-increasing pressure for the cost-conscious healthcare provider to reduce the duration of hospitalisation, the policy of admission to hospital days before an operation needed to be revised. Added to this is the fact that administration of broad-spectrum antibiotics to all patients undergoing surgery, under the umbrella of prophylaxis, is out of tune with 21st century thinking. However, there is no evidence to suggest that the policy of ‘blanket prophylaxis’ has been able to significantly reduce the rate of postoperative infection following pulmonary surgery.
In the past 20 years a number of studies have been carried out with the objective of identifying the source of pathogens involved in postoperative infection after lung resection and to determine risk factors for the development of post-resection infection [2–5]. The shortcoming of many publications has been the lack of meticulous microbiological survey in the perioperative period. This has partially been due to the fact that many centres have not been able to admit patients for microbiological study in advance of surgery due to financial constraints. In this respect, the article of Dr Sok and colleagues is both unusual and of particular interest in providing a good perioperative microbiological survey of patients. Their study concerns 194 patients, all of whom had microbiological examination of sputa 3 days before and 3 days after operation. At operation, a sample of secretions was obtained from the bronchial ’cut‘ surface. All patients were given intravenous Cefuroxime, 1 h after induction of anaesthesia and 3 h after surgery. Up to this point the protocol of the study seems quite straightforward in that analysis of the data could have shown positive or negative correlation between the pre- and postoperative microbiology in infected vs. non-infected patients. It might have also permitted identification of the infective agent in the sputa of patients on admission. However, the authors non-randomly divided their patients into two groups with or without oral administration of Cefuroxime prophylaxis 1–6 days preoperatively. They thus introduced another variable in the protocol and somewhat digressed from their primary aim of the study which was identification of the source of pathogens causing pleuropulmonary infections after lung cancer resection. In effect, pathogens present in samples of sputa and bronchial secretion in the subset which received 1–6 day antibiotic preoperatively (+ additional intravenous injection at and immediately after operation) cannot be said to represent unaltered samples. It might even be argued that candida infection in those who received 6 days enteral prophylaxis in addition to parenteral doses of Cefuroxime could have been promoted by antibiotic over-prophylaxis. Although this study demonstrates the causative organism in the infected patients, it does not identify in which subset of patients these infected cases were. It follows that in this setting, no meaningful correlation between pre- and postoperative sputum microbiology can be established except for the 109 patients who did not received oral prophylaxis. However, the data for these patients are not provided.
It is interesting to note that in this study, the patients were apparently admitted 4–7 days preoperatively and that the sample of sputum could be examined on 3 days preoperatively. Not many thoracic surgical units in the EU countries would be able to follow such a routine under the watchful eyes of the health economists. This advance preoperative admission has obviously given an opportunity to obtain excellent microbiological sampling which gives this study advantage compared with others devoted to the subject in recent years.
The postoperative infection rate of 17% in this series appears lower than many previously reported with infection rates ranging from <10% to >50% [2–4]. Lower infection rate in this series might be due to a good preparation and chest physiotherapy extended over a few days preoperatively, rather than extended course of prophylaxis.
Comparison between the type of organism in pre- and postoperative sputum examination shows several important points:
- 34 patients (17%) in this series developed postoperative chest infection, of whom 20 had pathogens in their sputa preoperatively vs. 33 postoperatively. The conclusion one may draw from this is that in approx. 58% of patients with postoperative infection there was a possible correlation between pre- and postoperative sputum microbiology even though it is not clear if the organisms were the same strain.
- 20% of patients had gram-negative organisms in their sputum preoperatively. Since 50% of patients overall had pathogens in the sputum preoperatively it follows that 40% of all pathogens in preoperative sputa were gram-negative. This incidence of gram-negative pathogens preoperatively (though not necessarily on admission) is higher than what we found in the course of a number of trials carried out between 1980 and 1988 [2,3,6] involving over 400 patients.
- We note that postoperative sputa contained approximately four times as many isolates of gram-negative and candida as the preoperative samples. There were also 10 more postoperative isolates of candida than preoperatively. The inevitable conclusion is that these pathogens have been acquired in hospital, possibly by cross-infection and encouraged by over-prophylaxis added to by postoperative immunodepression. We think the conclusion by the authors that pleuropulmonary infection is probably acquired postoperatively from the micro-organisms present in the patients oral cavity, pharynx and hypopharynx cannot be totally supported. The route of infection appears to be via the naso/oro-pharynx which is anatomically part of the respiratory tract but these organisms were not present on admission. Therefore, we suggest that the conclusion of the study should be that the source of pathogens in the postoperative pulmonary infection in this series is unknown; in the majority the organisms were acquired in hospital. Finally, the suggestion by the authors that an extended course of antibiotic prophylaxis may further reduce the incidence of postoperative infection needs qualification. Rationally, such prophylaxis is justified only when it can be tailored to the needs of a high-risk patient, with previously identified type of pathogen.
K. Moghissia,, M. Miglioreb
aThe Yorkshire Laser Centre, Goole & District Hospital,Woodland Avenue, Goole, East Yorkshire, DN14 6RX, UK
bGeneral Thoracic Surgery, Department of Surgery, University of Cantania, Cantania, Italy
Corresponding author. Tel./fax: +44-1724-290456.E-mail address: kmoghissi@yorkshirelasercentre.org
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Top
Abstract
1. Introduction
