Pleural Empyema Caused by Streptococcus intermedius and Fusobacterium nucleatum: A Distinct Entity of Pleural Infections

Abstract

Background: Many community-acquired pleural infections are caused by facultative and anaerobic bacteria from the human oral microbiota. The epidemiology, clinical characteristics, pathogenesis, and etiology of such infections are little studied. The aim of the present prospective multicenter cohort study was to provide a thorough microbiological and clinical characterization of such oral-type pleural infections and to improve our understanding of the underlying etiology and associated risk factors.

Methods: Over a 2-year period, we included 77 patients with community-acquired pleural infection, whereof 63 (82%) represented oral-type pleural infections. Clinical and anamnestic data were systematically collected, and patients were offered a dental assessment by an oral surgeon. Microbial characterizations were done using next-generation sequencing. Obtained bacterial profiles were compared with microbiology data from previous investigations on odontogenic infections, bacteremia after extraction of infected teeth, and community-acquired brain abscesses.

Results: From the oral-type pleural infections, we made 267 bacterial identifications representing 89 different species. Streptococcus intermedius and/or Fusobacterium nucleatum were identified as a dominant component in all infections. We found a high prevalence of dental infections among patients with oral-type pleural infection and demonstrate substantial similarities between the microbiology of such pleural infections and that of odontogenic infections, odontogenic bacteremia, and community-acquired brain abscesses.

Conclusions: Oral-type pleural infection is the most common type of community-acquired pleural infection. Current evidence supports hematogenous seeding of bacteria from a dental focus as the most important underlying etiology. Streptococcus intermedius and Fusobacterium nucleatum most likely represent key pathogens necessary for establishing the infection.

Keywords: Fusobacterium nucleatum; Streptococcus intermedius; 16S rRNA; next-generation sequencing; pleural infection.

Figure 1.

Patient inclusion and distribution of key pathogens. *Precalculated number of patients based on reference [2]. ^§Related to pneumonia (10), pulmonary embolism (1), cholecystitis (1), systemic infection (1), or endocarditis (1). ^#Samples with F. nucleatum and/or A. aphrophilus often included many additional species not indicated in this figure (see Supplementary Table 2). Others: Bacillus cereus (1), Enterobacter cloacae (1), Listeria monocytogenes (1), and Streptococcus pyogenes (1). Abbreviations: A. aphr, A. aphrophilus; CAPIs, community-acquired pleural infections; E. coli, Escherichia coli; F. nucl, F. nucleatum; S. aure, Staphylococcus aureus; S. inte, S. intermedius; S. pneu, Streptococcus pneumoniae.

Figure 2.

Patient outcome in relation to age for all oral-type pleural infections.

Figure 3.

Macroscopic appearance and pH value of oral-type pleural infections. pH value was reported for 48 out of 63 (76%) patients. For 3 of these patients, the macroscopic appearance was not reported. Thirteen (27%) of the 48 oral-type pleural infections had a pH ≥7.2. Abbreviation: NA, not available.

Figure 4.

Axial contrast-enhanced CT images from 4 patients with oral-type pleural infection showing communications between a lung abscess and the pleural empyema. A, Patient PE66. CT image with a mediastinal setting showing a consolidated opacity (33 × 29 mm) with central hypodensity and peripheral contrast enhancement (arrow) in the right lower lobe that communicates with the pleural space. In the adjacent pleura, there is a pocket with central hypodense content and peripheral contrast enhancement that extends along the pleura approximately 30 mm in craniocaudal direction. B, Patient PE60. CT image with a mediastinal setting showing a consolidated opacity (arrow) with central hypodensity (∼20 × 20 mm) and air bubbles that continue into the lateral pleural cavity. The pleural fluid here communicates with the larger posteriorly located fluid accumulation. C, Patient PE42. CT image with a mediastinal setting showing lobular organized pleural fluid in the right hemithorax. In the lower lobe is a consolidated opacity with a small hypodense area (arrow) of 8-mm diameter that communicates with the adjacent pleural fluid. D, Patient PE56. CT image with a mediastinal setting showing several apparently encapsulated fluid loculations in the left part of the thorax that compress adjacent lung tissue. They are lenticular in shape and provide compression of adjacent lung tissue. Medial to the largest loculation is a consolidated opacity containing several pockets with central hypodensity and peripheral contrast enhancement. The largest of these pockets (arrow) communicates with the adjacent pleural fluid. Abbreviation: CT, computed tomography.

Figure 5.

Phylogenetic tree of all species present in 3 or more (≥5%) samples of either oral-type pleural infection (20 species) and/or sinus-oral–derived brain abscesses (18 species). Each dot represents 1 sample containing the associated bacterium and is colored according to the type of infection.