Infection
Case Report
Pleural Enterococcus faecalis Empyema: An Unusual Case R. Bergman, D.H.T. Tjan, M.A. Schouten, L.E.M. Haas, A.R.H. van Zanten
Abstract A 63-year-old female patient was admitted to the department of neurology following an acute ischemic infarction of the right medial cerebral artery. She developed fever, respiratory failure, and hypotension and had to be transferred to the intensive care unit (ICU) for intubation and mechanical ventilation. Chest X-ray showed increased density of the complete right hemi-thorax, indicative of massive pleural effusion. Chest tube drainage produced 1.5 l of pus in 1 h. Cultures revealed growth of Enterococcus faecalis. The patient was treated with amoxicillin and clavulanic acid with good clinical response. Enterococci very rarely cause spontaneous pleural empyema. The natural resistance of enterococci to several types of antibiotics can lead to selection of enterococci as seen in other clinical studies and may lead to this unusual clinical consequence. Infection 2009; 37: 56–59 DOI 10.1007/s15010-007-6359-6
Introduction Pulmonary complications, such as pneumonia, are frequently seen in neurological patients after cerebral infarction. These are usually caused by aspiration and sputum retention. Patients usually respond well to antibiotic treatment without developing further pulmonary complications. Pleural empyema with enterococci in stroke patients has not been described before. We present a neurological patient with an unexpected pleural empyema due to Enterococcus faecalis as a complication of pneumonia.
Case Report A 63-year-old female patient was admitted to the neurological stroke unit with a large acute ischemic infarction of the right medial cerebral artery. Her medical history was unremarkable. On the second day of admission, she developed fever, cough and leukocytosis. An initial chest X-Ray (CXR) did not show any abnormalities. Intra-venous cefotaxime was commenced empirically for suspected aspiration without clinical response. Additionally a single dose of gentamicin was given. She was not on any antibiotic treatment before admission.
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In the following days she developed progressive respiratory distress, became hypotensive and somnolent and was admitted to the ICU for intubation and mechanical ventilation on day 6. On ICU admission, her vitals signs were as follows: temperature 40 °C, heart rate 155 beats/min, blood pressure 80/ 50 mmHg, RR 40/min. SpO2 84% with a 10 l/min oxygen rebreathing face mask. The initial arterial blood gas showed pH 7.27 (7.37–7.45), pCO2 6.6 kPa (4.5 kPa–6.0 kPa), pO2 7.0 kPa (9.5 kPa–13.0 kPa), HCO–3 19.4 mmol/l (22 mmol/l–26 mmol/l), BE-6.8 mmol/l (– 2.0 mmol/l ± 2.0 mmol/l, SaO2 86% (92%–99%). Laboratory examination showed: lactate 4.6 mmol/l (0.5 mmol/l–1.7 mmol/l), leukocytes 1.8/nl (4–11/nl) with toxic staining, hemoglobin 6.8 mmol/l (8.5 mmol/l–11 mmol/l), Creactive protein (CRP) 497 mg/l (0 mg/l –5 mg/l) and procalcitonin (PCT) > 10 ng/ml (< 0.5 ng/ml). A new CXR post intubation showed increased density of the complete right hemi-thorax, with blunted costophrenic angle, and loss of the hemidiaphragm, indicating pleural effusion (Figure 1). She eventually developed septic shock with oliguric acute renal failure. In addition she developed an acute coronary syndrome with arrhythmia. She was treated according to surviving sepsis campaign (SSC) guidelines. A urine test for Legionella antigen as well as serology for respiratory pathogens was negative. Empirically ciprofloxacin was added to cefotaxime to cover other atypical pathogens. Endotracheal aspirate cultures taken before the addition of new antibiotics and sputum cultures became positive for E. faecalis. Bloodcultures were negative. Thoracocentesis yielded pussy white fluid with the following characteristics: WBC 291.4/nl, LDH content 21,117 U/l, pH 7.0, and protein content 22.5 g/l indicative of an exudate. Insertion of a chest tube drained 1.5 l of pus. Gram stain showed a large number of leucocytes, but no bacteria. Cultures of the specimen revealed growth of E. faecalis sensitive to amoxicillin, vancomycin and low-level aminoglyco-
R. Bergman, D.H.T. Tjan (corresponding author), L.E.M. Haas, A.R.H. van Zanten Dept. of Intensive Care, Gelderse Vallei Hospital, PO-Box 9025, 6716 RP, Ede, The Netherlands; Phone: (+31/318) 434-115, Fax: -116, e-mail:
[email protected] M.A. Schouten Dept. of Clinical Microbiology, Gelderse Vallei Hospital, Ede, The Netherlands Received: December 19, 2006 Æ Revision accepted: June 27, 2007 Published online: October 31, 2007
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aspiration flora. Over the course of the week the drain was slowly retracted until fluid drainage ceased and could be successfully removed. Patient continued to improve, septic shock abated after 1 week and she was successfully extubated 3 weeks after ICU admission. She was discharged with a maximal GCS of 15 and no paralysis. After discharge the patient was readmitted twice due to respiratory failure but eventually made a good recovery with a normal CXR and left the hospital in reasonable order. Antibiotics were given for a total of 5 weeks.
Discussion
Figure 1. Chest X-ray on admission after endotracheal intubation: increased density of the complete right hemi-thorax, with blunted costophrenic angle, and loss of the hemidiaphragm.
side resistance. Diagnosis and sensitivity were determined with the automized Phoenix system by Becton Dickinson. Anaerobic cultures remained negative. In 2 days, total output was over 2.5 l of purulent fluid. Despite adequate drainage, there was no clinical improvement in the infectious parameters. CT chest showed two remaining pleural fluid collections with compression atelectasis of the lung. Unexpectedly, a small anterior pneumothorax was found (Figure 2). The chest tube was repositioned and repeat CT imaging showed a substantial decrease of fluid collections and resolution of the pneumothorax. Antibiotic therapy was switched to amoxicillin and clavulanic acid after cultures became positive for E. faecalis. Clavulanic acid was also added to cover other anaerobic commensal
Figure 2. CT-scan demonstrating a small anterior pneumothorax (arrow 1) and residual empyema (arrow 2). The intercostals route of the chest tube is visible (arrow 3).
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Thoracic empyema is defined as pus in the pleural cavity or as an effusion with bacteria seen on gram stain [1]. Empyema may be caused by a facultatively aerobic grampositive or gram-negative, anaerobic, or polymicrobial bacterialflora. Anaerobic and facultative gram-positive bacteria account for 41% of complicated pleural effusions, mostly due to Staphylococcus aureus and Streptococcus pneumoniae, only 0.7% are due to enterococci [2]. Enterococci are gram-positive cocci that occur singly, in pairs, or in short chains. They are facultative anaerobes and rarely cause empyema [3], but have been described causing infection of the abdomen, heart and kidneys [3]. However, they usually cause bloodstream [4] and urinary tract infections [5]. The distribution of the commonly known species is shown in table 1. The reported incidence of pleural empyema due to enterococci is only 4% of all Enterococcus infections. Only a few cases of E. faecalis thoracic empyema have been reported. Although enterococcal empyema is rare, its occurrence has previously been linked to intraabdominal infections spreading out to susceptible parts of the body [6, 7]. Most cases were patients who had undergone recent abdominal surgery or were suffering from liver cirrhosis and/or associated peritonitis [6–9]. In three separate retrospective reviews of empyema and one prospective study of empyema in liver cirrhosis, 30 cases of enterococcal empyema were reported [6–9]. The source of infection was an endocarditis with a splenic abscess in one case and an esophago-pleural fistula after pneumonectomy in another case [10, 11] In the other 28 reported cases, the origin of enterococci was never identified [6]. However, infections caused by enterococci have been on the rise [12] probably due to their innate antimicrobial resistance to commonly used antibiotics like all cephalosporins, which allows them to thrive while competitive organisms susceptible to antibiotics are suppressed [13–15]. The use of antibiotics has been known to change the flora in the gastro-intestinal tract. The natural resistance of enterococci to several types of antibiotics including aminoglycosides and cephalosporins [16–18] can lead to selection of enterococci [19] and may lead to unusual clinical consequences and complications as we describe.
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R. Bergman et al. An Unusual Cause of Spontaneous Pleural Empyema
Table 1 Distribution of Enterococcus Species in clinical isolates from different sites.
Body sites
E. faecalis
E. faecium
E. casseliflavus
E. gallinarum
E. avium
E. raffinosus
Urine (%) Blood and catheter (%) Deep abscess (%) Wounds and mucous membranes (%) Resp. tract (ICU) (%) Total (%)
93.7 53.8 72.7 90.9 50.0 85.5
5.3 42.3 22.7 6.8 45.5 12.1
0.7 3.8 0.9 0 0 0.7
0 0 1.8 0.8 0 0.5
0 0 0.9 0 0 0.2
0.3 0 0 0 4.5 0.4
Adapted from [22]
In our patient with a medical history of ischemic cerebral infarction aspiration is the most likely cause of colonization of the lower respiratory tract, further underlined by the positive culture of E. faecalis from the tracheal aspirate and sputum. Compared to most cases of community-acquired pneumonia, the onset of aspiration pneumonia is often relatively slow [20]. Many patients with aspiration pneumonia do not present with acute infections but later develop complications characterized by suppuration and necrosis [20]. Later stages of untreated aspiration pneumonia may present as lung abscess, necrotizing pneumonia, or empyema [20]. Our case is remarkable since the empyema developed early in the course of the disease with no history of antibiotic exposure. Antimicrobial therapy with cefotaxime and ciprofloxacin may have led to enterococcal overgrowth and localized pleuro-pneumonia. Empyema is a potentially life threatening complication with a reported mortality of 41% [21]. Therefore, early diagnosis and immediate (diagnostic) thoracocentesis and drainage with supportive and targeted antimicrobial therapy are of paramount importance. In conclusion, although extremely rare, pleural empyema caused by E. faecalis can occur in patients with only a short disease history and limited use of antibiotics. In addition this can lead to septic shock with multiple organ dysfunction syndrome, but with proper treatment and interventions can be treated well.
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Acknowledgments We are grateful to A. van Die, radiologist for his help with the description of radiological findings.
References Colice GL, Curtis A, Deslauriers J, Heffner J, Light R, Littenberg B, Sahn S, Weinstein RA, Yusen RD: Medical and surgical treatment of parapneumonic effusions: an evidence-based guideline. Chest 2000; 118: 1158–1171. 2. Chen KY, Hsueh PR, Liaw YS, Yang PC, Luh KT: A 10-year experience with bacteriology of acute thoracic empyema. Chest 2000; 117: 1685–1689. 3. MacEachern P, Giannoccaro JP, Elsayed S, Read RR, Laupland KB: A rare case of pleuropulmonary infection and septic shock
15.
16.
1.
58
17.
18.
associated with Enterococcus faecium endocarditis. J Infect 2005; 50: 84–88. Gross PA, Harkavy LM, Barden GE, Flower MF: The epidemiology of nosocomial enterococcal urinary tract infection. Am J Med Sci 1976; 272: 75–81. Emori TG, Gaynes RP: An overview of nosocomial infections, including the role of the microbiology laboratory. Clin Microbiol Rev 1993; 6: 428–442. Behnia M, Clay AS, Hart CM: Enterococcus faecalis causing empyema in a patient with liver disease. South Med J 2002; 95: 1201–1203. Xiol X, Castellvi JM, Guardiola J, Sese E, Castellote J, Perello A, Cervantes X, Iborra MJ: Spontaneous bacterial empyema in cirrhotic patients: a prospective study. Hepatology 1996; 23: 719–723. Smith JA, Mullerworth MH, Westlake GW, Tatoulis J: Empyema thoracis: 14-year experience in a teaching center. Ann Thorac Surg 1991; 51: 39–42. Alfageme I, Munoz F, Pena N, Umbria S: Empyema of the thorax in adults. Etiology, microbiologic findings, and management. Chest 1993; 103: 839–843. Tornos MP, Mayor G, Nadal A, Soler-Soler J: Empyema and splenic abscess in infective endocarditis. Int J Cardiol 1984; 6: 746–748. Benjamin I, Olsen AM, Ellis FH Jr: Esophagopleural fistula. A rare postpneumonectomy complication. Ann Thorac Surg 1969; 7: 139–144. Blaimont B, Charlier J, Wauters G: Comparative distribution of Enterococcus species in faeces and clinical samples. Microb Ecol Health Dis 1995; 8: 87–92. Suppola JP, Volin L, Valtonen VV, Vaara M: Overgrowth of Enterococcus faecium in the feces of patients with hematologic malignancies. Clin Infect Dis 1996; 23: 694–697. Berk SL, Verghese A, Holtsclaw SA, et al. Enterococcal pneumonia: occurrence in patients receiving broad-spectrum antibiotic regimens and enteral feeding. Am J Med 1983; 74: 153–154. Bonten MJM, van Tiel FH, van der Geest S, et al. Enterococcus faecalis pneumonia complicating topical antimicrobial prophylaxis. N Engl J Med 1993; 328: 209–210. Filipova M, Bujdakova H: Factors of virulence and mechanisms of resistance to aminoglycosides in clinical isolates of Enterococcus faecalis and Enterococcus faecium with high-level gentamicin resistance. Epidemiol Mikrobiol Imunol 2005; 54: 65–74. Kobayashi N, Alam M, Nishimoto Y, Urasawa S, Uehara N, Watanabe N: Distribution of aminoglycoside resistance genes in recent clinical isolates of Enterococcus faecalis, Enterococcus faecium and Enterococcus avium. Epidemiol Infect 2001; 126: 197–204. Dupre I, Zanetti S, Schito AM, Fadda G, Sechi LA: Incidence of virulence determinants in clinical Enterococcus faecium and
Infection 37 Æ 2009 Æ No. 1 Ó URBAN & VOGEL
R. Bergman et al. An Unusual Cause of Spontaneous Pleural Empyema
Enterococcus faecalis isolates collected in Sardinia (Italy). J Med Microbiol 2003; 52: 491–498. 19. Scott IU, Loo RH, Flynn HW Jr, Miller D: Endophthalmitis caused by Enterococcus faecalis: antibiotic selection and treatment outcomes. Ophthalmology 2003; 110: 1573–1577. 20. Bartlett JG: Anaerobic bacterial infections of the lung and pleural space. Clin Infect Dis 1993; 16: 248–255.
Infection 37 Æ 2009 Æ No. 1 Ó URBAN & VOGEL
21.
Tu CY, Hsu WH, Hsia TC, Chen HJ, Chiu KL, Hang LW, Shih CM: The changing pathogens of complicated parapneumonic effusions or empyemas in a medical intensive care unit. Intensive Care Med 2006; 32: 570–576. 22. Blaimont B, Charlier J, Wauters G: Comparative distribution of Enterococcus species in faeces and clinical samples. Microb Ecol Health Dis 1995; 8: 87–92.
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