Accepted Manuscript Skin and soft-tissue infection caused by Actinobaculum schaalii: report of two cases and literature review Daniel Tena, Dr. Cristina Fernández, María R. Lago, Marta Arias, María José Medina, Juan Antonio Sáez-Nieto PII:

S1075-9964(14)00059-6

DOI:

10.1016/j.anaerobe.2014.05.009

Reference:

YANAE 1297

To appear in:

Anaerobe

Received Date: 12 March 2014 Revised Date:

20 May 2014

Accepted Date: 21 May 2014

Please cite this article as: Tena D, Fernández C, Lago MR, Arias M, Medina MJ, Sáez-Nieto JA, Skin and soft-tissue infection caused by Actinobaculum schaalii: report of two cases and literature review, Anaerobe (2014), doi: 10.1016/j.anaerobe.2014.05.009. This is a PDF file of an unedited manuscript that has been accepted for publication. As a service to our customers we are providing this early version of the manuscript. The manuscript will undergo copyediting, typesetting, and review of the resulting proof before it is published in its final form. Please note that during the production process errors may be discovered which could affect the content, and all legal disclaimers that apply to the journal pertain.

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Skin and soft-tissue infection caused by Actinobaculum schaalii: report of two cases and

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literature review

3 Authors: Daniel Tena1, Cristina Fernández1, María R. Lago1, Marta Arias1, María José Medina2,

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Juan Antonio Sáez-Nieto2

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Sección de Microbiología. Hospital Universitario de Guadalajara. Guadalajara, Spain.

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Servicio de Bacteriología, Centro Nacional de Microbiología, Instituto de Salud Carlos III,

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Carretera de Majadahonda-Pozuelo km 2. 28220 Majadahonda, Madrid, Spain.

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Running title: Skin and soft tissue infection caused by Actinobaculum schaalii

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Corresponding author: Dr. Daniel Tena. Sección de Microbiología. Hospital Universitario de

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Guadalajara. C/. Donantes de sangre s/n. 19002 Guadalajara. Spain. Phone: +34-949-209236. Fax:

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+34-949-209213. E-mail: [email protected]

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ABSTRACT

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Skin and soft-tissue infections (SSTIs) caused by Actinobaculum spp. are very rare. In the present

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study, we report two cases and review the literature. The first case was an immunocompromised

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patient with an extensive cellulitis secondary to an inguinal abscess, and the second case was a

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patient with a pilonidal abscess. Clinical outcome of both patients was good after surgical drainage

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and treatment with cloxacillin. The review of the literature shows that SSTIs caused by

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Actinobaculum spp. are usually located on the perineal and inguinal regions and can be severe,

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particularly in immunocompromised patients. SSTIs caused by Actinobaculum spp. can be

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overlooked because identification is often difficult and they can be considered as contaminants.

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Keywords: Skin and soft tissue infection; Actinobaculum schaalii; cellulitis; pilonidal abscess

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INTRODUCTION Actinobaculum spp. are Gram-positive, facultative anaerobic, non-motile, rod-shaped

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organisms phylogenetically related to Actinomyces spp. [1]. To date, four different species have been

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described: A. suis, A. schaalii, A. massiliense and A. urinale. These organisms are emerging

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pathogens, with more than 127 human infections reported during the last decade [2, 3]. A. schaalii is

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the most common species and has been reported as a cause of urinary tract infection, mainly in

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elderly patients with underlying urological conditions [2, 3, 4]. In addition, numerous cases of severe

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infections have been described such as urosepsis, bacteremia, endocarditis, spondylodiscitis,

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osteomyelitis and abscesses of different locations [2]. In contrast, skin and soft-tissue infections

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(SSTIs) are very rare. In the present report we describe two cases of SSTIs caused by A. schaalii and

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review the literature.

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CASE 1

A 48-year-old woman currently receiving tamoxifen due to an invasive ductal breast cancer

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which was treated 2 years ago with surgery, chemotherapy and radiotherapy, was admitted to the

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emergency department complaining of inguinal pain. Physical examination revealed an inguinal

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abscess and an extensive inguinal cellulitis. The abscess was drained and a sample was taken for

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culture. Gram stain of the aspirate revealed abundant leukocytes without organisms. The sample was

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cultured on blood agar, chocolate agar and McConkey agar plates and incubated at 37ºC in 5% CO2.

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In addition, the sample was also cultured on a Schaedler agar plate and incubated at 37ºC in

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anaerobic conditions. After 48 hours of incubation under anaerobic conditions, tiny gray colonies

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were observed. Gram staining of the colonies revealed small non-spore-forming Gram-positive

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coccoid rods. The catalase reaction was negative. The Api rapid ID32A system (bioMérieux, Marcy-

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l´Etoile, France) failed to identify the organism. The strain was sent to the National Reference

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Laboratory of Majadahonda for identification. The isolate was identified as A. schaalii by means of

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16S rRNA sequence analysis using a previously reported method [5]. The fragment of 16S rRNA

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gene obtained from this isolate was 1392 bp. and the similarity with the GenBank sequences was

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99.8% (GeneBank sequences FJ711192, AF487680, HQ992248 and others). Antimicrobial

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susceptibility testing was performed using the E-Test method (AB Biodisk, Solna, Sweden) on

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Brucella agar plates incubated at 37ºC in anaerobic atmosphere for 48 h. The breakpoints used were

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those defined by the Clinical and Laboratory Standards Institute (CLSI) for anaerobic organisms [6].

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The strain was susceptible to penicillin (MIC: 0.06 mg/L), cloxacillin (MIC: 0.06 mg/L),

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amoxicillin/clavulanic acid (MIC: 0.016 mg/L), imipenem (MIC: 0.003 mg/L), clindamycin (MIC:

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0.32 mg/L), and resistant to metronidazole (MIC: > 256 mg/L) and moxifloxacion (MIC: > 32

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mg/L). The patient was initially treated with cloxacillin for 10 days with resolution of the infection.

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CASE 2

A 25-year-old man was admitted to the emergency department with a 48-hour history of

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coccygeal pain. His medical history was unremarkable. Physical examination revealed a painful

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pilonidal abscess. The abscess was drained and a sample was taken for culture. Gram stain of the

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aspirate revealed abundant leukocytes and Gram-positive coccoid rods. The sample was cultured on

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blood agar, chocolate agar and McConkey agar plates and incubated at 37ºC in 5% CO2. In addition,

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the sample was also cultured on a Schaedler agar plate and incubated at 37ºC in anaerobic

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conditions. Small colonies (0.2 to 0.5 mm) were observed after 48 hours of incubation under

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anaerobic conditions. The colonies appeared grey and nonhemolytic. The catalase reaction was

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negative. Gram staining of the colonies revealed small non-spore-forming Gram-positive coccoid

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rods. Aerobically grown colonies were hardly visible even after 4 days. The Api rapid ID 32A

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system (bioMérieux, Marcy-l´Etoile, France) failed to identify the organism. The strain was sent to

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the National Reference Laboratory of Majadahonda for identification. The isolate was identified as

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A. schaalii by means of 16S rRNA sequence analysis using a previously reported method [5]. The

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fragment of 16S rRNA gene obtained from this isolate was 1187 bp. and the similarity with the

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GenBank sequences was 99.6% (GeneBank sequences FJ711192, AF487680, HQ992248 and

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others). Antimicrobial susceptibility testing was performed using the same method described in the

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case 1. The strain was susceptible to penicillin (MIC: 0.023 mg/L), cloxacillin (MIC: 0.016 mg/L),

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amoxicillin/clavulanic acid (MIC: 0.016 mg/L), imipenen (MIC: 0.003 mg/L), moxifloxacin (MIC:

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0.012 mg/L), and resistant to clindamycin (MIC: >256 mg/L) and metronidazole (MIC: >256 mg/l).

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The patient was treated with cloxacillin for 7 days with resolution of the infection.

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Actinobaculum spp. is a very uncommon cause of SSTI. The role of this group of organisms

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as primary pathogens in these infections is poorly understood. Only sporadic SSTIs have been

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previously described in the literature [7-10]. Relevant data of these cases are presented in table 1. In

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addition, two surgical site infections (upper jaw and after bladder-stone extraction), and three skin

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abscesses have been reported [11, 12]. Two of these abscesses were located on the breast and

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inguinal fold. Actinobaculum spp. are probably part of the commensal flora of the human

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genitourinary tract [1]. A recent study showed that 22% of 252 urine samples from patients > 60

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years were positive for A. schaalii using real-time PCR [4]. Interestingly, A. schaalii was found on

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skin, urine and vaginal mucosa in the human urogenital area in elderly patients with kidney or ureter

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stones [13]. In our review, most of SSTIs caused by Actinobaculum spp. were located on perineum,

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groin, scrotum and coccyx. However, SSTIs can be located in other anatomical regions, including

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jaw, chest wall and breast [7, 12]. Although the number of patients is very small, these cases suggest

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that Actinobaculum spp. may be also a commensal organism in other locations outside the

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genitourinary tract. Further studies should be performed in the future to know better the habitat of

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this organism. The elderly are at greatest risk of being colonized with A. schaalii in the genitourinary

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tract [2, 4, 13], but only one patient was elderly in our review [10]. The invasive potential of Actinobaculum spp. has long been considered limited although

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recent studies describe the implication of this organism in infections such as bacteremia,

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osteomyelitis and endocarditis [2]. SSTIs caused by Actinobaculum spp. can be very serious in

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patients with underlying diseases. Vanden Bempt et al. reported a Fournier´s gangrene caused by A.

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schaalii in an obese smoker diagnosed of diabetes mellitus [9]. In addition, a perineal necrotizing

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cellulitis was described in a patient with prostatic cancer [10]. One of our patients suffered an

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extensive inguinal cellulitis and she had breast cancer. These severe cases show the invasive

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potential of this organism, especially in immunocompromised patients.

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SSTIs caused by Actinobaculum spp. can be underdiagnosed. Because of its slow growth and

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its similarity to normal bacterial flora on skin and mucosa, A. schaalii is difficult to identify by

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culture and can be considered as a contaminant. Most isolates grew only after at least 48 hours of

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incubation and the organism could easily be missed [9]. It is difficult to establish a microbiology

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laboratory protocol to identify this organism because of the limitations of current phenotypic assays

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and commercially available assays. Actinobaculum spp. should be suspected when non-spore-

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forming, catalase-negative, Gram-positive coccoid rods grow preferentially under anaerobic

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conditions. However, there are difficulties with identifying A. schaalii by using traditional

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phenotypic tests. In addition, commercial systems do not provide reliable identification since they do

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not include Actinobaculum spp. in their data base. Like numerous Actinomyces spp. and related taxa,

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accurate identification can only be performed by 16S rRNA gene sequencing and suspicious isolates

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should be sent to a reference laboratory for identification [8]. All isolates of our review were

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identified using this method. The use of MALDI TOF mass spectrometry could be a powerful

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complement to confirm identification [14]. Actually, no recommendations have been established yet to perform antimicrobial

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susceptibility testing for Actinobaculum spp., but the E-test method seems to be reliable [8, 10, 12].

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A. schaalii is intrinsically susceptible to penicillin, amoxicillin, cefuroxime, ceftriaxone, gentamicin,

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vancomycin, linezolid and tetracycline, and resistant to fluoroquinolones and co-trimoxazole [8, 15,

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16]. In addition, acquired resistance to fluoroquinolones is possible [15] and clindamycin resistance

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is high [17]. This organism seems to be intrinsically resistant to metronidazole and treatment failure

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has been reported with the use of this antibiotic [18]. The recommended treatment for infections

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caused by A. schaalii includes β-lactams such as amoxicillin, cefuroxime or ceftriaxone [2, 15]. The

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optimal duration of antimicrobial treatment is not clearly defined. Our patients were successfully

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treated with cloxacillin. This antibiotic is not commonly used for treating infections caused by

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Actinobaculum spp. We empirically used this antibiotic and we decided not to change treatment

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because both isolates were susceptible in vitro and clinical outcomes were excellent. However,

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surgical drainage is the most important procedure for treating clinical abscesses. Aggressive

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debridement and antimicrobial coverage were necessary in patients with necrotizing cellulitis [9, 10].

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In conclusion, this paper aims to alert clinicians of the implication of Actinobaculum spp. in

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SSTIs. The infection is usually located on the perineal and inguinal regions and can be severe,

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particularly in immunocompromised patients. SSTIs caused by Actinobaculum spp. can be

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overlooked because identification of these organisms is difficult and can be considered as

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contaminants.

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Conflict of interest: the authors declare no conflicts of interests

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REFERENCES

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1. Lawson PA, Falsen E, Akervall E, Vandamme P, Collins MD. Characterization of some

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Actinomyces-like isolates from human clinical specimens: reclassification of Actinomyces suis as

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Actinobaculum suis comb. nov. and description of Actinobaculum schaalii sp. nov. Int J Syst

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Bacteriol 1997;47:899-903.

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2. Cattoir V. Actinobaculum schaalii: review of an emerging uropathogen. J Infect 2012;64:260-7.

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3. Salvadó M, Plasencia V, Segura C, Gómez J, Medina MJ, Sáez-Nieto JA. Infection due to

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Actinobaculum spp.: report of 12 patients in Spain. J Infect 2013;66:107-13.

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4. Bank S, Jensen A, Hansen TM, SoØby KM, Prag J. Actinobacullum schaalii, a common

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uropathogen in elderly patients, Denmark. Emerg Infect Dis 2010;16:76-80.

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5. Drancourt M, Bollet C, Carlioz A, Martelin R, Gayral JP, Raoult D. 16S ribosomal DNA

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sequence analysis of a large collection of environmental and clinical unidentifiable bacteria isolates.

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J Clin Microbiol. 2000;38:3623-30.

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6. Clinical and Laboratory Standards Institute. Performance standards for antimicrobial susceptibility

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testing, 23th informational supplement. M100-S23, vol. 33, no. 1. Clinical and Laboratory Standards

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Institute, Wayne, PA. 2013.

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7. Waghorn DJ. Actinobaculum massiliae: a new cause of superficial skin infection. J Infect

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2004;48:276-7.

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8. Reinhard M, Prag J, Kemp M, Andresen K, Klemmensen B, HØjlyng N, et al. Ten cases of

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Actinobaculum schaalii infection: clinical relevance, bacterial identification, and antibiotic

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susceptibility. J Clin Microbiol 2005;43:5305-8.

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9. Vanden Bempt I, Van Trappen S, Cleenwerck I, De Vos P, Camps K, Celens A, et al.

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Actinobaculum schaalii causing Fournier´s gangrene. J Clin Microbiol 2011;49:2369-71.

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10. Gomez E, Gustafson DR, Rosenblatt JE, Patel R. Actinobaculum bacteremia: a report of 12

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cases. J Clin Microbiol 2011;49:4311-13.

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11. Tschudin-Sutter S, Frei R, Weisser M, Goldenberger D, Widmer AF. Actinobacullum schaalii –

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Invasive pathogen or innocent bystander? A retrospective observational study. BMC Infectious

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Diseases 2011;11:289.

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12. Beguelin C, Genne D, Varca A, Tritten ML, Siegrist HH, Jaton K, et al. Actinobacullum schaalii:

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clinical observation of 20 cases. Clin Microbiol Infect 2011;17:1027-31.

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13. Olsen AB, Andersen PK, Bank S, Søby KM, Lund L, JØrgen P. Actinobacullum schaalii, a

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commensal of the urogenital area. BJU Int 2013;112:394-7.

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14. Farfour E, Leto J, Barritault M, Barberis C, Meyer J, Dauphin B, et al. Evaluation of the

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Andromas matrix-assisted laser desorption ionization-time of flight mass spectometry system for

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identification of aerobically growing Gram-positive bacilli. J Clin Microbiol 2012;50:2702-7.

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15. Cattoir V, Varca A, Greub G, Prod´hom G, Legrand P, Lienhard R. In vitro susceptibility of

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Actinobaculum schaalii to 12 antimicrobial agents and molecular analysis of fluoroquinolone

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resistance. J antimicrob Chemother 2010;65:2514-7.

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16. Nielsen HL, Soby KM, Christensen JJ, Prag J. Actinobaculum schaalii: a common cause of

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urinary tract infection in the elderly population. Bacteriological and clinical characteristics. Scand J

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17. Hays C, Lienhard R, Auzou M, Barraud O, Guérin F, Ploy MC, et al. Erm(X)-mediated

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resistance to macrolides, lincosamides and streptogramins in Actinobaculum schaalii. J Antimicrob

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Table 1. Characteristics of patients with skin and soft-tissue infections due to Actinobaculum spp. Age/sex

Underlying diseases

Clinical presentation

Source of isolate

Microorganism isolated

Method used for identification

Waghorn (2004)

53/F

None

Boil (anterior chest wall)

Aspirate from boil

Actinobaculum massiliae

16S rRNA gene sequence analysis

Reinhard et al (2005)

02/F

Cauda equine syndrome, Syringomyelia

Intradural abscess with fistulation to the skin

ND

Actinobaculum schaalii

16S rRNA gene sequence analysis

Vanden Bempt et al (2011)

33/M

Obesity, smoking, diabetes mellitus

Fournier´s gangrene (groins, scrotum)

Tissue

Actinobaculum schaalii

Gomez et al (2011)

77/M

Prostate cancer, cystoprostatectomy, artificial urethral sphincter

Perineal necrotizing cellulitis

Tissue, blood

Case 1

48/F

Breast cancer, treatment with tamoxifen

Inguinal abscess, cellulitis

Aspirate from abscess

Case 2

25/M

None

Pilonidal abscess

Antibiotic treatment

Surgical treatment

Outcome

No

Metronidazole

No

Cured

Yes (nonhemolytic streptococci)

Penicillin, metronidazole

Surgical drainage

ND

16S rRNA gene sequence analysis

No

Amoxicillin/ clavulanic acid, ciprofloxacin + metronidazole

Surgical debridement

Cured

Actinobaculum schaalii

16S rRNA gene sequence analysis

No

Vancomycin + metronidazole

ND

ND

Actinobaculum schaalii

16S rRNA gene sequence analysis

No

Cloxacillin

No

Cured

Actinobaculum schaalii

16S rRNA gene sequence analysis

No

Cloxacillin

No

Cured

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Note. M: male; F: female; ND: No data. In parenthesis: other organisms isolated; 29 months.

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Aspirate from abscess

Mixed infection1

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Highlights • Actinobaculum spp. should be considered as a cause of skin and soft-tissue infection. • These infections are usually located on the perineal and inguinal regions and can be

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severe, particularly in immunocompromised patients. • Skin and soft-tissue infection caused by Actinobaculum spp. can be overlooked

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because identification is often difficult and they can be considered as contaminants.

Skin and soft-tissue infections caused by Actinobaculum schaalii: report of two cases and literature review.

Skin and soft-tissue infections (SSTIs) caused by Actinobaculum spp. are very rare. In the present study, we report two cases and review the literatur...
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