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JOURNAL OF CLINICAL MICROBIOLOGY, July 2006, p. 26502654 0095-1137/06/$08.00 0 doi:10.1128/JCM.02485-05 Copyright 2006, American Society for Microbiology.

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Vol. 44, No. 7

Clearance of Cellulosimicrobium cellulans Bacteremia in a Child without Central Venous Catheter Removal
Marie-Claire Rowlinson,1 David A. Bruckner,1 Claudia Hinnebusch,1 Karin Nielsen,2 and Jaime G. Deville2*
Department of Pathology and Laboratory Medicine1 and Department of Pediatrics,2 UCLA Medical Center, Los Angeles, California 90095
Received 30 November 2005/Returned for modication 9 January 2006/Accepted 27 April 2006

Cellulosimicrobium cellulans (formerly known as Oerskovia xanthineolytica) rarely causes human infection. Infections have been reported in immunocompromised hosts or in patients with foreign bodies, such as catheters, where treatment has generally involved removal of the foreign body. We report on a case in which the organism was isolated in multiple blood cultures from a 13-year-old male. After initial therapy failed, treatment with vancomycin and rifampin resulted in infection clearance without removal of the central venous catheter.

CASE REPORT A 13-year-old male with a history of midgut volvulus and subsequent short-bowel syndrome, who had received total parenteral nutrition since shortly after birth, presented to the Emergency Department at the University of CaliforniaLos Angeles with fever of 39C, malaise, and bilateral conjunctivitis. The patient had had numerous urinary tract infections and central venous catheter (CVC) line infections in the last few years with organisms such as Micrococcus, coagulase-negative Staphylococcus, Staphylococcus aureus, and Enterococcus species. In the emergency room, blood was drawn from the CVC and from a peripheral vein. Both specimens grew pleomorphic gram-positive rods in aerobic and anaerobic blood culture bottles that were identied as Cellulosimicrobium cellulans. The patient was hospitalized and initially treated with intravenous vancomycin and cefotaxime, which was changed 2 days later to vancomycin and gentamicin. After 3 days in the hospital, the patient became afebrile and was discharged home to continue intravenous vancomycin therapy. Blood cultures (drawn on hospital day 2) became positive for Cellulosimicrobium cellulans after 72 h. Because the patient had been discharged, he was readmitted even though he was afebrile. Due to the difculty of nding another line of intravenous access for this patient, an attempt to preserve the CVC was made by adding oral rifampin to the treatment regimen. Once rifampin was begun, subsequent blood cultures (drawn 2, 3, and 5 days after readmission, respectively) were negative. The patient was discharged home to complete therapy of 3 weeks on intravenous vancomycin and oral rifampin. A repeat culture obtained 72 h after discontinuation of antibiotics was negative. The patient has not had any recurrent infections with this organism and continues to use the CVC line on a daily basis (1 year posttherapy).

* Corresponding author. Mailing address: UCLA School of Medicine, Department of Pediatrics, 10833 LeConte Avenue, Los Angeles, CA 90095-1752. Phone: (310) 825 9660. Fax: (310) 825 9175. E-mail: jdeville@mednet.ucla.edu. 2650

Microbiology. Aerobic and anaerobic BacT/Alert (SA and SN, respectively) blood culture bottles (BioMerieux, Durham, NC) were positive after 2 days of incubation. Pleomorphic, branching and lamentous, gram-positive bacilli were detected from both bottles; however, morphology from the agar plate culture was more coccobacillary when Gram stained (Fig. 1 and 2). The organism was easily decolorized on Gram staining and was acid fast negative. Aliquots from the positive blood bottles were plated onto 5% sheep blood agar and chocolate agar plates, incubated overnight at 35C in 5% CO2, and used for further biochemical analysis. On blood agar plates, 2-mm shiny yellow colonies were evident after overnight incubation; upon subsequent incubation (5 to 7 days), the colonies became fringed with some agar penetration (Fig. 3). In this case, the pigment production was a useful diagnostic, in addition to the following biochemical reactions: catalase positive, reduction of nitrate, and hydrolysis of gelatin and esculin (27). Cellulosimicrobium cellulans and bacteria of the related genus Oerskovia are aerobic or facultatively anaerobic and metabolize a range of carbohydrates fermentatively (including glucose, maltose, mannose, sucrose, and xylose). The API Coryne biochemical strip (BioMerieux) keyed out with the number 7572727, an excellent identication for Oerskovia xanthineolytica, which is now known as Cellulosimicrobium cellulans. The API Coryne strip has proved useful in identication of this species and other coryneforms (7) and was used for identication in many of the reports reviewed (4, 10, 14, 17, 19, 23). We attempted to conrm this identication with further tests which distinguish Cellulosimicrobium cellulans from Oerskovia turbata. The organism was nonmotile in semisolid motility medium, grew at 42C, and tolerated 6% NaCl but did not hydrolyze xanthine as expected. Since hydrolysis of xanthine or hypoxanthine is a key distinguishing feature between these two species, 16S rRNA sequencing was carried out at Quest Diagnostics, Nichols Institute, San Clemente, CA, which identied the isolate as Cellulosimicrobium cellulans. Antimicrobial susceptibility tests were performed using our in-house broth microdilution microtiter panel, which was made and set up according to CLSI standard protocol (21, 22). The MICs, measured in micro-

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2651

FIG. 1. Cellulosimicrobium cellulans Gram stain from positive aerobic blood culture bottle.

grams/milliliter, were reported as follows: erythromycin, 2.0; penicillin, 2.0; vancomycin, 0.5; and rifampin, 1.0. In the absence of CLSI interpretive guidelines, the organism was presumed to be susceptible, due to the low MICs (8, 29).

FIG. 3. Cellulosimicrobium cellulans growth on 5% sheep blood agar plate after 48 h of growth, 35C, under aerobic conditions.

Discussion. Cellulosimicrobium cellulans is a nocardia-like bacillum in the suborder Micrococcineae. Cellulosimicrobium cellulans is formerly of the genus Oerskovia/Cellulans, along with other cellulolytic species, such as Cellulomonas turbata, basonym Oerskovia turbata. The relationships within and around this genus have now been reclassied on the basis of phylogenetic evidence (including 16S rRNA sequences and DNA-DNA interactions) and chemotaxonomic status (including cell wall compositions and GC content) (2, 27, 31). Identication and drug susceptibilities for this gram-positive rod and others in this group are challenging. They are uncommon pathogens, and there has been much confusion over their classication. However, there are published guides for the identication of gram-positive rods and suggested antimicrobial resistance proles (68). Conrmation by 16S rRNA sequencing is recommended. We report a catheter-related bacteremia due to Cellulosimicrobium cellulans in a child with short-bowel syndrome. A review of the literature reveals a strong correlation with compromised immune status and the presence of a foreign body (Table 1). There have been 22 reports concerning Oerskovia

FIG. 2. Cellulosimicrobium cellulans Gram stain from colony isolated on sheep blood agar.

infections in humans, 1 for Cellulosimicrobium cellulans (11), 15 for O. xanthineolytica (1, 4, 5, 8, 10, 12, 13, 1719, 23, 26, 28, 32, 33), 4 for O. turbata (14, 16, 24, 25), 1 reported as nonmotile Oerskovia (3), and 1 reported as Oerskovia species (9). The types of infections were similar for all species described and included bacteremia, peritonitis, endocarditis, and joint, ocular, and soft-tissue infections. CVC-related bacteremia was a feature in ve determined cases (4, 9, 14, 16, 18). Treatment of Oerskovia infections varies, but in more than half of the reported cases, removal of the foreign body was necessary, because therapy with single- and multidrug combinations failed to eradicate the infection. Even when treated with an antibiotic to which the organisms was presumed susceptible in vitro, there are reports of recurrence and persistence of infections (4, 13, 16, 25, 26, 33). In cases where there was a foreign body, symptoms disappeared when the foreign body was removed. It is possible that antibiotics were unable to penetrate the infected area, perhaps inhibiting but not eradicating the organism (4, 20). Oerskovia species are widely distributed in the environment and have been isolated from soil, water, and grass cuttings (15), and as with other environmental bacteria, these bacteria are fairly resistant to antimicrobial agents but do not appear to be particularly virulent; no deaths were attributed to the infections (29, 33). In vitro, they have exhibited resistance to a range of antimicrobials: penicillins, aminoglycosides, macrolides, and cephalosporins. They were reported as resistant (or intermediate) to erythromycin in many reports, although specic antibiotics and the methods by which resistance was assessed varied (3, 5, 10, 19, 23, 26, 28, 32). This is expected, since resistance to erythromycin and other macrolides is high among aerobic and facultative anaerobic, non-spore-forming grampositive bacilli (29). These bacteria are considered vancomycin susceptible in vitro, and in most reports, this has been the antibiotic of choice. Although three cases involved catheterrelated infection, intravenous vancomycin alone was enough to clear the infection without removal of the line (9, 17, 18). In

TABLE 1. Summary of Oerskovia species (i.e., Cellulosimicrobium cellulans and Oerskovia turbata) infection case reports in the medical literature to date, in chronological order a 2652
Underlying condition Infection Unknown Unknown Unknown Foreign body/removal 26 O. xanthineolytica isolates; 9 O. turbata isolates O. turbata Aortic heart valve/yes None Machine metal/yes VP shunt/yes CVC/yes CVC/no AMK Nonmotile Oerskovia Pyonephrosis Endophthalmitis Meningitis CVC-related bacteremia O. xanthineolytica O. xanthineolytica O. turbata Oerskovia species O. xanthineolytica O. turbata O. xanthineolytica Axillary abscess Bacteremia Soft tissue infection O. xanthineolytica O. xanthineolytica O. xanthineolytica Probable bacteremia (Cholecystitis) Bacteremia Pneumonia? CVC/no Peritoneal catheter/ yes Unknown None Bacteremia (TPN contamination) Peritonitis VAN GEN MET 3 VAN alone VAN GEN 8 O. xanthineolytica from blood (clinical signicance unknown) Endocarditis Cellulosimicrobium/ Oerskovia species Treatment regimenb Reported resistancec Laboratory identication method

Case report author (reference)

Patients age (yr)/ sex/other signicance

Sottnek d (30)

Suspected infection; 35 cases

CASE REPORTS

Reller (25)

68/M/urban

Cruickshank (3)

47/F/rural; farmer

Crohns, ankylosing spondylitis Kidney trouble?

Hussain (12)

None

No single agent was highly active BEN, TET, ERY, KAN, SUL CLI, GEN

Kailath (13)

47/M/rural; farmer 38/F

VP shunt

SXT AMP 3 AMX Nephrectomy, antibiotic regimen unknown AMB GEN 3 PEN 3 CFL PEN RIF

LeProwse (16)

3/M/camping

Acute myelogenous leukemia

Culture morphology, biochemical tests, and whole-cell analysis Culture, biochemical tests Culture, biochemical tests Culture, biochemical tests Culture, biochemical tests (hydrolysis of xanthine) Culture, biochemical tests -Lactamase negative (I-PEN, AMP, ERY) OXA, CFZ

Guss (9)

40/F

Rihs (26)

70/M

Crohns, short bowel syndrome ESRD

Reina (24) Truant (32)

23/M 40/M

AIDS Cirrhosis, Variceal hemorrhage

CTX, CRO DOX, CLI, GEN, ERY Unknown GEN, CLI, ERY For both isolates CIP, CLI, ERY, GEN, PEN

Culture, biochemical tests Culture, biochemical tests Unknown Culture, biochemical tests

Funkee (5)

53/F/iatrogenic

Unknown CRO CLI, 3 CRO VAN 3 GEN DOX Laparotomy, CFX CXM 3 VAN

72/M/iatrogenic

Arthropathy in several joints Gall stones, jaundice

McDonald (19)

54/F

Metastatic breast cancer O. xanthineolytica O. xanthineolytica O. xanthineolytica O. xanthineolytica Keratitis Prosthetic knee joint infection CVC-related bacteremia Peritonitis

Rumalon, steroid injections Cholangio-pancreatic endoscopy CVC (role?)/no

PEN, OXA, AMP (I-CLI, ERY) VAN VAN CFZ VAN TOB 3 DOX GEN drops SXT

Maguire (18)

49/F

Culture, biochemical tests (API hydrolysis of xanthine) Culture, biochemical tests (API hydrolysis of xanthine) Culture -Lactamase positive PEN Culture ERY, SXT CLI, PEN (I-ERY) (sendout tests at CDC found R to SXT, CIP, ERY) Culture Culture, biochemical tests (API hydrolysis of xanthine)

Borra (1)

59/F

Shah (28) Harrington (10)

28/F 72/M

Peritoneal catheter/ No Soft contact lens/yes Prosthetic knee joint/ yes

Lair (14) O. xanthineolytica O. xanthineolytica O. xanthineolytica

27/M/nosocomial

Metastatic colonic adeno carcinoma Diabetes mellitus, ESRD None Heart bypass surgery, hypothyroidism, ethanol abuse, total left knee replacement HIV O. turbata Nosocomial CVCrelated bacteremia

CVC/Yes CVC/Yes

IPM

AMK

CTX, NET CRO (I-PEN)

Ellerbroek (4)

53/F

Lujan-Zilbermann (17)

13/F

Non-Hodgkins lymphoma (and BMT) ESRD

CVC-related bacteremia3 Endocarditis Peritonitis Bacteremia

DOX 3 CLI 3 MPM 3 SXT AMX 3 PEN VAN Peritoneal catheter/ No None TZP 3 NET again NET 3 VAN 3 TZP

J. CLIN. MICROBIOL.

Niamut (23)

64/F

Immunocompromised

AMP, CRO, CLI, PEN, OXA, TOB PEN, NET, TET, ERY

Culture, biochemical tests (API hydrolysis) Culture, biochemical tests (API hydrolysis) Culture, biochemical tests (API) Culture, biochemical tests (API), 16S rRNA sequencing

VOL. 44, 2006


a ESRD, end-stage renal disease; BMT, bone marrow transplant; CVC, central venous catheter; HIV, human immunodeciency virus; VP shunt, ventriculoperitoneal shunt; I, intermediate resistance; R, resistance. Antimicrobial agents used were amikacin (AMK), amoxicillin (AMX), amphotericin B (AMB), ampicillin (AMP), ampicllin-sulbactam (SAM), azithromycin (AZI), benzylpenicillin (BEN), cefazolin (CFZ), cefotaxime (CTX), cefoxitin (CFX), ceftriaxone (CRO), cefuroxime (CXM), cephalexin (CFL), ciprooxacin (CIP), clindamycin (CLI), doxycycline (DOX), erythromycin (ERY), gentamicin (GEN), imipenem (IPM), kanamycin (KAN), meropenem (MPM), metronidazole (MET), netilmicin (NET), oxacillin (OXA), penicillin (PEN), piperacillin-tazobactam (TZP), rifampin (RIF), sulfonamide (SUL), tetracycline (TET), tobramycin (TOB), trimethoprim-sulfamethoxazole (SXT), and vancomycin (VAN). b An arrow indicates a change or an addition to a treatment regimen. c Resistance to antibacterial agents was tested by various previously reported methods, mainly the disk diffusion or microdilution method. However, with a few CLSI guidelines for Coryneform bacteria, susceptibility testing is not standardized. d A retrospective review of 35 diphtheroids submitted to CDC from 1957 to 1977. e Funke et al. also report on a third isolate that was thought to be a contaminant and is therefore not included here.

CASE REPORTS

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the case reported by Truant et al., the patient was receiving vancomycin (to treat methicillin-resistant S. aureus) prior to isolating the organism from blood culture; the isolate was subsequently susceptible to vancomycin in vitro (32). Rihs et al. reported that despite prolonged treatment with vancomycin, it was not sufcient in clearing the infection until the line was removed (26). In the present case, vancomycin was also not adequate, and rifampin was added to clear infection without catheter removal. The epidemiology and pathogenicity of Cellulosimicrobium cellulans (Oerskovia xanthineolytica) and Oerskovia turbata infections is of growing relevance in clinical microbiology. Oerskovia species have been isolated from the environment (and caused infections in both rural and urban patients), but in addition there have also been cases of nosocomial and iatrogenic infection, indicating their ubiquity in nature (5, 14). We should be aware of these opportunistic pathogens, as it is likely that there will be an increase in infections caused by them, related to the ever-increasing number of patients with immunocompromised status and the presence of long-term foreign bodies.
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PEN, AMP, CRO, CLI None VAN AZI PEN Cellulosimicrobium cellulans 48/M/urban Heym (11) Aortic heart valve/ Yes None Endocarditis (line related?) Chronic tongue ulcer ESRD, renal transplant HIV 31/M Urbina (33) O. xanthineolytica SAM

Present case

13/M/urban

Short-bowel syndrome

Cellulosimicrobium cellulans

CVC-related bacteremia

CVC/No

VAN 3

RIF

CTX, CRO, CLI

The organism was not isolated; 16S rRNA sequencing Culture, biochemical tests (API), 16S rRNA sequencing

Culture

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27. Schumann, P., N. Weiss, and E. Stackebrandt. 2001. Reclassication of Cellulomonas cellulans (Stackebrandt and Keddie 1986) as Cellulosimicrobium cellulans gen. nov., comb. nov. Int. J. Syst. Evol. Microbiol. 51:10071010. 28. Shah, M., R. C. Gentile, S. A. McCormick, and S. H. Rogers. 1996. Oerskovia xanthineolytica keratitis. CLAO J. 22:96. 29. Soriano, F., R. Fernandez-Roblas, R. Calvo, and G. Garcia-Calvo. 1998. In vitro susceptibilities of aerobic and facultative non-spore-forming gram-positive bacilli to HMR 3647 (RU 66647) and 14 other antimicrobials. Antimicrob. Agents Chemother. 42:10281033. 30. Sottnek, F. O., J. M. Brown, R. E. Weaver, and G. F. Carroll. 1977. Recognition of Oerskovia species in the clinical laboratory: characterization of 35 isolates. Int. J. Syst. Bacteriol. 27:263270. 31. Stackebrandt, E., S. Breymann, U. Steiner, H. Prauser, N. Weiss, and P. Schumann. 2002. Re-evaluation of the status of the genus Oerskovia, reclassication of Promicromonospora enterophila (Jager et al. 1983) as Oerskovia enterophila comb. nov. and description of Oerskovia jenensis sp. nov. and Oerskovia paurometabola sp. nov. Int. J. Syst. Evol. Microbiol. 52:1105 1111. 32. Truant, A. L., V. Satishchandran, R. Eisenstaedt, P. Richman, and M. M. McNeil. 1992. Oerskovia xanthineolytica and methicillin-resistant Staphylococcus aureus in a patient with cirrhosis and variceal hemorrhage. Eur. J. Clin. Microbiol. Infect. Dis. 11:950951. 33. Urbina, B. Y., R. Gohh, and S. A. Fischer. 2003. Oerskovia xanthineolytica endocarditis in a renal transplant patient: case report and review of the literature. Transpl. Infect. Dis. 5:195198.

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