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(Chest. 2005;128:2647-2652.)
© 2005 American College of Chest Physicians

Nosocomial Infection After Lung Surgery*

Incidence and Risk Factors

Daniel N. Nan, MD; Marta Fernández-Ayala, MD; Concepción Fariñas-Álvarez, MD, PhD; Roberto Mons, MD, PhD; Francisco J. Ortega, MD, PhD; Jesús González-Macías, MD, PhD and M. Carmen Fariñas, MD, PhD

* From the Infectious Diseases Unit, Department of Internal Medicine (Drs. Nan, Fernández-Ayala, González-Macías, and M.C. Fariñas), Division of Preventive Medicine (Dr. C. Fariñas), and Department of Thoracic Surgery (Drs. Mons and Ortega), Hospital Universitario Marqués de Valdecilla, University of Cantabria, Santander, Spain.

Correspondence to: M. Carmen Fariñas, MD, PhD, Infectious Diseases Unit, Department of Internal Medicine, Hospital Universitario Marqués de Valdecilla, Avda. Valdecilla s/n, E-39008 Santander, Spain; e-mail: mirfac{at}humv.es


   Abstract
TOP
 Abstract
Introduction
 Materials and Methods
 Results
 Discussion
 References
 
Study objectives: To assess the incidence and risk factors for nosocomial infection after lung surgery.

Design: Prospective cohort study.

Setting: Service of thoracic surgery of an acute-care teaching hospital in Santander, Spain.

Patients: Between June 1, 1999, and January 31, 2001, all consecutive patients undergoing lung surgery were prospectively followed up for 1 month after discharge from the hospital to assess the development of nosocomial infection, the primary outcome of the study.

Interventions: During the hospitalization period, patients were visited on a daily basis. Postdischarge surveillance was based on visits to the surgeon.

Measurements and results: We studied 295 patients (84% men; mean age, 60.9 years), 89% of whom underwent resection operations. Ninety episodes of nosocomial infection were diagnosed in 76 patients, including pneumonia (n = 10), lower respiratory tract infection (n = 47), wound infection (n = 16; one third were detected after hospital discharge), urinary tract infection (n = 9), and bacteremia (n = 8; three fourths were catheter-related bacteremia). Twenty patients had severe infections (pneumonia or empyema), with a mortality rate of 60%. COPD (adjusted odds ratio [OR], 2.70; 95% confidence interval [CI], 1.52 to 4.84), duration of surgery with an increased risk for each additional minute (Mantel-Haenzel {chi}2 test for trend, p = 0.037), and ICU admission (OR, 3.69; 95% CI, 1.94 to 7.06) were independent risk factors for nosocomial infection. The use of an epidural catheter was a protective factor (OR, 0.45; 95% CI, 0.22 to 0.95). There were no differences according to the use of amoxicillin/clavulanate or cefotaxime for surgical prophylaxis.

Conclusions: Nosocomial infections are common after lung surgery. One third of wound infections were detected after hospital discharge. The profile of a high-risk patient includes COPD as underlying disease, prolonged operative time, and postoperative ICU admission.

Key Words: lung resection • nosocomial infection • risk factors • thoracic surgery


   Introduction
TOP
 Abstract
 Introduction
Materials and Methods
 Results
 Discussion
 References
 
Operative mortality and morbidity after lung surgery has decreased over the past decade,1 mostly in association with substantial improvement in the postoperative care of patients and advances in anesthetic techniques. However, postoperative infection is one of the major morbidity factors after thoracic surgery.2 Pneumonia, wound infection, and empyema account for 11 to 46% of postoperative infections in patients undergoing pulmonary surgery.234567891011 Differences in the reported prevalence rates are related to criteria employed to diagnose the major categories of infection, type of surgery, and use of different preoperative prophylactic antibiotic regimens.23471011 Several studies1213 have documented that an important proportion of postoperative infections develop after discharge from the hospital, and it has been emphasized that reliable methods for identifying postdischarge wound infections are necessary to ensure accurate surgical wound infection rates. However, the incidence of nosocomial infections has been determined in specific groups of patients to evaluate the relationship between hospital-acquired infection and patient outcomes, such as in patients undergoing cardiac surgery,14 but there is limited information regarding nosocomial infections in patients undergoing pulmonary surgery. Risk factors identified for the development of a nosocomial infection include patient-related variables and extrinsic factors associated with the surgical procedure and hospitalization.914 However, predisposing factors for nosocomial infection in the subset of adult patients undergoing lung surgery were not prospectively assessed. Therefore, a prospective cohort study was designed to assess the incidence and risk factors of nosocomial infection after lung surgery, including wound infections detected after hospital discharge.


   Materials and Methods
TOP
 Abstract
 Introduction
 Materials and Methods
Results
 Discussion
 References
 
Study Location and Patients
The study was conducted at a university-affiliated teaching hospital, Marqués de Valdecilla (1,100 beds), in Santander, Spain. The Division of Thoracic Surgery includes four staff surgeons and one resident. Approximately 400 thoracic procedures are performed annually, 150 of which are lung resections. During a 19-month period (June 1999 to January 2001), all patients undergoing pulmonary surgery were potentially eligible for this investigation. Patients < 14 years of age and patients undergoing lung transplantation were excluded. The study was approved by the institutional review board.

Study Design and Data Collection
Patients were visited on a daily basis to collect all pertinent data, which was recorded on a standardized data collection form. The following characteristics were prospectively recorded by one of the investigators: age; sex; body mass index; smoking history; alcohol consumption; presence of COPD; diabetes mellitus; hypoalbuminemia (serum albumin level < 3 g/L); anemia (hemoglobin < 12 g/dL); renal failure (serum creatinine level > 2 mg/dL); preoperative American Society of Anesthesiologists (ASA) physical status15; FEV1; preoperative length of hospital stay; duration of surgery from the first skin incision until closure; type of lung surgery performed (pneumonectomy, lobectomy, other lung and chest wall resections); whether the surgery was performed on an emergent basis; blood transfusion; reoperation; placement of a central venous catheter; use of mechanical ventilation; use of a nasogastric tube; and urinary tract catheterization (including dates of starting and ending).

Postoperative care was consistent across patients. Standard measures included bronchial hygiene therapy started in the immediate postoperative period, which included aggressive chest physiotherapy, incentive spirometry, control of secretions, and early ambulation with exercising in the inpatient pulmonary rehabilitation unit. Antibiotic prophylaxis included the administration of cefotaxime, 2 g q6h IV for 48 h (from June 1999 to December 1999), and amoxicillin/clavulanate, 1 g q8h IV for 48 h (from January 2000 to January 2001). Hospital infections were identified through active concurrent surveillance and were diagnosed according to Centers for Disease Control and Prevention criteria.1617

Major categories of infection included pneumonia, lower respiratory tract infection, and catheter-related bloodstream infection. Pneumonia was diagnosed by the presence of new and/or progressive pulmonary infiltrates on chest radiography plus two or more of the following criteria: fever (> 38°C), leukocytosis (12 x 109/L), purulent sputum, or isolation of pathogen in respiratory secretions. Lower respiratory tract infection was defined as the presence of purulent tracheobronchial secretions plus two or more of the following criteria: fever (> 38°C), leukocytosis (12 x 109/L), or significant bacteriologic counts in respiratory secretions in patients without pulmonary infiltrates, suggesting pneumonia on the chest radiograph. Catheter-related bloodstream infection was defined as the isolation of the same organism (ie, identical species and antibiotic susceptibility pattern) from culture of a catheter segment and from the blood in a patient with suggestive clinical symptoms of bloodstream infection and no other apparent source of infection. In the absence of laboratory confirmation, defervescence after removal of an implicated catheter from a patient with bloodstream infection was considered indirect evidence of catheter-related bloodstream infection.

For the purpose of this study, surveillance was extended to 30 days after hospital discharge to detect hospital infections developing at home. Postdischarge surveillance was based on scheduled visit to the surgeon.

Statistical Analysis
For each category of potential risk factors for infection, the incidence of nosocomial infection was calculated by dividing the number of events by the number of patients in each category. Relative risks (RRs) and their 95% confidence intervals (CIs) were calculated. All tests of significance were two tailed, and p values ≤ 0.05 were considered to indicate statistical significance. Multiple logistic regression analysis was performed to identify variables that were significantly related to the likelihood of developing nosocomial infection. Potential predictor variables for model entry were identified using univariate analysis. Regression models were controlled for the effects of confounding variables. Results of the logistic regression analysis are reported as adjusted odds ratios (ORs) with 95% CIs. Statistical analyses were performed software (Stata Corporation; College Station, TX).


   Results
TOP
 Abstract
 Introduction
 Materials and Methods
 Results
Discussion
 References
 
Patients
A total of 295 consecutive patients undergoing lung surgery were prospectively evaluated. The mean age of the patients was 60.9 years (range, 14 to 83 years); 247 patients were men. The mean (± SD) length of preoperative stay was 3.0 ± 3.5 days. The surgical procedures performed included pneumonectomy (n = 78), lobectomy (n = 110), lung-sparing procedures (n = 76), and other surgical procedures (n = 31; including chest wall resections). Lung cancer was diagnosed in 231 patients, and benign pulmonary conditions were found in 64 patients. The most common histologic type was squamous cell carcinoma (109 patients), followed by adenocarcinoma (67 patients). Histologically, obstructive pneumonitis secondary to lung cancer was shown in 54 patients. Four patients (1.4%) underwent urgent surgery. The mean (± SD) duration of operation was 110.9 ± 49.2 min. A total of 14 patients died during hospitalization (inpatient mortality rate, 4.8%). Postdischarge surveillance could not be completed in 17 patients (6%) because their place of residence was far away from the hospital.

Incidence of Nosocomial Infection
Nosocomial infections developed in 76 patients (25.8%). Sixty-four patients presented a single infection episode, 10 patients had two infection episodes, and 2 patients had three episodes, a total of 90 nosocomial infections. These included respiratory infection (n = 57; pneumonia [n = 10], lower respiratory tract infection [n = 47]), wound infection (n = 16), urinary tract infection (n = 9), and bacteremia (n = 8; three fourths were catheter-related bloodstream infection). Of the 16 cases of surgical site infection, 11 were diagnosed during hospitalization and 5 were diagnosed after hospital discharge. In the group of 16 surgical site infections that occurred during inpatient care, there was 1 case of superficial surgical wound infection, 3 cases of deep wound infection, and 7 cases of infections in organs or spaces (empyema [n = 6] and mediastinitis [1]). In the group of postdischarge surgical site infections, there was one case of superficial wound infection, one case of deep wound infection, and three cases of infections in organs of spaces (these patients were readmitted to the hospital and required reoperation). Sepsis developed in 28 of the 76 patients with infection (36.8%).

Microorganisms were isolated in 14 cases (24.6%) of respiratory infection, in 13 cases (81.2%) of wound infection, in 5 cases (55.6%) of urinary tract infection, and in all cases of bacteremia. Those most commonly isolated pathogens were Staphylococcus aureus and coagulase-negative Staphylococcus, Pseudomonas aeruginosa, and Escherichia coli (Table 1 ).


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  		Table 1.. Microorganisms Isolated According to Type of Infection*

 
The mean length of hospital stay was significantly longer in patients with nosocomial infection than in patients without nosocomial infection (18.0 ± 10.4 days vs 11.5 ± 5.8 days, p < 0.001). Fourteen patients (4.74%) died during the postoperative period; in 8 of these patients (57.1%), death was related to the infectious process. Differences in risk of death or duration of hospital stay among types of infection were not observed.

Antibiotic Prophylaxis
A total of 283 patients received perioperative antibiotic prophylaxis: cefotaxime (n = 96), amoxicillin/clavulanate (n = 174), and vancomycin or teicoplanin due to penicillin allergy (n = 13). There were no statistically significant differences in the risk of infections between the two first regimens (RR, 1.41; 95% CI, 0.9 to 2.3).

Risk Factors
With regard to preoperative variables (Table 2 ), COPD (OR, 2.70; 95% CI, 1.5 to 4.8), FEV1 < 1,500 mL (OR, 2.46; 95% CI, 1.1 to 6.0), ASA physical status > 3 (OR, 1.82; 95% CI, 1.1 to 3.3), and anemia (serum hemoglobin < 12 g/dL) [OR, 1.90; 95% CI, 1.1 to 3.5] were risk factors for nosocomial infection. Other comorbidities (eg, chronic heart failure), body mass index, hypoalbuminemia, and renal failure as well as the length of preoperative stay were not identified as risk factors for the development of nosocomial infection. In relation to intraoperative events (Table 3 ), risk factors included the duration of surgery, with an increased risk for each additional minute of surgery (Mantel-Haenzel {chi}2 test for trend, p = 0.037) and the type of operation, with higher risk for other surgical procedures, which included chest wall resections and mediastinal surgery (OR, 2.79; 95% CI, 1.0 to 7.4). Patients with COPD were predisposed to respiratory infection (RR, 2.08; p = 0.002) and wound infection (RR, 2.77; p = 0.07). The corresponding figures for patients with FEV1 < 1,500 mL were RR of 2.27 (p = 0.004) for respiratory infection and RR of 1.89 (p = 0.39) for surgical site infection.


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  		Table 2.. Preoperative Variables and Risk for Nosocomial Infection

 

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  		Table 3.. Intraoperative Variables and Risk for Nosocomial Infection

 
The analysis of postoperative variables (Table 4 ) showed that admission to the ICU (OR, 3.69; 95% CI, 1.9 to 7.0) with an increased risk for each additional day of ICU stay (Mantel-Haenzel {chi}2 test for trend, p = 0.018) was an independent risk factor for the development of a nosocomial infection. Mechanical ventilation for > 1 day, placement of a central venous catheter, as well as use of a nasogastric tube and urinary tract catheterization for > 1 day increased the risk for nosocomial infection, but statistical significance was not reached. A total of 229 patients (77.6%) received an epidural catheter, and this was found to be a protective factor against nosocomial infection (OR, 0.45; 95% CI, 0.2 to 0.9).


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  		Table 4.. Postoperative Variables and Risk for Nosocomial Infection

 

   Discussion
TOP
 Abstract
 Introduction
 Materials and Methods
 Results
 Discussion
References
 
This study shows that nosocomial infections are common among patients undergoing lung surgery, with a rate of 25.8%. As far as we are aware, this is the first epidemiologic study of nosocomial infections in the subset of patients undergoing pulmonary surgery. Previous studies211 were comparative studies of antibiotic prophylactic regimens or studies on mortality. We included all types of infections, varying from respiratory or wound infections developing in patients undergoing major operations, such as pneumonectomy or chest wall resection, to minor infections, such as urinary infections or catheter-related bacteremia, because any type of infectious complication increases postoperative morbidity. In addition, postdischarge surveillance of patients for 1 month allowed detection of one third of the surgical site infections. In agreement with other reports,1213 this finding emphasizes that reliable methods for identifying postdischarge wound infections are necessary to ensure accurate surgical wound infection rates. Severe postoperative infections, such as pneumonia or empyema, were less frequent than in other reports, in which empyema accounted for 7.5% of all postoperative infections.1819 We also found that the presence of a nosocomial infection increases the length of hospital stay and the inpatient mortality rate.14

Predominantly isolated bacteria included Gram-negative bacilli and Gram-positive cocci, which are typical causative pathogens of hospital infections and are usually associated with the hospital environment.2714 We did not find significant differences regarding infection between the two prophylactic regimens, likely because microorganisms resistant to our prophylactic antibiotic caused most of the infections.

Similar to a series14 of cardiac surgery in which COPD was shown to be a risk factor for postoperative infection including mediastinitis, in our study COPD and FEV1 < 1,500 mL were the most important host factors for nosocomial infection. Several studies820 have correlated poor pulmonary function with increased morbidity and mortality after thoracotomy. Anemia and ASA physical status were predisposing factors for infection. Anemia frequently develops in cancer patients due to the cancer itself or to the effects of cancer-related therapy.21 However, ASA physical status grouping has been shown to be a highly predictive variable of postoperative wound infections in surgery patients.22 An ASA score ≥ 3 has been reported as an independent factor associated with postoperative pulmonary complications after lung resection.5 The high operative risk commonly cited in patients > 70 years old has led some authors to conclude that advanced age is a contraindication to pulmonary resection, but other authors have demonstrated satisfactory long-term survival following pulmonary resection in the elderly.523 In our study, age was not found to be a risk factor for postoperative infection. It seems that postoperative infections in patients undergoing pulmonary surgery are more strongly related to coexisting conditions than to chronologic age.

A history of smoking has been correlated with postoperative pneumonia and mediastinitis, with subsequent impairment in ciliary mobility and altered bronchial mucosa,724 although in this study smoking did not affect the incidence of postoperative infection. Local factors, such as the presence of cancer or obstructive pneumonia, were not found to be risk factors for postoperative infection; probably the use of antibiotic prophylaxis and an adequate surgical technique may have a higher influence to reduce the development of postoperative infections. The duration of operation and the need for reoperation were significantly associated with an increased risk for nosocomial infection, as reported in other groups of surgical patients.22 The most complex surgical operations, such as pneumonectomies and those involving wall resection, are recognized as one of the primary risk factors for mortality and in this study were also found to be risk factors for postoperative infection.6

Almost all of postoperative variables studied increased the risk for nosocomial infection, but only admission to the ICU was a significant independent variable associated with infection. Patients admitted to the ICU appear to be at increased risk for the development of nosocomial infection due to a number of factors, including severity of illness and utilization of invasive devices.14 Although the timing of chest tube removal had been correlated with the developing of empyema, the use of thoracic tube for > 3 days was not associated with postoperative infection.18 In our study > 75% of patients received an epidural catheter. It is well known that pain control in patients undergoing pulmonary surgery allows early active physiotherapy to prevent pulmonary complications.25 Placement of an epidural catheter appeared to be a protective factor after adjusting for age, sex, smoking status, COPD, duration of surgery, and side of thoracotomy. However, the lack of an epidural catheter would hardly identify a particular group of patients with unique characteristics.

We conclude that nosocomial infections are relatively frequent after lung surgery. Some types of postoperative infections are severe and associated with high mortality. Besides the presence of COPD, which is an intrinsic patient-related factor, all other risk factors for nosocomial infection were associated with intraoperative and postoperative variables, particularly duration of operation and need of postoperative care in the ICU setting. More studies are necessary to identify risk factors for nosocomial infection in lung surgery patients and to find new strategies to diminish infection rates in this subgroup of patients.


   Acknowledgements
 
We thank Marta Pulido, MD, for editorial assistance.


   Footnotes
 
Abbreviations: ASA = American Society of Anesthesiologists; CI = confidence interval; OR = odds ratio; RR = relative risk

Dr. Nan received a fellowship from the "Fundación Marqués de Valdecilla," Santander, Spain.

Received for publication January 7, 2004. Accepted for publication April 13, 2005.


   References
TOP
 Abstract
 Introduction
 Materials and Methods
 Results
 Discussion
 References
 

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