In this retrospective study, surgical outcomes were poor, with a higher in-hospital mortality rate observed among patients with a common pathogen in the intraoperative pleural fluid/tissue culture and a respiratory secretion culture set. After confirming diagnosis of stage II to stage III thoracic empyema, decortication was performed, and pleural fluid and tissue cultures were obtained intraoperatively. Additionally, respiratory secretion cultures were obtained if recurrence or progression of the pulmonary infection was suspected, and antibiotic use was adjusted accordingly. To explain the higher in-hospital mortality in the identical pathogen group, the consistency between a patient’s respiratory secretion culture and intraoperative pleural fluid/tissue culture may imply the larger bacterial colony, the development of drug resistance, the inefficacy of antibiotics treatment, or inadequate length of therapy. It is essential for surgeons to recognize this result to consider the causes for improving surgical outcomes.
A previous study revealed that approximately twenty percent of community-acquired pneumonia cases developed parapneumonic effusions, and only 1.4% of those met the criteria of empyema.[15] The upper airway appears to be the most common route of pathogen invasion, and the cause of secondary bacterial invasion to pleural space is not completely understood. Several studies suggest that pleural infection can occur spontaneously even in the absence of underlying lung consolidation.[16–18] This finding implies there is another route causing infection in the pleural space. Possible mechanisms include visceral pleural defects or fistula formation, dispersion from the mediastinum, transdiaphragmatic infection, hematogenous spread, and trauma or iatrogenic injury.[19] In our data, 195 out of 225 patients had completely different pathogens cultured from respiratory secretion specimens and pleural space.
Based on positive interoperative pleural effusion or tissue culture findings, we differentiated the methods of obtaining respiratory secretion cultures to determine the most effective one for pathogen identification. In an early research, Fabrice et al. investigated the role of routine endotracheal aspiration respiratory secretion culture on ventilator-associated pneumonia (VAP) patients. They compared endotracheal aspiration culture results to positive BAL cultures and found an 82% identical rate among the patients with less than 5 days of mechanical ventilation and an 86% identical rate among those with more than 5 days of mechanical ventilation.[20] This suggests that VAP can be detected sooner, allowing for the prescription of adequate antibiotics for treatment. However, Johannes et al. recently reviewed diagnostic studies of endotracheal aspiration and BAL culture methods for VAP and concluded in favor of BAL analysis due to the poor positive predictive value of endotracheal aspiration cultures.[21] In our research, the positive rate of BAL cultures is higher than endotracheal aspiration cultures (40% versus 32%), and the comparison of concordance rates to the pleural cultures showed an opposite result that was not statistically significant (25% versus 37%, p = 0.346). Both endotracheal aspiration and BAL culture methods provide an efficacy in antibiotic therapy adjustment and surgical outcome prediction in empyema patients.
The pathogen spectrum varies geographically and in terms of the timing of cultures. In a major review of microbiology of pleural infection by Hassan et al, Staphylococcus aureus was reported as the most common organism worldwide, with pneumococci and viridans streptococci being the most common organism in tropical regions.[22] The cases we collected were all from Taiwan, a tropical island, and in our study, the most common organism causing pleural infection was Streptococcus species, which was compatible to the geographical trends reported in the review.
We emphasized empyema related to bacterial pneumonia and excluded the patients with fungal or tuberculosis empyema. Numerous studies have highlighted that the primary causes of community-acquired pneumonia were Streptococcus species and anaerobes, while hospital-acquired pneumonia was mostly caused by Staphylococcus aureus.[23, 24] Major pathogens of VAP were reported to be Pseudomonas aeruginosa, Klebsiella pneumoniae, and methicillin-resistant Staphylococcus aureus (MRSA).[25, 26] Our data indicated that the primary pathogens of respiratory secretion cultures were Pseudomonas aeruginosa (44%) and Klebsiella pneumoniae (16%), while the main pathogens in pleural effusion/tissue cultures were Streptococcus species (38%), Klebsiella pneumoniae (11%), and Staphylococcus aureus (10%). We performed VATS decortication soon after empyema was diagnosed or when it was suspected, usually within 7 days. Intraoperative pleural cultures could be obtained early in the hospital course. However, 61.8% of our patients experienced ICU admission and received endotracheal tube intubation with ventilator for oxygen support. Respiratory secretion cultures could be collected at any time during the hospital course. Notably, the specimens obtained by endotracheal aspiration or BAL would be highly associated with VAP, potentially explaining our observed pathogen spectrum.
It is essential to start the treatment for empyema with broad-spectrum antibiotics initially.[4] Additionally, appropriately escalating the antibiotics regimen with anti-Pseudomonas or anti-MRSA agents based on the respiratory secretion culture result is crucial in both adult and pediatric patients.[27, 28] In our center, we initially prescribed empiric anti-Pseudomonas antibiotics when the empyema patients were admitted to ICU. Simultaneously, respiratory secretion and blood cultures were repeatedly collected until the infection was well under control. Further use of therapeutic anti-MRSA agent would be indicated based on the culture results.
Our study has several limitations. Firstly, the data are derived from a single medical center. The pathogen spectrum changes geographically, and the evidence is insufficient to be universally applicable. Secondly, this is a retrospective study, which may involve selection bias. Thirdly, the culture techniques vary among different institutes, potentially affecting sensitivity. A larger database or a multi-center study is needed to confirm our findings. Fourthly, the differences between respiratory secretion and pleural results may be due to the presence of two different and subsequent infections. The lack of data about infection source may cause potential bias. Lastly, the timing to obtain respiratory secretion specimens during hospitalization was not regular. The number of cultures and the collection methods varied among different cases. Despite the limitations, respiratory secretion culture plays a crucial role in the prediction of surgical outcomes in bacterial empyema patients.