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Ann Thorac Surg 2007;84:1669-1673. doi:10.1016/j.athoracsur.2007.05.059
© 2007 The Society of Thoracic Surgeons
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Original Articles: General Thoracic

Postoperative Pneumonia After Major Pulmonary Resections: An Unsolved Problem in Thoracic Surgery

Dana M. Radu, MDa,*, Françoise Jauréguy, Pharm Db, Agathe Seguin, MDa, Clément Foulon, Pharm Db, Marie Dominique Destable, MDa, Jacques Azorin, MDa, Emmanuel Martinod, MD, PhDa

a Department of Thoracic and Vascular Surgery, Avicenne Hospital, Bobigny, and Assistance Publique des Hôpitaux de Paris, Paris XIII University, Paris, France
b Department of Microbiology and Hygiene, Avicenne Hospital, Bobigny, and Assistance Publique des Hôpitaux de Paris, Paris XIII University, Paris, France

Accepted for publication May 22, 2007.

* Address correspondence to Dr Radu, Laboratoire d’Etudes des Greffes et Prothèses Cardiaques, Hôpital Broussais, 96 rue Didot, Paris Cedex 14, 75014, France (Email: danabudescu{at}gmail.com).


   Abstract
Top
 Abstract
Introduction
 Patients and Methods
 Results
 Comment
 References
 
Background: Antibiotics currently recommended for prophylaxis in thoracic surgery are first-generation and second-generation cephalosporins. Despite this prophylaxis, postoperative pneumonia after major pulmonary resections remains frequent and severe. However, in the medical literature, the origin of these infections is poorly documented.

Methods: To evaluate the efficiency of current prophylactic regimens, we retrospectively analyzed 312 consecutive cases of major pulmonary resection, performed between January 2000 and December 2004. For patients who experienced postoperative pulmonary infection, the microbiologic agents and their antibiotic susceptibility were studied.

Results: A postoperative pneumonia was diagnosed in 76 patients (24.4% ± 0.43%). Sixty patients (78.9%) experienced the infection in the first 5 postoperative days. A microbiologic documentation was obtained in 44 cases (57.9%) with 56 microorganisms involved. Pathogens responsible for the infections were Staphylococcus aureus (n = 10), Streptococcus pneumoniae (n = 8), group B Streptococcus organisms (n = 1), nongroupable Streptococcus organisms (n = 2), Enterococcus faecalis (n = 1), Haemophilus spp. (n = 9), Branhamella catarrhalis (n = 2), Enterobacteriaceae (n = 15), Pseudomonas aeruginosa (n = 3), Acinetobacter baumannii (n = 1), and Candida spp. (n = 4). According to the antibiotic susceptibility testings, the prophylactic regimen by cefazolin proved ineffective for 84% of the microbiologically documented cases.

Conclusions: This study confirmed the inefficiency of current prophylaxis against pathogens involved in postoperative pneumonia after major lung resections. Evaluation of new and more-adapted approaches of antibiotic prophylaxis should be the subject of prospective multicenter trials.


   Introduction
Top
 Abstract
 Introduction
Patients and Methods
 Results
 Comment
 References
 
Patients undergoing major pulmonary resections are at high risk of experiencing pulmonary infections in the postoperative period. Despite a correct use of antibiotic prophylaxis recommended today, the prevalence of these infections has reached more than 20% in recent studies [1, 2].

Presently, there are no specific guidelines regarding antibiotic prophylaxis for pulmonary surgery. Current recommendations [3, 4] enclose pulmonary resections in the vast category of "cardiothoracic surgery," therefore applying the same antibiotic prophylactic regimen as for cardiac surgery. Agents proposed are first-generation and second-generation cephalosporins (eg, cefazolin, cefuroxime, and cefamandole). In case of ß-lactam allergy, vancomycin or clindamycin are the alternatives. In cardiac surgery these antibiotics are targeted against surgical wound contaminants, mainly skin flora and their contaminants, and their aim is to reduce the rate of surgical wound infections [5, 6].

According to these recommendations [3], today’s usual practice in general thoracic surgery in France for antibiotic prophylaxis is the use of one or two doses of cefazolin, depending on the duration of the surgical intervention, therefore intended to reduce only the surgical wound infections.

Pulmonary surgery is quite different from cardiac and mediastinal surgery, regarding pathologic diagnosis, organs involved, and contamination class. Cardiac surgery is considered as clean surgery (class I of Altemeier’s Classification of Surgical Wound Contamination). In contrast, pulmonary surgery is a clean-contaminated surgery (Altemeier’s class II) as the bronchus or trachea is opened during the procedure. As a result, besides skin flora, microbiologic pathogens responsible for postoperative infections belong also to oropharyngeal flora and contaminants, with subsequent tracheobronchial colonization.

Infectious complications after pulmonary surgery include operative wound infection, empyema, and nosocomial pneumonia. Antibiotic prophylaxis should therefore be guided against these three entities.

Although the rate of operative wound infections has declined ever since the use of first-generation and second-generation cephalosporins in prophylaxis [7–9], this is not the case for empyema or postoperative pneumonia. The first prospective trial investigating the benefits of antibiotic prophylaxis in elective pulmonary resections demonstrated a significantly reduced rate of postoperative pneumonia [10]. However, in this trial, Kvale and coworkers [10] used a 5-day cefazolin schedule, which is more a treatment approach than a prophylaxis. To our knowledge, no other study has shown a significant reduction of this type of complication with the prophylactic use of first-generation or second-generation cephalosporins.

In this context, the aim of this study is to analyze the causative agents responsible for postoperative pneumonia and their antibiotic susceptibility spectra to evaluate the efficiency of current prophylactic antibiotic regimen.


   Patients and Methods
Top
 Abstract
 Introduction
 Patients and Methods
Results
 Comment
 References
 
Population
Between January 1, 2000, and December 31, 2004, a total of 326 major pulmonary resections (pneumonectomy, lobectomy, or bilobectomy) were performed in our department. Data were analyzed retrospectively with the approval of our institutional review board. Individual consent was not required. Information was obtained reviewing the hospital records of all these patients for demographic characteristics, preoperative pulmonary status, and postoperative course.

Exclusion criterion was a history of antibiotic therapy in the 14-day period that preceded the operation with or without preoperative pulmonary infection. Thus, 312 cases of major pulmonary resections were retained for analysis.

Patients who experienced postoperative pulmonary infections were evaluated for microorganisms involved and their antibiotic susceptibility, delay of manifestation, and hospital mortality. The diagnosis of pneumonia was made on the basis of a composite item of clinical, radiologic, and bacteriologic criteria of nosocomial pneumonia [11]. For patients who had repetitive pneumonia, only the first episode was considered. Characteristics of patients who exhibited postoperative pulmonary infections and of those who did not are summarized in Table 1.


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  		Table 1 Patients’ Characteristics a
 
According to the recommendations of The French Society of Anesthesiology [3], the antibiotic prophylaxis used for pulmonary surgery was cefazolin (a first-generation cephalosporin), 2 g at the induction of the anesthesia, followed by cefazolin, 1 g every 4 hours, if the operation lasted more than 4 hours.

Strains and Antibiotic Susceptibility
Pulmonary samples were obtained by sputum, endotracheal aspirate, bronchoalveolar lavage, protected specimen brush, or blinded plugged telescopic catheter. Samples were transferred to the microbiology laboratory within 30 minutes for Gram staining and culture. Quantitative cultures were performed. Vortexed, undiluted samples (1 mL) were used to prepare 10–3 and 10–5 dilutions. From each dilution, 0.1 mL was plated for aerobic and anaerobic culture on blood agar, selective blood agar with colistin (10 µg/mL) and nalidixic acid (15 µg/mL), and IsoVitaleX chocolate agar for culture in CO2 (5 %). Cultures were evaluated after 24 and 48 hours at 37°C. The number of bacteria in the original sample was expressed in colony-forming units per milliliter of the original 1-mL sample (CFU/mL).

We used the previously established quantitative threshold for positive cultures: ≥107 CFU/mL for sputum, ≥105 CFU/mL for endotracheal aspirate, ≥104 CFU/mL for bronchoalveolar lavage, and ≥103 CFU/mL for protected specimen brush or plugged telescopic catheter [12].

Bacteria were identified by conventional methods, and antibiotic susceptibility was determined on Mueller Hinton agar by the agar diffusion method according to CA-SFM standards (Comité de L’Antibiogramme de la Société Française de Microbiologie [The Group for Antibiotic Susceptibility from the French Society of Microbiology]) [13].

Statistical Analysis
Statistical analysis was performed using SPSS Base12.0 statistical software (SPSS Inc, Chicago, IL). Categorical variables are presented as percentages ± standard deviation, calculated assuming normal distribution.


   Results
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 Abstract
 Introduction
 Patients and Methods
 Results
Comment
 References
 
Seventy-six cases (24.4% ± 0.43%) of major pulmonary resections were complicated with postoperative pulmonary infections. Seventy-six different patients were involved, of whom 62 (81.6%) were men. Age range varied between 35 and 88 years (mean age, 63.5 years).

Most of the pneumonia cases occurred in the first 5 postoperative days (60 patients, 78.9%; Fig 1). In-hospital mortality rate among patients presenting with postoperative pneumonia was 26.3% ± 0.443% (20 patients), whereas patients who did not experience pneumonia had an in-hospital mortality rate of 3.4% ± 0.181%, resulting in an overall mortality of 8.9% ± 0.286%.


Figure 1
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  		Fig 1. Onset of postoperative pneumonia in patients after lung resection.

 
Among the 76 postoperative pulmonary infections, pathogens were identified in 44 patients (57.9%). The remaining 32 pneumonias (42.1%) were not microbiologically documented. Of the 44 microbiologically documented cases, 11 were polymicrobial.

A total of 56 pathogenic microorganisms was recovered from 2 sputum samples, 21 endotracheal aspirates, 11 bronchoalveolar lavage, and 6 protected specimen brush and 4 plugged telescopic catheter procedures. The identification of germs and their susceptibility to first-generation cephalosporins are presented in Table 2. Enterobacteriaceae organisms (26.9%), Staphylococcus aureus (17.9%), Haemophilus spp. (16.1%), and Streptococcus pneumoniae (14.3%) were the germs most frequently responsible for postoperative pneumonia.


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  		Table 2 Pathogens Responsible for Postoperative Pneumonia and Their Susceptibility to First-Generation Cephalosporins (Cefazolin)
 
According to their antibiotic susceptibility testing, 17.9% of the 56 identified germs were susceptible to cefazolin. Among the 11 polymicrobial cases of pneumonia, none were susceptible to first-generation cephalosporins. Therefore, for 84% of the documented cases,cefazolin was not effective.


   Comment
Top
 Abstract
 Introduction
 Patients and Methods
 Results
 Comment
References
 
This study highlights that despite currently used antibiotic prophylaxis, postoperative pulmonary infection still represents an important problem after major pulmonary resection surgery. In this frequent complication, associated with high mortality rate, cultures recover mostly microorganisms not susceptible to the agents used in prophylaxis.

One of the main concerns of postoperative pneumonia is its prevalence and its outcome. The rate differs among studies and may be related to the criteria used in defining the pulmonary infection, the pathologic entity included in the study, and the type of lung resection performed. As a result, it varies from 5% to 6% [14, 15] to about 20% [1, 16]. In our group of patients, the prevalence of postoperative pneumonia was as high as 24.4%, and this is in agreement with other authors who took into account only major lung resections [2]. As a consequence to nosocomial pneumonia after thoracic surgery procedures, studies have shown increased hospital mortality in these patients, up to 19% [1, 2], as well as increased length of hospital stay and costs [17]. In our group, the mortality among the 76 patients experiencing postoperative pneumonia was also high: 26.3% ± 0.443%, despite intensive postoperative measures meant to facilitate airway clearance, such as chest physical therapy, pain control, bronchodilators, and early ambulation. The in-hospital 30-day mortality rates we observed in the entire cohort and in the subgroup of patients who had postoperative pneumonia were similar to those of other French studies [2].

The microorganisms implicated in this complication are related to the colonization of the tracheobronchial tree. In our study, 53.6% of the germs identified were gram-negative bacteria, 39.3% gram-positive bacteria, and 7.1% were fungi. The gram-positive germs encountered are common respiratory pathogens. Fifty percent of the microorganisms responsible for postoperative pulmonary infection were gram-negative bacilli. These germs are consistently associated with nosocomial pneumonia [18], and this is owing to the colonization of oropharyngeal and tracheobronchial tree. Indeed, the study of Sok and colleagues [19] shows that there is substantial difference in the microbiologic patterns of sputum between the preoperative and the early postoperative period, with a predominance of gram-negative bacteria in postoperative sputum. The change in these patterns is thought to be favored by contamination during the early postoperative period by mechanisms such as aspiration of gastric contents and airway manipulations in the intensive care units.

Several studies have looked into the impact of airway colonization with potentially pathogenic microorganisms in patients with pulmonary resections. Whether already present at the time of operation [2, 20, 21] or acquired in the early postoperative period [19], airway colonization was found to represent a risk factor for the development of postoperative pulmonary infection.

Regarding the Candida species recovered from our patients with postoperative pneumonia, there is a controversy whether these germs should be considered etiologic or colonizing agents [12].

In our study, we investigated the susceptibility of the microorganisms recovered from postoperative pneumonia to cefazolin. In only 17.9% of cases, antibiotic prophylaxis by cefazolin was appropriate. As second-generation cephalosporins are also recommended for antibiotic prophylaxis in pulmonary surgery, we also looked for the activity of these agents against the isolates (data not shown). Among the isolated microorganisms, besides those susceptible to first-generation cephalosporins, only Haemophilus spp. would have added to the susceptibility spectrum of second-generation cephalosporins, according to their minimal inhibitory concentrations [22]. Thus, second-generation cephalosporins would not have been effective in 70.5% of microbiologically documented cases.

The use of first-generation or second-generation cephalosporins for antibiotic prophylaxis [3, 4] in general thoracic surgery is based on several prospective randomized trials [8–10, 23], which compared the effect of these drugs against placebo. The authors looked for an influence of these antibiotics on all the three types of infectious complications of pulmonary surgery, namely wound infection, empyema, and postoperative pneumonia. The results of these trials proved that first-generation or second-generation cephalosporins significantly reduced the rate of wound infection, but did not control empyema or pneumonia.

As shown by our investigation, one of the reasons for that appears to be that first-generation and second-generation cephalosporins are not appropriate for the microorganisms encountered in pneumonia after major pulmonary resections. On the one hand this is explained by the high rate of gram-negative bacteria associated with postoperative pneumonia. Except for some strains of Enterobacteriaceae spp, most of the gram-negative bacilli isolated in hospital-acquired pneumonia are resistant to these antibiotics. In our study, first-generation or second-generation cephalosporins were active on only 3 of the 15 recovered strains of Enterobacteriaceae spp.

In our study, pulmonary infection commonly developed early in the postoperative period, 78.9% in the first 5 postoperative days. The associated high rate of early-onset pneumonia [18] could be explained by the particular early postoperative setting of patients with major lung resections, which favors the accumulation of airway secretions. Therefore, the question that ensues is this: would postoperative pneumonia occur less often if antibiotic prophylaxis covered the early postoperative period, most liable to infective complications?

Recently, The Society of Thoracic Surgeons has published new guidelines for antibiotic prophylaxis in cardiac surgery [5, 6]. Recommended antibiotic prophylaxis addresses the main postoperative infectious problems in cardiac surgery, represented by the surgical site infections, with mediastinitis at the extreme of the spectrum. This prophylaxis is targeted against the most frequent microorganisms involved. At no point did these guidelines analyze the postoperative infectious complications and microbiologic spectra in pulmonary surgery, as they specifically address cardiac surgery. Nevertheless, some problems, shared also by pulmonary surgery, are debated: the rationale of adding a gram-negative effective antibiotic [6] and duration of prophylaxis [5].

In our opinion, besides surgical wound infections, antibiotic prophylaxis in thoracic surgery should also address empyema and postoperative pneumonia. The justification for this is that pneumonia developing after major pulmonary resections is a postoperative complication, it develops early in the postoperative period, it is associated with a high mortality rate, and it is caused by perioperative airway manipulation and favored by the surgical intervention.

Presently, few trials have studied the efficiency of other antibiotic agents, like ampicillin associated with sulbactam [24] or third-generation cephalosporins [25], which appear to reduce the rate of postoperative pneumonia. Likewise, few prospective studies are available regarding the effect of longer-duration regimens [7, 26], with controversial results concerning the control of postoperative infections. Meanwhile, the use of prophylactic antibiotics throughout thoracic surgery departments remains inconsistent [27]. These facts reflect the necessity of establishing an antibiotic prophylactic regimen specifically designed for lung resections.

In France, the use of the combination of amoxicillin and clavulanic acid, 2 g and 200 mg, respectively, every 8 hours for 24 hours, to reduce postoperative pneumonia after major lung resection is proposed to be evaluated in a large randomized multicenter trial. This approach was recommended by Schussler and associates [28]. According to its activity spectrum, this antibiotic would better cover both gram-positive and gram-negative bacteria involved in postoperative pneumonia. A 24-hour regimen would protect the postoperative period most favorable to airway colonization, without the risk of developing bacterial resistance [5].

Postoperative pneumonia after major lung resection remains a frequent and feared complication, in view of its outcome. Therefore more effort should be made regarding the control of factors that may influence its development. From this perspective, we believe that antibiotic prophylaxis in pulmonary resection surgery should be targeted not only toward surgical wound infections but also against postoperative pneumonia, which should be considered indeed a surgical site infection after major lung resection.


   References
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 Abstract
 Introduction
 Patients and Methods
 Results
 Comment
 References
 

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