Staphylococcus lugdunensis Endocarditis - Journal of Clinical ...

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May 21, 1992 - Extensive testing revealed all of theseisolates to be S. lugdunensis. ... glass tissue grinder with a small amount of nutrient broth, and the homogenate ..... Performance standards for antimicrobial disk susceptibility tests, 4th ed.
JOURNAL OF CLINICAL MICROBIOLOGY, Aug. 1992, p. 1948-1952

Vol. 30, No. 8

0095-1137/92/081948-05$02.00/0 Copyright © 1992, American Society for Microbiology

Staphylococcus lugdunensis Endocarditis R. SHUITLEWORTH AND W. DAVID COLBY* Department of Microbiology, University Hospital, London, Ontario, Canada N6A SA5 Received 19 February 1992/Accepted 21 May 1992

Staphylococcus lugdunensis is a recently described coagulase-negative species which has been associated with human infections, including infective endocarditis. A case of native valve endocarditis caused by this organism is described. The initial laboratory detection of S. lugdunensis is facilitated by a positive test for ornithine decarboxylase. The identification of such isolates should not cause difficulty unless undue reliance is placed upon a small number of tests.

Staphylococcus lugdunensis is a coagulase-negative species first described in 1988 by Freney et al. (10). They characterized 11 strains isolated from clinical specimens, and in a later publication (9) gave detailed descriptions of 13 isolates, including 3 from cases of endocarditis (two prosthetic valves and one native valve). One large retrospective study indicated that S. lugdunensis occurs commonly on human skin (14), although some investigators disagree (20). Nevertheless, there is agreement that S. lugdunensis is an opportunistic pathogen of humans. Seven cases of endocarditis due to S. lugdunensis have been reported (7, 9, 23, 25) (Table 1). Two cases involved prosthetic valves, and four cases involved native valves. In one case the type of valve was not specified, but it was presumably native valve endocarditis. We present here a sixth case of S. lugdunensis native valve endocarditis.

i.v.) and cefazolin (1 g i.v.) during the dialysis visit and gentamicin (50 mg i.v.) at the next two dialysis visits. Five weeks before the 29 May 1991 admission he was seen by an internist with regard to his left upper quadrant pain. Two blood cultures obtained at that consultation were positive for gram-positive cocci initially reported as most closely resembling S. hominis by using API Staph-Ident (Analytab Products, Inc., Plainview, N.Y.) and Microscan (Baxter Healthcare Corporation, Microscan Division, West Sacramento, Calif.) commercial systems. One week later the patient complained of severe back pain radiating down the right leg at a hemodialysis visit. He was admitted to hospital with a fever of 38.2°C and was noted to have a grade II of VI systolic heart murmur. A blood culture was obtained from his subclavian catheter, and he was given one dose of i.v. vancomycin. His fever abated 24 h later, and the blood culture grew gram-positive cocci after overnight incubation which most closely resembled S. hominis. The patient refused further investigations and left the hospital 48 h after admission without informing the staff. On his next dialysis appointment, the patient seemed confused and the subclavian catheter site was noted to be purulent. A swab from the exit site showed few pus cells and occasional gram-positive cocci. The culture grew moderate numbers of diphtheroid bacilli and unidentified staphylococci (not S. aureus) which were judged not significant. On a dialysis visit 6 days prior to 29 May 1991 admission, the right forearm AV fistula was used for the first time. Two days later, the fistula was used again and the patient was noted to be experiencing chills. Hospital course. The subclavian exit site was swabbed the day after admission, but the Gram stain and culture were negative. Nevertheless, within 48 h of admission, the patient developed a fever and changes were noticed on the electrocardiogram which were accompanied by elevation of the cardiac enzymes. These findings were consistent with a small myocardial infarction. Four days after admission, he was noted to be lethargic, and on his fifth hospital day, two blood cultures were positive for coagulase-negative staphylococci which were identified as S. lugdunensis. This prompted reexamination of the three previous blood culture isolates which had been presumptively identified as S. hominis. Extensive testing revealed all of these isolates to be S. lugdunensis. An ultrasound examination the following day revealed a vegetation on the posterior mitral valve leaflet which was confirmed by echocardiography. Two more blood cultures yielded S. lugdunensis, and the culture of an intravenous catheter tip yielded a heavy growth of the same species. He was started on vancomycin and gentamicin and

CASE REPORT A 60-year-old man was admitted to hospital on 29 May 1991 with acute left upper quadrant abdominal pain. This had been a recurrent problem for at least 9 months. Medical history. The patient had a long history of atherosclerotic disease including myocardial infarction, cerebrovascular accident, hypertension, renal failure, and intermittent claudication as well as an abdominal aortic aneurysm. In 1985 he was placed on regular hemodialysis treatments and had a left forearm arteriovenous (AV) fistula constructed to facilitate vascular access. In December 1990 the patient was admitted after it was noted at a regular hemodialysis session that his AV fistula was clotted, with localized cellulitis. Oral cloxacillin was ordered and surgical intervention was planned, but the patient left the hospital against medical advice 48 h after admission. At a subsequent dialysis visit a long-term subclavian catheter was placed. He also received vancomycin (1 g intravenously [i.v.]) during a dialysis visit. Subsequently, 2 months after he left the hospital, the patient was briefly readmitted for construction of an AV fistula in the right forearm. He was discharged after 48 h without incident. Nevertheless, a few days later a blood culture was obtained (no growth), and he was placed on oral cloxacillin (500 mg every 6 h) for 2 weeks. A few days later, pneumonia was suspected and a chest X ray showed persistent pleural effusions with an increase in the right effusion since the last chest X-ray. He received gentamicin (80 mg *

Corresponding author. 1948

S. LUGDUNENSIS ENDOCARDITIS

VOL. 30, 1992

1949

TABLE 1. Previously reported cases of S. lugdunensis endocarditis Case no.

Valve type

(sex,Patient age [yr])

1 2 3 4 5 6 7

Native, mitral Native, aortic Prosthetic, aortic Native, aortic, mitral, tricuspid Native, mitral Prosthetic, aortic Not stated

Female, 67 Male, 32 Male, 64 Female, 72 Female, 65 Male, 58 Female, 70

on the eighth hospital day underwent surgery to have the mitral valve replaced. The valve was found to have mucinous degenerative changes and vegetations containing grampositive cocci. Culture of the valve tissue was positive for S. lugdunensis in moderate numbers. During the night after surgery the patient suffered an episode of ventricular fibrillation from which he could not be resuscitated. Postmortem examination. Initial findings included a hyper-

trophied heart with extensive posterior bilateral infarctions and evidence of recent valve replacement. The kidneys had extensive polycystic changes bilaterally, and there was severe renal artery atherosclerosis. The spleen was enlarged, with recent infarcts, and there was also a parietal cerebral infarct. Culture of postmortem blood yielded no growth. The final major diagnoses were S. lugdunensis endocarditis and ventricular fibrillation secondary to acute massive myocardial infarction. MATERIALS AND METHODS Microbiological investigations. (i) Blood cultures. Up to 6-ml quantities of blood were inoculated into Bactec NR16A and NR17A bottles, and the cultures were tested on the Bactec NR660 system (Becton Dickinson, Towson, Md.) according to the standard protocol. Cultures with positive indices were Gram stained and subcultured to appropriate solid media for biochemical testing and antimicrobial susceptibility testing. (ii) Catheter tips. i.v. catheter tips were rolled on an aerobic horse blood agar plate and then placed in Cooked Meat Medium (Difco, Inc., Detroit, Mich.). After incubation at 35°C for 24 h, the colonies on the plate were counted and isolates received further testing. (iii) Mitral valve tissue. Tissue was ground aseptically in a glass tissue grinder with a small amount of nutrient broth, and the homogenate was Gram stained and inoculated to appropriate aerobic and anaerobic media which were incubated for 5 days before being considered negative. (iv) Identification of staphylococci. Five isolates from the patient's specimens were simultaneously subjected to biochemical testing and antimicrobial susceptibility testing. The staphylococci were identified by using a set of 39 biochemical tests, including ornithine decarboxylase (16), modified oxidase (8), tests for free coagulase using rabbit plasma and for bound coagulase using both rabbit and human plasma (16), production of thermonuclease by the microslide method (18), nitrate reduction (17), urea hydrolysis using Christensen's urea agar (2), pyrrolidonyl arylamidase (13), hydrolysis of Tween 80 (4), resistance to 0.02% furazolidone (1), and production of CAMP factor (12). Glucose fermentation was tested with the medium of Davis and Hoyling (5), phosphatase production was tested by using the agar plate method of Geary and Stevens (11),

Underlying disease or condition

None stated Vasectomy 3 mo earlier None stated None stated Cutaneous lesion on finger None stated

None stated

Outcome

Reference

Recovered Recovered Died Died Recovered Recovered None stated

23 25 7 7 7 9 9

and hydrolysis of arginine was tested by using Moeller decarboxylase base (Difco #0890-01). Acetoin production was demonstrated by using the Coblentz method (3) after 48 h of incubation. Hydrolysis of esculin was tested by using modified esculin agar (24). DNase production was demonstrated by using DNAse test agar (BBL #11179), inoculated with a short streak and tested after 20 to 24 h of incubation by flooding with 1 N HCl. Gelatinase production was tested by using a medium consisting of 2 g of Bacto-Peptone (Difco), 0.5 g of yeast extract (Difco), 15 g of gelatin (BBL #11868), 15 g of agar, and 500 ml of distilled water. The medium was inoculated with a short streak and examined for a halo of opacity around the growth. Resistance to novobiocin was tested on Mueller-Hinton II Agar (BBL #11438) containing 1.6 mg of novobiocin per liter. The medium was spot inoculated by using a standard 0.001-ml loopful of a 0.5 McFarland standard suspension of the organism in saline. Acid production from carbohydrates was tested in Phenol Red broth (BBL #11506) containing 1% carbohydrate. The medium was dispensed in 3-ml amounts, and tubes were inoculated from an overnight heart infusion agar culture. Unless otherwise indicated, all biochemical test cultures were incubated for 72 h at 35°C. The type strain of S. lugdunensis, ATCC 43809, was tested in parallel with the clinical isolates. All of the clinical isolates and the type strain were tested with the API StaphIdent system by the method described by the manufacturer. Disk diffusion susceptibility tests were performed according to the National Committee for Clinical Laboratory Standards approved standard M2-A4 (21) with the following antibiotics: penicillin G, oxacillin, methicillin, cefazolin, tetracycline, erythromycin, clindamycin, gentamicin, vancomycin, and trimethoprim-sulfamethoxazole. Antimicrobial MICs were determined by using the Microscan broth microdilution system. The isolates were also subjected to bacteriophage typing using the international set of S. aureus bacteriophages.

RESULTS Biochemical tests. All of the clinical isolates showed identical biochemical reactions which were in turn identical to those of the type strain, ATCC 43809 (Table 2). The patient's isolates autoagglutinated in saline, so the slide coagulase test could not be performed on these isolates. In the API StaphIdent system, all the clinical isolates and the type strain yielded a code of 6500, which is not listed in the manufacturer's data base but has been previously described as characteristic of S. lugdunensis (12). Disk diffusion tests. All of the isolates appeared to be susceptible to the following antimicrobial agents: penicillin G, oxacillin, methicillin, cefazolin, tetracycline, erythromy-

1950

SHUTTLEWORTH AND COLBY

J. CLIN. MICROBIOL.

TABLE 2. Results of biochemical tests on patient isolates and the type strain of S. lugdunensis, ATCC 43809

TABLE 3. Results of broth microdilution MIC tests

Result for: Test

Patient isolates

Oxidase Tube coagulase (rabbit plasma) Clumping factor Human Rabbit Glucose fermentation Nitrate reduction Phosphatase DNase Acetoin Hydrolysis of: Urea

Antimicrobial agent Type strain

NDa ND + +

Weak

Weak

+

Arginine Esculin Gelatin Tween 80 Resistance to: Novobiocin (1.6 mg/ml) Furazolidone (0.02%) Ornithine decarboxylase CAMP factor Pyrrolidonyl arylamidase Thermonuclease production Aerobic acid from: Glucose Lactose Sucrose Mannitol Salicin Sorbitol Arabinose Raffinose Maltose Xylose Trehalose Cellobiose

Weak

Weak

+ + + +

+

+

+

Fructose Mannose Turanose

+ +

Galactose Xylitol Melezitose Ribose

+

a

ND, test not performed

as

the strains were autoagglutinable.

cin, clindamycin, gentamicin, vancomycin, and trimethoprim-sulfamethoxazole. None of the isolates produced P-lactamase as determined by nitrocefin hydrolysis. Results of broth microdilution MIC tests for the patient's strains and for the type strain ATCC 43809 are given in Table 3. All isolates from the patient gave identical results. They were susceptible to all the antibiotics tested and did not produce 13-lactamase. The type strain differed slightly from the patient's strains in tests with imipenem and erythromycin. None of these strains was phage typeable with the international set of S. aureus phages.

DISCUSSION Detailed studies of the distribution of S. lugdunensis over the human body have not been reported. Herchline and

Amikacin Amoxicillin-Clavulanate Ampicillin-Sulbactam Ampicillin Cefazolin Cefotaxime Ceftriaxone Cefuroxime Cephalothin Chloramphenicol Ciprofloxacin Clindamycin Erythromycin Gentamicin Imipenem Oxacillin Penicillin Rifampin Tetracycline Ticarcillin-Clavulanate Trimethoprim-Sulfamethoxazole Vancomycin

MIC (mg/liter) Type strain, ATCC 43809 isolatesa Patient

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