Enterococcus faecalis causing empyema in a patient with liver disease.

ABSTRACT

A 57-year-old man with a history of liver disease had shortness of breath, fever, and pleuritic chest pain. Ascites was not present. Computed tomography (CT) of the chest revealed a large unilateral pleural effusion, compressive atelectasis, and no evidence of consolidation. Culture of the pleural fluid grew Enterococcus faecalis. Treatment with ampicillin in conjunction with tube thoracostomy resulted in clinical improvement. This case illustrates the development of spontaneous monomicrobial empyema due to E faecalis in a patient with liver disease, in the absence of pneumonia and peritonitis.

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ENTEROCOCCUS FAECALIS is a rare cause of respiratory tract and pleural space infections. (1) The pathogen has been uncommonly associated with nosocomial pneumonia in severely debilitated patients. (2,3) On rare occasions, it can also cause empyema in patients with liver disease. This often occurs in the presence of peritonitis, possibly because of a dysfunctional reticuloendothelial system, (4) but cases of E faecalis empyema in the absence of peritonitis have been reported as well. The approach to E faecalis pleural space infection in patients with liver disease is not well established. In fact, in a large reported series of patients with cirrhosis, none of the patients with evidence of E faecalis in the pleural space required chest tube placement. (5)

In the following report, a patient with liver disease had isolated E faecalis empyema in the absence of peritonitis. Furthermore, clinical and radiographic features of pneumonia were not present. Unlike previously reported cases of enterococcal empyema, this pleural space infection necessitated chest tube drainage.

CASE REPORT

A 57-year-old man was seen after 2 weeks of shortness of breath, malaise, and pleuritic chest pain. There was no history of cough or sputum production. He was not taking any medication. His medical history included open reduction and internal fixation of a hip fracture, cataract surgery, and longstanding hepatomegaly. There was no history of hepatitis. He had a 50 pack-year history of smoking and had consumed 8 beers per week until 3 years before the current illness. The family history was noncontributory. There was no history of exposure to toxins or fumes, and no history of illicit drug abuse.

On physical examination, the temperature was 101[degrees]F, heart rate 97/mm, respiratory rate 25/mm, and blood pressure 147/81 mm Hg. Spider angiomas were seen on the anterior thorax, and palmar erythema was present. Cardiac examination revealed a regular rate and rhythm, with no gallop or murmur. The chest was dull to percussion at the base of the right lung, and rales were audible in the same area. The abdomen was protuberant, with a caput medusa and an umbilical hernia. Shifting dullness and hepatosplenomegaly were not detected. There was no edema of the extremities.

Laboratory data included a white blood cell (WBC) count of 19,500/[micro]L (92% neutrophils, 5% lymphocytes, and 3% monocytes), hemoglobin value of 14.3 g/dL, and platelet count of 156,000/[mm.sup.3]. Electrolyte, amylase, and lipase levels were within normal limits. Other values were bilirubin 3.2 mg/dL (normal, <1.5 mg/dL), alkaline phosphatase 196 IU/L (normal, 25 to 125 IU/L), aspartate aminotransferase 22 IU/L (normal, 25 to 45 IU/L), protein 6.6 g/dL, and albumin 2.8 g/dL. Erythrocyte sedimentation rate was 95 mm/hr. International normalized ratio was 1.1. Arterial blood gas values (on room air) were pH 7.47, [Pco.sub.2] 30 mm Hg, and [Po.sub.2] 48 mm Hg. Urine test for Legionella antigen was negative. Chest roentgenogram showed a large right-sided pleural effusion (Fig 1). Empiric antibiotic therapy with intravenous clindamycin and levofloxacin was initiated. Thoracentesis yielded thick yellow fluid with the following characteristics: pH 6.9, glucose <20 mg/dL, protein 4.7 g/dL, lactate dehydrogenase 6 ,668 IU/L, WBC count 15,000/[micro]L (96% neutrophils, 2% band forms, and 2% eosinophils), and RBC count 2,000/[micro]L. Because of the purulent nature of the fluid, a thoracostomy tube was inserted in the pleural space and 400 mL of turbid, brownish fluid was drained. Fluid cultures were positive for E faecalis, sensitive to ampicillin, vancomycin, and chloramphenicol. Anaerobic cultures were negative. Antibiotic therapy was adjusted to ampicillin, 2 g IV every 6 hours. Intrapleural urokinase was instilled to facilitate adhesionolysis. Within 48 hours, drainage from the chest tube diminished. Computed tomography of the chest showed an extensive pleural effusion and compressive atelectasis (Fig 2). The chest tube was repositioned and approximately 2,000 mL of fluid was drained. To evaluate further for the presence of ascites and liver disease, CT of the abdomen was done, which revealed minimal ascites and the presence of hepatosplenomegaly and varices, suggestive of portal hypertension. The chest tube was rem oved on the eighth hospital day. Repeat CT of the chest revealed a small pocket of loculated pleural fluid, with no evidence of consolidation in the lung parenchyma. The patient's fever, leukocytosis, and hypoxemia were improving gradually. He completed a 2-week course of intravenous ampicillin and was discharged with a 3-week course of oral amoxicillin.

DISCUSSION

Empyema, or infection of the pleural space, is typically associated with pneumonia. (69) The most common organisms isolated from empyema are Streptococcus pneumoniae, Staphylococcus aureus, Hemophilus influenzae, Escherichia coli, Kiebsiella pneumoniae, and species of Bacteroides. (7) Enterococcus is rarely present in chest infections. Our case illustrates that E faecalis can cause community-acquired empyema in patients with liver disease who lack peritonitis.

Previously classified in the genus Streptococcus (Lancefield group D), Enterococcus is a chain-forming coccus that ordinarily resides within the bowel flora. (10) Of its several species, E faecalis and E faecium are the most prevalent, the former being isolated in 85% to 90% of clinical entero-coccal infections. (1,10,11) Enterococci are rarely acquired in the community but are the second leading cause of nosocomial infections (10,11) with a mortality rate approximating 15%. (12) Enterococci most commonly infect the urinary tract or abdominal and pelvic wounds (10,11) and may cause bacteremia (10) and endocarditis. (10,11)

Respiratory tract infections rarely result from enterococci. (10) Enterococcal pneumonia has been reported as a nosocomial infection in severely debilitated patients receiving long-term antibiotic therapy. (2,3) Empyema due to E faecalis is also uncommon. In three separate retrospective reviews of empyema (6-8) and one prospective study of empyema in cirrhosis, (5) 30 cases of enterococcal empyema were reported (Table). A specific source of infection was found in two cases of E faecalis empyema--one in a patient with endocarditis and splenic abscess (13) and one related to an esophago-pleural fistula after pneumonectomy. (14) In the other 28 cases reported in the literature, the source of infection was never identified.

Some have hypothesized that liver disease may predispose patients to enterococcal respiratory tract infection through seeding of hepatic hydrothorax. (15) Transdiaphragmatic migration of ascitic fluid causes hepatic hydrothorax in 5% to 25% of cirrhotic patients. (16,17) Infection of pleural fluid parallels the pathogenesis of spontaneous bacterial peritonitis, in which bacteria migrate through the bowel wall into the lymphatic system and infect the blood through the thoracic duct. (4) The impaired reticuloendothelial system of patients with liver disease prolongs bacteremia (4,18,19) and favors inoculation of pleural and ascitic fluid. The low protein content of ascitic and pleural fluid precludes opsonization and phagocytosis of bacteria and prevents resolution of the infection. (4)

Although infrequently identified as a source of bacteremia, Enterococcus has been proven to migrate across the gut (20) and cause transient bacteremia. In a prospective study of 120 cirrhotic patients with pleural effusion and ascites, two cases of pleural fluid infection with E faecalis were identified. (5) Twenty-two additional cases of pleural fluid infection with other bacterial species were also identified in this study. Given the similar pathogenesis to spontaneous bacterial peritonitis, infection of pleural fluid in cirrhotic patients was termed "spontaneous bacterial empyema" (SBE) and defined as pleural fluid with a polymorphonuclear cell count >500/[micro]L. (5) In that series, 43% of the cases of SBE occurred without concomitant infection of the ascitic fluid, and none of the cases of SBE necessitated chest tube drainage. The reason for the presence of SBE in the absence of peritonitis is not well established. Poorer opsonization in pleural fluid as compared with peritoneal fluid may favor infectio n in the pleural space.

This case illustrates the development of E faecalis empyema in a patient with liver dysfunction and little evidence of ascites. The lack of cough, sputum production, and radiographic evidence of consolidation of the lung parenchyma supports the diagnosis of SBE due to E faecalis. This case differs from previously reported cases of SBE due to enterococci because the empyema necessitated chest tube drainage. This case emphasizes that in patients with liver disease, careful evaluation and management of pleural effusions should include diagnostic thoracentesis and fluid analysis as well as consideration of the potential role of intra-abdominal disease in the pathogenesis of the pleural effusion.

TABLE

Reported Cases of Empyema Due to Enterococcus faecalis

                       No. of Enterococcus  Total No.
Reference                faecalis Cases     of Cases

Xiol et al (5)                  2               24
Alfageme et al (6)              6               82
Brook and Frazier (7)           4              197
Smith et al (8*)               18              102
                               --              ---
  Total                        30              405

* Total number of enterococcal cases; subspecification was not done.

References

(1.) Ruoff KL, de la Mala L, Murtagh MJ, et al: Species identities of enterococci isolated from clinical specimens. J Clin Microbiol 1990; 28:435-437

(2.) 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

(3.) 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

(4.) Arroyo V. Navasa M, Rimola A: Spontaneous bacterial peritonitis in liver cirrhosis: treatment and prophylaxis. Infection 1994; 22:S167-S173

(5.) Xiol X, Castellvi JM, Guardiola J, et al: Spontaneous bacterial empyema in cirrhotic patients: a prospective study. Hepatology 1996; 23:719-723

(6.) Alfageme I, Munol F, Pena N, et al: Empyema of the thorax in adults: etiology, microbiologic findings, and management. Chest 1993; 103:839-843

(7.) Brook I, Frazier EH: Aerobic and anaerobic microbiology of empyema: a retrospective review in two military hospitals. Chest 1993; 103:1502-1507

(8.) Smith JA, Mullerworth MH, Westlake GW, et al: Empyema thoracis: 14-year experience in a teaching center. Ann Thorac Surg 1991; 51:39-42

(9.) Strange C, Sahn SA: The definitions and epidemiology of pleural space infection. Semin Respir Infect 1999; 14:3-8

(10.) Moellering RC: Emergence of enterococcus as a significant pathogen. Clin Infect Dis 1992; 14:1173-1178

(11.) Tailor SAN, Bailey EM, Rybak MJ: Enterococcus, an emerging pathogen. Ann Pharmacother 1993; 27:1231-1242

(12.) Jones RN, Marshall SA, Pfaller MA, et al: Nosocomial enterococcal blood stream infections in the SCOPE program: antimicrobial resistance, species occurrence, molecular testing results, and laboratory testing accuracy. Diagn Microbiol Infect Dis 1997; 29:95-102

(13.) Tornos MP, Mayor G, Nadal A, et al: Empyema and splenic abscess in infective endocarditis. Int J Cardiol 1984; 6:746-748

(14.) Benjamin I, Olsen AM, Ellis J, et al: Esophagopleural fistula: a rare postpneumonectomy complication. Ann Thoroc Surg 1969; 7:139-144

(15.) Flaum MA: Spontaneous bacterial empyema in cirrhosis. Gasteroenterology 1976; 70:416-417

(16.) Lieberman FL, Hidemura R, Peters RL, et al: Pathogenesis and treatment of hydrothorax complicating cirrhosis with ascites. Ann Intern Med 1966; 64:341-351

(17.) Strauss RM, Soyer TO: Hepatic hydrothorax. Semin Liver Dis 1997; 17:227-231

(18.) Kirchmair R, Allerberger F, Bangerl I, et al: Spontaneous bacterial pleural empyema in liver cirrhosis. Dig Dis Sci 1998; 43:1129-1132

(19.) Streifler J, Pitlik S, Dux S, et al: Spontaneous bacterial pleuntis in a patient with cirrhosis. Respiration 1984; 46:382-385

(20.) Wells CL, Jechorek RP, Erlandsen SL: Evidence for the translocation of Enterococcus faecalis across the mouse intestinal tract. J Infect Dis 1990; 162:82-90

RELATED ARTICLE: KEY POINTS

* Enterococcus faecalis, an uncommon cause of pneumonia in severely debilitated patients, can rarely cause empyema in patients with liver disease.

* Enterococcus faecalis empyema can be seen in the absence of pneumonia and peritonitis.

* Unlike previously reported cases in the literature, our case shows that Enterococcus faecalis pleural space infection warrants chest tube drainage.

* All patients with liver disease and pleural effusion should have diagnostic thoracentesis to rule out an infected pleural space.

From the Departments of Medicine, Richard L. Roudebush Veterans Affairs Medical Center, and Indiana University Medical Center, Indianapolis.

Supported by grants from the Research Service of the Roudebush Veterans Affairs Medical Center and the American Diabetes Association.

Reprint requests to Mehrdad Behnia, MD, 2330 Wrightsboro Rd, Augusta, GA 30904.