Journal of Medical Microbiology (2015), 64, 369–374

DOI 10.1099/jmm.0.000038

Bacteriological characteristics of Arcanobacterium haemolyticum isolated from seven patients with skin and soft-tissue infections Hitoshi Miyamoto,1,2 Takashi Suzuki,2,3 Shinobu Murakami,1,2 Mina Fukuoka,1 Yuri Tanaka,1 Takuya Kondo,1 Tatsuya Nishimiya,1 Koichiro Suemori,2,4 Hisamichi Tauchi2,5 and Haruhiko Osawa1 Correspondence

1

Takashi Suzuki

2

[email protected]

Department of Clinical Laboratory, Ehime University Hospital, Toon, Japan Infection Control Team, Ehime University Hospital, Toon, Japan

3

Department of Ophthalmology, Ehime University, Graduate School of Medicine, Toon, Japan

4

Department of Hematology, Clinical Immunology and Infectious Disease, Ehime University Graduate School of Medicine, Toon, Japan.

5

Department of Pediatrics, Ehime University Graduate School of Medicine, Toon, Japan

Received 20 November 2014 Accepted 7 February 2015

Bacteriological examinations were conducted for seven Arcanobacterium haemolyticum strains isolated from elderly patients with skin and soft-tissue infections, such as cellulitis and skin ulcers. Streptococcus dysgalactiae or Gram-positive cocci were isolated together with A. haemolyticum from all patients. The strains were identified as A. haemolyticum based on their being catalase negative, reverse Christie, Atkins and Munch-Petersen (CAMP) positive and phospholipase D gene positive in respective tests. Moreover, API Coryne and matrix-assisted laser desorption/ ionization time-of-flight mass spectrometry confirmed the identification of A. haemolyticum. All strains showed good susceptibility to minocycline, vancomycin and b-lactam antibiotics, but several strains were resistant to gentamicin and levofloxacin.

INTRODUCTION Arcanobacterium haemolyticum is a pleomorphic, nonspore-forming, facultative anaerobic, Gram-positive rod. Originally known as Corynebacterium haemolyticum, it was later removed from the genus Corynebacterium and assigned to the new genus Arcanobacterium (Yassin et al., 2011). It was first described in 1946 and was reported as a causative agent of acute pharyngitis and skin lesions (Maclean et al., 1946), and was considered a pathogen, causing wound infections and pharyngitis (Miller et al., 1986; Karpathios et al., 1992; Mackenzie et al., 1995; Funke et al., 1997; Linder, 1997). In some cases, A. haemolyticum can cause septicaemia, osteomyelitis, brain abscesses and endocarditis (Jobanputra & Swain, 1975; Vargas et al., 2006; Wong et al., 2011; Brown et al., 2013). It is often difficult to identify A. haemolyticum due to its slow growth, similar appearance to Corynebacterium spp. upon Gram Abbreviations: CAM, clarithromycin; CAMP, Christie, Atkins and MunchPetersen; CLDM, clindamycin; CLSI, Clinical and Laboratory Standards Institute; CTRX, ceftriaxone; EM, erythromycin; GM, gentamicin; IPM, imipenem; LVFX, levofloxacin; MALDI-TOF MS, matrix-assisted laser desorption/ionization time-of-flight mass spectrometry; MEPM, meropenem; MINO, minocycline; PCG, benzylpenicillin; TC, tetracycline; VCM, vancomycin.

000038 G 2015 The Authors

Printed in Great Britain

staining and weak haemolytic activity on conventional media (Garcı´a-de-la-Fuente et al., 2008). It is therefore important to assess the bacteriological characteristics and presence of virulence factors, such as phospholipase, to identify A. haemolyticum (Lucas et al., 2010). We previously reported three cases of skin and soft-tissue infections caused by A. haemolyticum (Miyamoto & Nishimiya, 2014). In this study, we report four additional cases from which seven A. haemolyticum isolates were characterized and their antibiotic susceptibilities determined.

METHODS Bacterial strains and patients. Between May 2011 and February

2014, seven A. haemolyticum strains were isolated from skin secretion and pus specimens. All isolates were subcultured and stored at 280 uC for antimicrobial susceptibility testing and molecular characterization. The patient information is shown in Table 1. Four male patients and three female patients were included in the study. The mean patient age (±SD) was 70.71±10.37 years. Three patients presented with cellulitis and four with skin ulcers. Other bacteria isolated together with the A. haemolyticum strains were also identified. Bacterial identification was performed by Gram staining, biochemical testing and matrix-assisted laser desorption/ionization time-of-flight mass spectrometry (MALDI-TOF MS). To identify anaerobic bacteria, 369

370

a RapID ANA II system (Remel) was used. Staphylococcus aureus was considered to be meticillin resistant if its MIC against oxacillin was ¢4 mg ml21. This study was performed in accordance with the tenets of the Declaration of Helsinki.

Streptococcus dysgalactiae, Corynebacterium striatum, Staphylococcus aureus Streptococcus dysgalactiae, Corynebacterium striatum, Peptoniphilus asaccharolyticus Meticillin-resistant Staphylococcus aureus Streptococcus dysgalactiae, Streptococcus agalactiae, Streptococcus anginosus group, Peptostreptococcus anaerobius Streptococcus dysgalactiae, Streptococcus agalactiae, Staphylococcus aureus, Streptococcus anginosus group, Anaerococcus prevotii Corynebacterium striatum, Prevotella disiens, Finegoldia magna

Phenotypic identification. Skin secretions and pus from the sites of

infection were cultured on trypticase agar with 5 % sheep blood (Kyokuto Pharmaceutical) and incubated in a CO2 atmosphere for 48 h. The following tests were performed to identify A. haemolyticum, as described previously (Krech & Hollis, 1991): colony morphology, microscopic appearance, motility, catalase production, DNase production, a Christie, Atkins and Munch-Petersen (CAMP) test and a reverse CAMP test. Catalase production was determined by the addition of a drop of hydrogen peroxide (3 %). The reverse CAMP test for the presence of phospholipase D activity was conducted by streaking a b-haemolytic strain of Staphylococcus aureus (ATCC 25923) onto sheep blood agar plates and then streaking the test strain perpendicular to Staphylococcus aureus. An arrow-shaped zone of enhanced haemolysis was taken as a positive reaction after 24 h incubation at 37 uC in a CO2 atmosphere. An API Coryne (bioMe´rieux) test was performed according to the manufacturer’s instructions (Soto et al., 1994). Identification by MALDI-TOF MS. To identify the isolates, MALDI-

TOF MS was performed on a Bruker MALDI Biotyper (Bruker Daltonics) using the default settings (positive linear mode; laser frequency, 60 Hz; ion source 1 Vage, 20 kV; ion source 2 Vage, 16.7 kV; lens voltage, 7.0 kV; mass range, 2000–20 000 Da), according to the manufacturer’s instructions. Bacteria were applied as a thin film onto a 48-spot steel plate (Bruker Daltonics) and allowed to dry at room temperature. Each spot was overlaid with 1 ml a-cyano-4hydroxycinnamic acid as a matrix and allowed to dry. The target plate was then inserted into the Bruker Microflex LT MALDI-TOF MS system for analysis. The composite profile was analysed using the BiotyperRTC 3.1 software with reference database version 4.0.0.1 (Bruker Daltonics), which queried a reference bank of 2290 spectra and returned the top 10 matches along with confidence scores ranging from 0.0 to 3.0. The identification criteria used in our analysis, as outlined by the manufacturer, were as follows: a score of ¢2000 indicated species level identification, a score of 1700–1999 indicated identification to the genus level and a score of ,1700 was interpreted as not being identified.

Skin secretion F 53 7

Detection of the A. haemolyticum phospholipase D (pld) gene.

F, female; M, male. *Data derived from Miyamoto & Nishimiya (2014).

Pus

Primary hypertension post-surgery for an Achilles tendon rupture Articular rheumatism osteoarthrosis 76 6

M

Calf cellulitis

Skin secretion Pus T2 squamous cell carcinoma in the femur Quadriplegia 71 65 4 5

F M

Femoral ulcer Pressure sore in buttocks Femoral ulcer

Pus Uncontrolled diabetes with gangrene in the foot 70 3*

M

73 2*

M

Foot, former cellulitis Leg ulcer

Skin secretion

Streptococcus dysgalactiae, Corynebacterium striatum Skin secretion

Non-Hodgkin’s malignant lymphoma (diffuse, large cell type, B-cell phenotype) in the neck Brainstem infarction post-treatment for laryngeal cancer Calf cellulitis F 87 1*

Co-morbid condition(s) Clinical diagnosis Sex Age (years) Case

Table 1. Summary of the seven patients with a skin soft-tissue infection

Specimen

Organisms isolated with A. haemolyticum

H. Miyamoto and others

The pld gene was identified by simplex PCR amplification using the following primers, as described previously (Hassan et al., 2009): AhF (59-ATGTACGACGATGAAGACGCG-39) and AhR (59-GCTTCCTTGTCGTTGAGATTATTAGC-39). The expected amplicon size was 528 bp. The PCR programme was as follows: denaturation for 10 min at 95 uC, followed by 30 cycles of 30 s at 95 uC, 1 min at 60 uC and 1 min at 72 uC, and a final step of 7 min at 72 uC. Antimicrobial susceptibility testing. Antimicrobial susceptibility

testing was performed using a broth microdilution assay as described by the Clinical and Laboratory Standards Institute (CLSI, 2009). The MIC was determined using dry plates (Eiken Chemical Co.) with Mueller–Hinton broth (cation adjusted) and StreptoHemo supplement (Eiken Chemical Co.). After 24 h incubation at 37 uC in CO2, an ellipse appeared on the MIC value scale (in mg ml21) at the point at which the concentration of the antibiotic tested inhibited bacterial growth. The antimicrobial agents included benzylpenicillin (PCG), ceftriaxone (CTRX), imipenem (IPM), meropenem (MEPM), gentamicin (GM), clarithromycin (CAM), clindamycin (CLDM), minocycline (MINO), levofloxacin (LVFX) and vancomycin (VCM). All results were interpreted using cut-off values for susceptibility and resistance according to criteria for Corynebacterium set by the CLSI (2010). As there are no established cut-off values for CAM, MINO Journal of Medical Microbiology 64

Bacteriological characteristics of A. haemolyticum and LVFX, the cut-off values for erythromycin (EM), tetracycline (TC) and ciprofloxacin were used for CAM, MINO and LVFX, respectively.

RESULTS Bacterial strains isolated together with A. haemolyticum The bacterial strains isolated with A. haemolyticum are shown in Table 1. Strains other than A. haemolyticum were isolated from all seven patients. Streptococcus dysgalactiae, Corynebacterium striatum and Staphylococcus aureus were detected in five, four and three patients, respectively. Moreover, two strains of Streptococcus agalactiae and Streptococcus anginosus, and five anaerobic bacteria (Peptoniphilus asaccharolyticus, Peptostreptococcus anaerobius, Anaerococcus prevotii, Prevotella disiens and Finegoldia magna) were detected in the samples. However, Gram-negative bacilli were not isolated simultaneously. Phenotypic and MALDI-TOF MS identification of A. haemolyticum The results of the characterization of the seven clinical isolates using API Coryne and other tests are shown in Table 2. All seven isolates presented slightly curved, nonspore-forming, facultative anaerobic, Gram-positive rods, and were catalase and motility negative and required CO2 for growth. All strains were b-haemolytic on trypticase agar with 5 % sheep blood. DNase production by all seven strains was detected. Reverse CAMP tests were positive in all strains. The bacteriological profiles according to the API Coryne system are shown in Table 2. Strains producing the numerical patterns 6530360 (four strains) and 6530361 (three strains) were identified by the API Coryne database as A. haemolyticum, with 99.9 % probability. All strains were identified as A. haemolyticum using the MALDI Biotyper, with high confidence scores of ¢2.0. Detection of pld Identification to the species level of the seven A. haemolyticum strains was confirmed by PCR amplification of the gene pld, which encodes phospholipase D (Table 2). Antimicrobial susceptibility testing The antimicrobial susceptibilities and MICs of the strains for the drugs tested are summarized in Table 3. Two strains were susceptible to all drugs tested. All strains showed susceptibility to MINO, VCM and b-lactam antibiotics such as PCG, CTRX, IPM and MEPM. Two strains showed resistance to GM and LVFX, and one strain showed resistance to CAM and CLDM. http://jmm.sgmjournals.org

DISCUSSION A. haemolyticum can cause wound infections in immunocompromised patients and pharyngitis in young adults and older people (Mackenzie et al., 1995; Linder, 1997; Tan et al., 2006). Less commonly, A. haemolyticum can cause invasive diseases, which are more frequent in older, immunocompromised patients (Ceilley, 1977). In this study, seven A. haemolyticum strains were isolated from skin and soft-tissue infections (cellulitis and skin ulcers). The mean age of our patients was 70.71±10.37 years, and some patients had immunocompromising conditions such as diabetes and carcinoma. However, A. haemolyticum has been detected in young adults and older patients. In this study, A. haemolyticum isolated from skin and soft-tissue infections was most often found together with b-haemolytic streptococci, Staphylococcus aureus or Corynebacterium striatum but not with Gram-negative bacteria. A previous study reported the detection of A. haemolyticum together with group A, C or G b-haemolytic streptococci, Staphylococcus aureus or Corynebacterium diphtheriae (Stacey & Bradlow, 1999). A. haemolyticum could be a co-pathogen in skin and soft-tissue infections, together with Gram-positive cocci and Corynebacterium spp., making its accurate identification critical. A. haemolyticum is often regarded as part of the normal skin flora due to its weak haemolytic activity on sheep blood agar, but it should be distinguished from other organisms, such as Listeria monocytogenes, Streptococcus agalactiae and Corynebacterium spp. A. haemolyticum was identified using catalase and reverse CAMP tests. As phospholipase D produced by A. haemolyticum inhibits b-haemolysin production and reduces haemolysis by Staphylococcus aureus, the absence of haemolysis in the reverse CAMP test enabled the identification of A. haemolyticum. In addition to the reverse CAMP test, the API Coryne test was used to accurately identify A. haemolyticum, as in previous studies (Soto et al., 1994; Hassan et al., 2009; Garcı´a-de-la-Fuente et al., 2012). As in previous reports, MALDI-TOF MS was also useful for the rapid identification of A. haemolyticum (Hijazin et al., 2012; Vila et al., 2012). The identification of A. haemolyticum strains at the species level was confirmed by the PCR amplification of pld, which encodes phospholipase D. Although little is known about the pathogenesis of the skin and soft-tissue infections in the cases in this study, phospholipase D produced by A. haemolyticum could be related to damage to the skin and soft tissues. Lucas et al. (2010) showed that phospholipase D reorganized lipid rafts, resulting in the clustering of adhesion receptors on host cells; thus, it could play a critical role in bacterial adhesion. Furthermore, phospholipase D-expressing A. haemolyticum was able to escape from vacuoles, and phospholipase D caused cellular necrosis. Given that phospholipase D promotes bacterial adhesion and host-cell necrosis following invasion, it could be important in the pathogenesis of A. haemolyticum infections. Moreover, other bacteria, such as Gram-positive cocci, could induce synergistic effects 371

H. Miyamoto and others

Table 2. Bacteriological profiles of the A. haemolyticum strains Strain no.* 1D Nitrate reductiond Pyrazinamidased Pyrrolidonyl arylamidased Alkaline phosphatased b-Glucuronidased b-Galactosidased a-Glucosidased N-Acetyl-b-glucosaminidased Aesculind Ureased Gelatind Glucosed Ribosed Xylosed Mannitold Maltosed Lactosed Sucrosed Glycogend Catalased API CODE Phospholipase D gene b-Haemolysis DNase Motility CAMP test CAMP inhibition test Reverse CAMP test

2 + + + 2 + + + 2 2 2 + + 2 2 + + + 2 2 6530361 + + + 2 2 + +

2D

3D

4

5

6

7

2 + + + 2 + + + 2 2 2 + + 2 2 + + 2 2 2 6530360 + + + 2 2 + +

2 + + + 2 + + + 2 2 2 + + 2 2 + + 2 2 2 6530360 + + + 2 2 + +

2 + + + 2 + + + 2 2 2 + + 2 2 + + + 2 2 6530361 + + + 2 2 + +

2 + + + 2 + + + 2 2 2 + + 2 2 + + + 2 2 6530361 + + + 2 2 + +

2 + + + 2 + + + 2 2 2 + + 2 2 + + 2 2 2 6530360 + + + 2 2 + +

2 + + + 2 + + + 2 2 2 + + 2 2 + + 2 2 2 6530360 + + + 2 2 + +

+, Positive result; 2, negative result. *Strains 1–7 were isolated from cases 1–7, respectively. DData derived from Miyamoto & Nishimiya (2014). dResults from the API Coryne test system.

Table 3. Antibiotic susceptibilities of the A. haemolyticum strains MIC (mg ml”1) and interpretation for strain no.*:

Agent 1D PCG CTRX IPM MEPM GM CAM CLDM MINO LVFX VCM

¡0.06 ¡0.25 ¡0.25 ¡0.25 2 .32 .32 ¡0.25 0.5 0.5

2D and 6 S S S S S R R S S S

¡0.06 ¡0.25 ¡0.25 ¡0.25 2 ¡0.25 ¡0.25 ¡0.25 0.5 0.5

3D S S S S S S S S S S

¡0.06 ¡0.25 ¡0.25 ¡0.25 .32 ¡0.25 ¡0.25 ¡0.25 0.5 0.5

4 S S S S R S S S S S

¡0.06 ¡0.25 ¡0.25 ¡0.25 .32 ¡0.25 ¡0.25 ¡0.25 8 0.5

5 and 7 S S S S R S S S R S

¡0.06 ¡0.25 ¡0.25 ¡0.25 2 ¡0.25 ¡0.25 ¡0.25 8 0.5

S S S S S S S S R S

S, Susceptible; R, resistant, according to CLSI (2010). *Strains 1–7 were isolated from cases 1–7, respectively. DData derived from Miyamoto & Nishimiya (2014). 372

Journal of Medical Microbiology 64

Bacteriological characteristics of A. haemolyticum

with A. haemolyticum and cause severe infections (Enany et al., 2012; Sammra et al., 2014). Further investigation into the relationship between A. haemolyticum and Grampositive cocci during the pathogenesis of A. haemolyticum infections is needed.

Enany, S., Yoshida, Y., Magdeldin, S., Zhang, Y., Bo, X. & Yamamoto, T. (2012). Extensive proteomic profiling of the secretome of European

Antibiotic susceptibility testing of the A. haemolyticum isolates revealed that only two strains were susceptible to all of the antibiotics tested. Other strains showed resistance to at least one antibiotic. Three and two strains had decreased susceptibility to LVFX and GM, respectively. Garcı´a-de-laFuente et al. (2012) investigated the susceptibility of 52 A. haemolyticum isolates from respiratory samples, and all tested strains showed good susceptibility to PCG, cefuroxime, cephalothin, EM, LVFX, VCM, azithromycin and CLDM, whilst 20 strains were resistant to TC. Because fluoroquinolone resistance is dependent on the use of fluoroquinolones, fluoroquinolone-resistant A. haemolyticum could also have been present. The treatment of skin and soft-tissue infections should focus on the elimination of A. haemolyticum and Gram-positive cocci. We demonstrated good susceptibility to MINO, VCM and b-lactam antibiotics such as PCG, CTRX, IPM and MEPM, which could be effective against Gram-positive cocci. Thus, MINO, VCM and b-lactam antibiotics may be useful in the treatment of skin and soft-tissue infections caused by A. haemolyticum. For effective treatment, antibiotics should be selected carefully, taking into account the results of confirmatory susceptibility testing.

Rev 10, 125–159.

In conclusion, seven A. haemolyticum strains isolated from skin and soft-tissue infections, such as cellulitis and skin ulcers, in elderly patients were characterized. A CAMP test, API Coryne and MALDI-TOF MS were used to identify A. haemolyticum. Haemolytic Gram-positive cocci were found together with A. haemolyticum, and several strains showed GM and LVFX resistance. A. haemolyticum skin and softtissue infections should be diagnosed as early as possible and patients should be referred for antimicrobial susceptibility testing.

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and molecular characterization of Arcanobacterium haemolyticum isolated from clinical samples. Diagn Microbiol Infect Dis 72, 1–7. Hassan, A. A., Ulbegi-Mohyla, H., Kanbar, T., Alber, J., La¨mmler, C., Abdulmawjood, A., Zscho¨ck, M. & Weiss, R. (2009). Phenotypic and

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ACKNOWLEDGEMENTS

Arcanobacterium haemolyticum during a 2-year study in Ottawa. Clin Infect Dis 21, 177–181.

The authors declare no conflicts of interest.

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corynebacterium resembling Corynebacterium ovis and Corynebacterium pyogenes in man. J Infect Dis 79, 69–90.

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Journal of Medical Microbiology 64

Bacteriological characteristics of Arcanobacterium haemolyticum isolated from seven patients with skin and soft-tissue infections.

Bacteriological examinations were conducted for seven Arcanobacterium haemolyticum strains isolated from elderly patients with skin and soft-tissue in...
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