Infection (2015) 43:103–106 DOI 10.1007/s15010-014-0672-7

CASE REPORT

First report of bacteremia by Janibacter terrae in humans M. I. Ferna´ndez-Natal • J. A. Sa´ez-Nieto • M. J. Medina-Pascual • S. Valdezate-Ramos • J. M. Guerra-Laso • R. H. Rodrı´guez-Polla´n F. Soriano



Received: 20 May 2014 / Accepted: 23 July 2014 / Published online: 19 August 2014 Ó European Union 2014

Abstract The genus Janibacter comprises nine different species mainly found in the environment. Only two human infections by these microorganisms have been previously reported, one by J. melonis and another one by an undescribed Janibacter sp. Herewith we report the first human cases of infection by J. terrae in four bacteremic patients. The microorganisms were isolated from two consecutive blood cultures taken from four febrile patients with several underlying conditions. All patients were treated with antibiotics, two of them with favorable outcome. Two severely immunocompromised patients died, and one was treated with an antibiotic in vitro active against the isolate. Janibacter terrae was identified by phenotypic and 16S rDNA amplification methods. This report includes also the first This work was presented in part to the 24th European Congress of Clinical Microbiology and Infectious Diseases, Barcelona, Spain, May 2014 (abstract no. P0413). M. I. Ferna´ndez-Natal (&)  R. H. Rodrı´guez-Polla´n Department of Clinical Microbiology, Complejo Asistencial Universitario de Leo´n, calle Altos de Nava, s/n, 24080 Leo´n, Spain e-mail: [email protected] M. I. Ferna´ndez-Natal Institute of Biomedicine (IBIOMED), Leo´n, Spain J. A. Sa´ez-Nieto  M. J. Medina-Pascual  S. Valdezate-Ramos Bacterial Taxonomy Laboratory, Centro Nacional de Microbiologı´a, Instituto de Salud Carlos III, Majadahonda, Madrid, Spain J. M. Guerra-Laso Department of Internal Medicine, Complejo Asistencial Universitario de Leo´n, Leo´n, Spain F. Soriano Public Health, School of Physiotherapy ONCE, Madrid, Spain

data on antimicrobial susceptibility of this opportunistic pathogen. Clinical microbiologists should be aware of this microorganism which can be identified by phenotypic and molecular methods. Keywords Bacteremia  Janibacter terrae  Identification  Antimicrobial susceptibility

Introduction Members of the genus Janibacter, family Intrasporangiaceae and class Actinobacteria were described in 1997 after identifying two strains of novel actinobacteria isolated from a wastewater treatment plant [1]. These microorganisms present a characteristic rod-coccus cycle during growth resembling the two faces which characterized Janus, a god in the old roman mythology. This is not a definitive feature of these microorganisms, as such morphologic characteristic is shared with some members of the Arthrobacter and Brevibacterium genus. The genus Janibacter is nonsporeforming, nonmotile, aerobic, oxidase variable, and catalase-positive gram-positive organisms. Colonies are smooth, circular, convex, and vary in color from white to yellow. The optimal growth is between 23 and 35 °C. Mycolic acids are absent, and the G ? C content is 69–73 mol%. At present, nine species have been described: J. limosus, J. terrae, J. indicus, J. melonis, J. anophelis, J. hoylei, J. corallicola, J. alkaliphilus, and J. cremeus [1–9]. Janibacter limosus and J. terrae have been isolated from wastewater-contaminated soils and J. indicus from hidrotermal sediment of the Indian Ocean, and J. corallicola and J. alkaliphilus from coral. Janibacter melonis, J. anophelis, and J. hoylei have been isolated from plants, insects, and air, respectively.

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To the best of our knowledge, only two cases of Janibacter isolation from human specimens have been reported. The first case was a bacteremia by an undescribed species of Janibacter in a patient treated for myeloid leukemia [10] and the second was a bacteremia by J. melonis in a patient with low-grade fever without underlying disease [11]. Herewith we present the clinical and microbiological features related to four patients, studied during a 3-year period, from whom J. terrae was isolated from blood cultures.

Case reports Four patients with a mean age of 69 years, attended between December 2001 and December 2003 in a regional hospital in Spain, were diagnosed of bacteremia by J. terrae after isolating this organism in pure culture from two separate and consecutive blood cultures. All patients had severe underlying conditions and had fever when blood cultures were taken. Two patients suffered from severe pulmonary infection, one of cholangitis, and in the fourth no identifiable focus was detected. One patient had a Hickman catheter. Patients 1–3 received antibiotics (amoxicillin, tobramycin, and amikacin) for which the isolates showed low MIC values (B3 mg/l) while the fourth patient was treated with an antibiotic later known to be inactive against the isolate (piperacillin MIC [256 mg/ l). Antibiotics were maintained for 10–16 days and patients 3 and 4, both severely immunocompromised, died. Table 1 presents the main clinical characteristics of the four patients. Blood samples were inoculated in BacT/AlerTTM aerobic and anaerobic blood cultures bottles (bioMe´rieux, Marcy-l´Etoile, France) incubated at 35 °C. The microorganisms were recovered from eight blood cultures (two positive blood cultures per patient) and only from the aerobic bottles. After 48 h incubation in air at 35 °C, colonies on blood agar were non-hemolytic, circular, convex, opaque, glistening, and cream-colored which changed to a

yellowish with longer incubation. The isolates were identified using API CoryneTM V2.0 (bioMe´rieux). Additional tests were studied with the aid of API StrepTM (hippurate hydrolysis) and API NETM (assimilation of maltose, Nacetyl-glucosamine, and phenylacetic acid). In addition, catalase, oxidase, lipophilia, glucose fermentation at 42 °C, growth on blood agar at 20 °C, and susceptibility to vibriostatic factor O/129 were also studied following the described methods [12]. All strains presented the same API profile (3112004) read after 48 h, and without modification after 7 days. Such a profile suggests its possibility to be a member of the Rhodococcus, Arthrobacter or Brevibacterium species. Positive reaction was observed for catalase, nitratase, pyrazinamidase, alkaline phosphatase, a-glucosidase, hydrolysis of gelatin and hippurate, and maltose assimilation. On the other hand, the organisms were oxidase-negative, assacharolytic, unable to assimilate, N-acetylglucosamine and phenylacetic acid. All strains were inhibited by the O/129 (150 lg) factor showing an inhibition diameter between 46 and 48 mm. In addition, 16S rDNA amplification and sequencing were also performed according to the method previously described [13]. The fragments of 16S rRNA obtained from the four isolates (CNM582-06, CNM586-06, CNM588-06, and CNM65406) were: 1,136, 1,198, 1,158 and 1,153 bp. respectively. The similarity with the GenBank previous sequences of J. terrae were: 99.6, 99.5, 99.6 and 99.6 % (GenBank sequence no. NR_036868). Antimicrobial susceptibility testing to 27 antimicrobials was determined by Etest on Mueller–Hinton agar with 5 % blood, incubated in air at 35 °C, and read after 48 h. Susceptibility to antibiotics was interpreted following the recommended criteria for coryneform organisms [14]. Table 2 presents the antimicrobial susceptibility to the antibiotics for the four strains tested.

Discussion The genus Janibacter has been mainly isolated from the environment including wastewater contaminated soils,

Table 1 Clinical data from four patients with Janibacter terrae bacteremia Case

Month/ year

Age (years)

Sex

Underlying conditions

Diagnosis

Antimicrobial treatment (days)

1

12/2001

66

M

2

03/2002

66

F

3

04/2002

67

F

4

12/2003

77

M

Non-Hodgking’s lymphoma, BMA, Hickman catheter Gastric cancer, liver metastasis CD toxin positive in stool

COPD

Acute bronchitis

Amoxicillin/clavulanic (10)

Cure

Diabetes

Cholangitis

Amoxicillin/clavulanic ? tobramycin (12)

Cure

Multilobar pneumonia Myelodysplastic syndrome, fever of unknown origin

Ceftazidime ? amikacin ? metronidazole (16) Piperacillin/tazobactam (15)

Exitus

COPD, chronic obstructive pulmonary disease; BMA, bone marrow aplasia; CD, Clostridium difficile

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Outcome

Exitus

First report of bacteremia Table 2 Antimicrobial susceptibility (MIC, mg/l) of four J. terrae strains to 27 antimicrobials

Antibiotics written in bold are those proposed for testing coryneform organisms, and MIC values within the range of susceptibility are in cursive (all based on reference [14])

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Antimicrobial

Strain 1 (CNM582-06)

Strain 2 (CNM586-06)

Strain 3 (CNM588-06)

Strain 4 (CNM654-06)

Benzylpenicillin

2

1

2

2

Ampicillin

8

4

8

8

Amoxicillin

3

2

3

3

Piperacillin

[256

[256

[256

[256

Cefotaxime

4

3

4

3

Ceftazidime

[256

[256

[256

[256

Imipenem

0.125

0.19

0.19

0.25

Vancomycin

0.5

0.5

0.5

0.5

Teicoplanin

0.75

0.75

0.75

1

Linezolid

0.5

0.75

0.5

1

Daptomycin Tetracycline

0.064 1.5

0.064 1.5

0.064 1

0.064 3

Tigecycline

0.19

0.38

0.38

0.5

Ciprofloxacin

0.25

0.19

0.25

0.25

Moxifloxacin

0.064

0.047

0.064

0.047

Levofloxacin

0.25

0.19

0.25

0.38

Erythromycin

0.5

0.38

0.25

0.25

Clarithomycin

0.25

0.125

0.064

0.064

Azithromycin

0.75

0.75

0.38

0.5

Clindamycin

3

6

6

6

Quinupristin-dalfopristin

[32

[32

[32

[32

Gentamicin

1.5

1.5

2

3

Tobramycin

2

3

2

4

Amikacin

0.75

0.75

1

0.5

Rifampin

[32

[32

[32

[32

Cotrimoxazole

\0.002

\0.002

\0.002

\0.002

Metronidazole

[256

[256

[256

[256

coral, plants, and air [1–3, 5–9]. Janibacter anophelis was isolated from the midgut of Anopheles arabiensis [4]. Only two bacteremias in humans caused by Janibacter have been reported and in both cases after one single positive blood culture. In one case, the species isolated could not be identified [10] and in the second it was identified as J. melonis [11]. Janibacter terrae had been exclusively isolated from environmental samples such as soil and water [2, 15]. Our case reports show that J. terrae is not only an environmental organism but may also be isolated from clinical specimens. At present, no human infections by J. terrae have been reported and we present four well-documented cases of bacteremia detected in different periods of time, making the possibility of a laboratory contamination very unlikely. Furthermore, the organisms were isolated from four febrile patients in whom two consecutive blood cultures taken gave the same microorganism. We do not know the mechanism favoring J. terrae bacteremia. As an environment inhabitant, we can speculate with a previous skin colonization and later penetration of the microorganism facilitated using invasive medical care. At least, one

patient (number 3) had a Hickman catheter and another one (number 4) was so severely immunocompromised that an invasive, although unregistered procedure, cannot be ruled out. Phenotypic methods can be used to identify Janibacter species and the API CoryneTM system may be used as an aid for identification, although this bacterial genus is not included in its data base. Amplification and sequencing of 16S rDNA were very useful and reliable tools for identifying J. terrae. There are no published data on antimicrobial susceptibility of any of the known species of Janibacter. Applying the Clinical and Laboratory Standards Institute for antimicrobial susceptibility of coryneform organisms [14], our J. terrae isolates were uniformly sensitive to imipenem, vancomycin, linezolid, daptomycin, tetracycline, ciprofloxacin, erythromycin, gentamicin, and cotrimoxazole. Only one isolate was susceptible to benzylpenicillin while the others had an MIC very close to the susceptibility value. On the contrary, all isolates were resistant to cefotaxime, clindamycin, quinupristin–dalfopristin, and

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rifampin. Loubinoux et al. [10] referred very low (\0.75 mg/l) MICs to penicillin G, amoxicillin, piperacillin, gentamicin, tobramycin, ciprofloxacin, vancomycin, and teicoplanin and higher values (falling in the resistance category) for cefotaxime and cefepime in the single unidentified species of Janibacter isolated from a bacteremic patient. Our results show moderate MIC values for benzylpenicillin, ampicillin, and amoxicillin and high MICs for piperacillin and cephalosporins suggesting a different affinity of the betalactams for the protein-binding penicillins of Janibacter species. In summary, these case report show that J. terrae is not only present in the environment but may also be isolated from clinical specimens. Thus, this species may be considered an opportunistic pathogen responsible for bacteremia in patients with severe underlying diseases. Clinical microbiologists should be aware of this microorganism which can be identified by phenotypic and molecular methods. Antimicrobial susceptibility should also be determined for a best election of the antimicrobial drug to be administered. Nucleotide sequence accession numbers 16S rRNA sequences of the studied strains CNM582-06, CNM586-06, CNM588-06 and CNM654-06 were assigned to the GenBank accession numbers KJ768434 to KJ768437. Acknowledgments Part of this study has been supported by the Gerencia Regional de Salud, Junta de Castilla y Leo´n, Spain. Research project GRS 698/A/2011. Conflict of interest

No conflict of interest.

References 1. Martin K, Schumann P, Rainey FA, Schuetze B, Groth I. Janibacter limosus gen. nov., sp.nov; a new Actinomycete with meso-diaminopimelic acid in the cell wall. Int J Syst Bacteriol. 1997;47:529–34. 2. Yoon J-H, Lee K-C, Kang S-S, Kho YH, Kang KH, Park Y-H. Janibacter terrae sp. nov., a bacterium isolated from soil around a wastewater treatment plant. Int J Syst Evol Microbiol. 2000;50:1821–7.

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3. Yoon J-H, Lee BL, Yeo S-H, Choi J-E. Janibacter melonis sp. nov., isolated from abnormally spoiled oriental melon in Korea. Int J Syst Evol Microbiol. 2004;54:1975–80. 4. Ka¨mpfer P, Terenius O, Lindh JM, Faye I. Janibacter anophelis sp. nov., isolated from the midgut of Anopheles arabiensis. Int J Syst Evol Microbiol. 2006;56:389–92. 5. Shivaji S, Chaturvedi P, Begum Z, Pindi PK, Manorama R, Padmanaban DA, Shouche YS, Pawar S, Vaishampayan P, Dutt CBS, Datta GN, Manchanda RK, Rao UR, Bhargava PM, Narlikar JV. Janibacter hoylei sp. nov., Bacillus isronensis sp. nov. and Bacillus aryabhattai sp. nov., isolated from cryotubes used for collecting air from the upper atmosphere. Int J Syst Evol Microbiol. 2009;59:2977–86. 6. Kageyama A, Takahashi Y, Yasumoto-Hirose M, Kasai H, Shizuri Y, Omura S. Janibacter corallicola sp. nov., isolated from coral in Palau. J Gen Appl Microbiol. 2007;53:185–9. 7. Li J, Long L-J, Yang L-L, Xu Y, Wang F-Z, Li Q-X, Zhang S, Li W-J. Janibacter alkaliphilus sp. nov., isolated from coral Anthogorgia sp. Antonie Van Leeuwenhoek. 2012;102:57–62. 8. Hamada M, Shibata C, Tamura T, Yamamura H, Hayakawa M, Suzuki K. Janibacter cremeus sp. nov., an actinobacterium isolated from sea sediment. Int J Syst Evol Microbiol. 2013;63:3687–90. 9. Zhang G, Ren H, Wang S, Chen X, Yang Y, Zhang Y, Jiang Y. Janibacter indicus sp.nov. isolated from the Indian ocean. Int J Syst Evol Microbiol. 2014;. doi:10.1099/ijs.0.059527-0. 10. Loubinoux J, Rio B, Mihaila L, Foı¨s E, Le Fleche A, Grimont PAD, Marie J-P, Bouvet A. Bacteremia caused by an undescribed species of Janibacter. J Clin Microbiol. 2005;43:3564–6. 11. Elsayed S, Zhang K. Bacteremia caused by Janibacter melonis. J Clin Microbiol. 2005;43:3537–9. 12. Ferna´ndez-Natal MI, Sa´ez-Nieto JA, Valdezate S, Rodrı´guezPolla´n RH, Lapen˜a S, Cacho´n F, Soriano F. Isolation of Corynebacterium ureicelerivorans from normally sterile sites in humans. Eur J Clin Microbiol Infect Dis. 2009;28:677–81. 13. Drancourt M, Bollet C, Carlioz A, Martelin R, Gayral JP, Raoult D. 16S ribosomal DNA sequence analysis of a large collection of environmental and clinical unidentifiable bacteria isolates. J Clin Microbiol. 2000;38:3623–30. 14. Clinical and Laboratory Standards Institute. Methods for Antimicrobial dilution and disk susceptibility testing of infrequently isolated or fastidious bacteria; approved guideline-second edition M45-A2. Clinical and Laboratory Standards Institute, Wayne, PA. 2013; vol 30, no 18. 15. Lang E, Kroppenstedt RM, Swiderski J, Schumann P, Ludwig W, Schmid A, Weiss N. Emended description of Janibacter terrae, including ten dibenzofuran-degrading strains and Janibacter brevis as its later heterotypic synonym. Int J Syst Evol Microbiol. 2003;53:1999–2005.

First report of bacteremia by Janibacter terrae in humans.

The genus Janibacter comprises nine different species mainly found in the environment. Only two human infections by these microorganisms have been pre...
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