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Journal of Clinical Microbiology, June 2002, p. 2308-2310, Vol. 40, No. 6
0095-1137/02/$04.00+0     DOI: 10.1128/JCM.40.6.2308-2310.2002
Copyright © 2002, American Society for Microbiology. All Rights Reserved.

Enterococcus gallinarum Endocarditis Occurring on Native Heart Valves

Sylvie Dargere,1* Michel Vergnaud,2 Renaud Verdon,1 Eric Saloux,3 Olivier Le Page,4 Roland Leclercq,2 and Claude Bazin1

Service de Maladies Infectieuses,1 Service de Bactériologie,2 Service de Cardiologie,3 Service de Chirurgie Cardiaque, Cote de Nacre University Hospital, 14033 Caen, France4

Received 17 December 2001/ Returned for modification 13 February 2002/ Accepted 15 March 2002


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ABSTRACT
 
We report the first case of Enterococcus gallinarum endocarditis developing on normal native heart valves. Using phenotypic and molecular methods, a precise identification of this naturally vancomycin-resistant species allowed an optimal antibiotic therapy and the patient's recovery.


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CASE REPORT
 
A 62-year-old Vietnamese man was admitted to our hospital in January 2001 because of presumptive endocarditis. He had been living in France since 1952 and worked as a veterinarian. He had a background history of cholecystectomy, gastrectomy for bleeding gastric ulcer in 1965, brucellosis treated with tetracycline in 1967, and polycythemia. The patient did not report any hospitalization stay of more than 1 day (for therapeutic phlebotomy) since 1965. He had no previously damaged cardiac valves. He did not receive any antimicrobial treatment during the months before hospitalization, but in the first days of January, he was treated with roxithromycin (150 mg twice a day [b.i.d.]) and corticosteroids for a putative diagnosis of pneumonia. On 14 January 2001, he was admitted to a local hospital because of heart failure and persistent fever. The combination amoxicillin-clavulanic acid (1 g three times a day [t.i.d.]) was added to the regimen. On 17 January, the transthoracic echocardiography demonstrated the presence of mitral and aortic vegetations. Amoxicillin-clavulanic acid and roxithromycin were switched to cefotaxime (2 g t.i.d.) and gentamicin (100 mg b.i.d.) for presumably infective endocarditis. On the third day of the cefotaxime-gentamicin regimen, the patient required mechanical ventilation because of heart failure and was admitted to our hospital. Transoesophageal echocardiography demonstrated voluminous aortic vegetation with valvular destruction, prolapsus, and aortic regurgitation. There were also two mitral vegetations with mitral regurgitation. Because an Enterococcus species was isolated from two blood cultures, cefotaxime was switched to vancomycin (1 g b.i.d.). The patient underwent replacement of the mitral and aortic valves on 23 January.

Based on the disk diffusion method (27), the strain was first reported as susceptible to ampicillin, erythromycin, vancomycin, teicoplanin, trimethoprim-sulfamethoxazole, and rifampin, but resistant to lincomycin. No high-level resistance to gentamicin was detected by a screening test on agar plates containing 500 µg of gentamicin per ml. The bacteriological analysis of surgically removed valves obtained 18 h after the beginning of vancomycin therapy yielded growth of an enterococcal strain. Blood culture and valve isolates were identified as Enterococcus gallinarum by physiological and molecular methods (12) and had identical antibiotic susceptibility patterns. Strains grew on a 6-µg/ml vancomycin agar plate, on bile esculin agar, were nonhemolytic on sheep blood agar, and were positive for Streptococcus group D antigen by latex agglutination (Slidex Strepto kit; bioMerieux, Marcy l'Etoile, France). They were identified as E. gallinarum by the API Rapid ID 32 Strep system (code 72375513371) (bioMerieux, La-Balme-les-Grottes, France).

Consistently, the strains were motile when tested by the 30° motility test (mannitol motility test medium) and did not produce pigment on blood agar. This identification was confirmed by two molecular methods: a multiplex PCR targeted at specific sequences in the glycopeptide resistance ligase genes vanA, vanB, vanC-1, and vanC-2 (3) and a restriction endonuclease analysis of a fragment of the sodA gene (sodAint) (20). The vanC-1 gene, which is present only in the motile E. gallinarum species, which is intrinsically resistant to low levels of vancomycin, was amplified. The restriction fragment length polymorphism of sodAint digested with AluI, HaeIII, or HinfI provided a specific pattern (data not shown). By the E-test method, the MICs for E. gallinarum isolates were as follows: amoxicillin, 0.5 µg/ml (susceptible); vancomycin, 6 µg/ml (intermediate); and teicoplanin, 0.125 µg/ml (susceptible).

Enterococci, most often E. faecalis, cause 5 to 20% of cases of infective endocarditis (17). Enterococcal endocarditis is usually a subacute disease of older men, the most frequent source of infection being the gastrointestinal or the genitourinary tract. A recent review of the literature reveals that bacteremia due to motile enterococci constituted less than 5% of all cases of enterococcal bacteremia (19, 21-23, 29).

According to a MEDLINE search, this is the second report of endocarditis due to E. gallinarum (or Streptococcus gallinarum, as previously named). Reid et al. described one case in a 66-year-old man with a bicuspid aortic valve who had undergone urologic surgery 2 years before (22). In our case, the patient's medical history as well as the pathological examination of the surgically removed valves did not reveal any preexisting valvular disease.

Motile enterococci, including E. gallinarum and Enterococcus casseliflavus, are rarely encountered in human clinical specimens and are primarily found in the gastrointestinal tract in poultry, in foods, and in domestic fowls (1, 28). They have rarely been associated with disease, but have been implicated in a wide variety of invasive infections in humans, especially immunocompromised or chronically ill patients, and sometimes are nosocomially acquired (5, 6, 16, 19, 22, 23, 29). The majority of cases of bacteremia due to these organisms involved patients with underlying conditions, such as renal failure, solid organ cancer or hematologic malignancy, receipt of solid organ or bone marrow transplant, antithrombin III deficiency, astrocytoma, chronic osteomyelytis, diabete mellitus, choledocholithiasis, and Caroli's disease (10, 11, 13, 17, 19, 21, 22, 29, 30, 33).

Our patient was not immunosuppressed and did not receive any antimitotic chemotherapy. Benign erythrocytosis without polycythemia vera was the only underlying disease that we could find.

The low prevalence of motile enterococcal endocarditis may be due to the difficulties in identifying these species (9). Motility testing is required to distinguish them from Enterococcus faecium because of the similarity of the phenotypic characteristics. E. gallinarum can usually be distinguished from E. casseliflavus by its lack of pigmentation (5). However, some authors have reported nonmotile E. gallinarum and E. casseliflavus, as well as nonpigmented E. casseliflavus isolates (31). These discrepancies make molecular methods useful to confirm definitive identification (3).

Several studies reported intestinal colonization by E. gallinarum and E. casseliflavus in both hospitalized individuals and nonhospitalized healthy individuals. No definite risk factors for colonization or infection have been identified (1, 7, 8, 26, 29). Motile enterococci are part of the normal stool flora of the general population. Because of intrinsic low-level resistance to cephalosporins and vancomycin, treatment with these antimicrobial agents may play a role in increasing colonization with these organisms (2, 4, 18). Our patient had not received such antibiotics within several months before admission.

Most of the patients with enterococcus-related disease have a presumptive gastrointestinal source of the bacteria. Our patient had no obvious gastrointestinal source of infection. The food chain may play a role as a source of infections (1). We emphasize that the patient worked as a veterinarian.

E. gallinarum has the capacity to express resistance to low-level vancomycin, with vancomycin MICs ranging from 2 to 32 µg/ml, and the strains can be classified as intermediate or susceptible to this antibiotic (2, 3, 25, 31). This feature is conferred by the chromosomal vanC1 gene (14, 15, 24, 29, 32). Antibiotic susceptibility patterns indicate that most isolates are ampicillin susceptible (6). Our case illustrates the importance of a careful identification of Enterococcus species because of its impact on the choice of the antibiotic regimen. Our patient had been receiving vancomycin therapy for 18 h when surgery was performed. The limited duration of vancomycin therapy before surgery did not allow us to evaluate its real impact on the persistence of bacteria in valvular tissue. We can retrospectively assume that such antibiotic treatment could have led to deleterious consequences.

In conclusion, while not frequently recovered from clinical specimen, motile enterococci may cause serious invasive infections. This case demonstrates the role of E. gallinarum as a cause of native valve endocarditis. This is of major clinical importance, because of the particular sensitivity profile of this species among species in the genus Enterococcus.


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FOOTNOTES
 
* Corresponding author. Mailing address: Service de Maladies Infectieuses, CHU Côte de Nacre, 14033 Caen Cedex, France. Phone (33) 02 31 06 47 14. Fax (33) 02 31 06 49 96. E-mail: dargere-s{at}chu-caen.fr. Back


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Journal of Clinical Microbiology, June 2002, p. 2308-2310, Vol. 40, No. 6
0095-1137/02/$04.00+0     DOI: 10.1128/JCM.40.6.2308-2310.2002
Copyright © 2002, American Society for Microbiology. All Rights Reserved.



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