J Infect Chemother 20 (2014) 650e652
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Case report
A psoas abscess caused by Propionibacterium propionicum Shota Yonetani a, Hiroaki Ohnishi a, *, Koji Araki a, Megumi Hiroi a, Yasushi Takagi a, Shoichi Ichimura b, Takashi Watanabe a a b
Department of Laboratory Medicine, Kyorin University School of Medicine, 6-20-2 Shinkawa, Mitaka-shi, Tokyo 181-8611, Japan Department of Orthopedic Surgery, Kyorin University School of Medicine, 6-20-2 Shinkawa, Mitaka-shi, Tokyo 181-8611, Japan
a r t i c l e i n f o
a b s t r a c t
Article history: Received 2 April 2014 Received in revised form 10 June 2014 Accepted 27 June 2014 Available online 13 August 2014
Pelvic actinomycosis-like disease due to Propionibacterium propionicum has been very rare and only a few cases have been reported in the literature. We herein report a probable first case of a psoas abscess caused by P. propionicum. Since P. propionicum is indistinguishable from Actinomyces israelii by morphological features or routine biochemical tests, 16S rRNA gene sequencing was useful to discriminate these two species in this case. © 2014, Japanese Society of Chemotherapy and The Japanese Association for Infectious Diseases. Published by Elsevier Ltd. All rights reserved.
Keywords: Actinomycosis-like disease Spider-form colonies 16S rRNA
1. Introduction Pelvic actinomycosis-like disease due to Propionibacterium propionicum has been very rare and only a few cases have been reported in the literature [1e3]. We herein report a probable first case of a psoas abscess caused by P. propionicum without any association with surgery or an implantation of foreign bodies.
2. Case report A 61-year-old female presented to the hospital in April 2013 with complaints of pain in her right thigh and right hip that had been present since November 2012. She was admitted to the hospital because of difficulty in walking. Her past medical history was unremarkable, and no foreign bodies, including an intrauterine contraceptive device (IUD), had been implanted. On examination, her axillary temperature was 36.4 C, and swelling in the right iliac site was observed. Hematological investigations revealed a hemoglobin level of 7.9 g/dl, a platelet count of 658 109/l and a white blood cell count of 12.7 109/l. Her C-reactive protein level was 13.5 mg/dl. A computed tomography (CT) scan showed a mass at the right hip indicative of a psoas abscess. Surgeons performed aspiration drainage and placed an indwelling catheter. Antibiotic treatment with imipenem at 0.5g 3/day and amikacin at 600 mg/ * Corresponding author. Tel.: þ81 42 247 5511; fax: þ81 42 279 3471. E-mail address:
[email protected] (H. Ohnishi).
day was started immediately. On the patient's second hospital day, the psoas abscess was incised. A follow-up abdominal CT performed on the 14th day of hospitalization demonstrated the disappearance of the fluid collection. The antimicrobial treatment was changed to oral minocycline at 100 mg/day, which was continued for more than a month, and the patient was discharged on the 42nd day of hospitalization. Gram staining of pus aspirated on admission demonstrated filamentous, beaded Gram-positive rods, compatible with Actinomyces or Nocardia, with many leukocytes (Fig. 1(a)). No other microorganisms were found by Gram staining. Sulfur granules were not found macroscopically or microscopically. Specimens of the abscess taken during the operation were plated onto the following media under appropriate conditions: 5% sheep's blood agar (Eiken Chemical, Tokyo, Japan) incubated at 37 C in air, chocolate agar (Becton Dickinson Japan, Tokyo, Japan) incubated at 37 C in air supplemented with 5% CO2, Brucella HK agar (RS) (Kyokuto Pharmaceutical Industrial, Tokyo, Japan) incubated at 37 C anaerobically and thioglyollate broth (Eiken Chemical, Tokyo, Japan) incubated at 37 C in air. After a 48-h incubation, very small smooth white colonies were evident on the Brucella HK agar (RS) under anaerobic conditions (Fig. 1(b)). Upon Gram staining, the isolate was found to be Gram-positive filamentous rods with possible branching. The cultures were subsequently streaked on brain heart infusion agar (BHIA: Becton Dickinson Japan, Tokyo, Japan) and incubated at 37 C under anaerobic conditions. The development of spider colonies, 0.5 mm in size, was observed microscopically at 200 magnification on the
http://dx.doi.org/10.1016/j.jiac.2014.06.013 1341-321X/© 2014, Japanese Society of Chemotherapy and The Japanese Association for Infectious Diseases. Published by Elsevier Ltd. All rights reserved.
S. Yonetani et al. / J Infect Chemother 20 (2014) 650e652
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Fig. 1. (a) The Gram straining of a psoas abscess specimen (1000 by light microscopy). Filamentous Gram-positive rods with many leukocytes were seen. (b) After 48 h of incubation under anaerobic conditions, very small smooth white colonies were evident on Brucella HK agar (RS). (c) Spider colonies, 0.5 mm in size, appeared on the surface of the BHIA after 24 h of incubation. (200 by light microscopy). (d) The growth of bacteria in the thioglycollate broth after seven days of incubation.
surface of the BHIA after a 24-h incubation (Fig. 1(c)). Bacterial growth was also found in the thioglycolate broth after a one-week period. Typical bread crumb colonies were formed in this medium (Fig. 1(d)). The Gram-positive rods were catalase and oxidase negative. A biochemical evaluation using an API 20A system (SYSMEX bioMerieux, Tokyo, Japan) suggested that the microorganism was P. propionicum/avidum (profile: 47105222) with an identification reliability of 57.9%. Sequencing of the 16S rRNA showed >99% homology with the sequence of P. propionicum registered in Genbank, finally identifying this microorganism to be P. propionicum. Susceptibility testing was performed on Brucella HK agar (RS) using E-tests (SYSMEX bioMerieux). The minimal inhibitory concentrations were determined after 48 h of incubation anaerobically at 37 C. The isolate was susceptible to penicillin, ceftriaxone, imipenem, sulbactam/ampicillin, minocycline, clarithromycin, clindamycin, vancomycin and levofloxacin, but less susceptible to ceftazidime, amikacin and sulfamethoxazole e trimethoprim (Table 1). 3. Discussion P. propionicum is pleomorphic, slow-growing, non-spore-forming, Gram-positive, anaerobic bacteria first described as Actinomyces israelii [4]. The organism was then assigned to the genus Actinomyces as Actinomyces propionicus, and transferred to the genus Arachnia thereafter [5,6]. Further analysis of ribosomal RNA and a fatty acid pattern supported transfer of this species to the genus Propionibacterium [7,8]. Among the genus Propionibacterium, P. propionicum is the most pathogenic species, causing actinomycosis-like disease. These bacteria are normal inhabitants of the human oral cavity and the gastrointestinal tract, and are generally nonpathogenic, but become
pathogenic in patients with implantation of foreign bodies, immunosuppression or after surgery. P. propionicum produces diseases that are clinically indistinguishable from those caused by Actinomyces species. P. propionicum has been isolated in cases of tympanomastoiditis, vertebral osteomyelitis, epidural abscess, lacrimal canaliculitis, brain abscess, pulmonary infection and abdominal actinomycosis-like disease [1e4,9e13]. Pelvic actinomycosis-like disease due to P. propionicum has been very rare and only three cases have been reported in the literature [1e3]. To the best of our knowledge, this case report represents the first finding of P. propionicum in association with a psoas abscess. We consider P. propionicum to be the main pathogen of the psoas abscess in this case, because it was the only isolate that can cause an actinomycosis-like disease. Abdominal Actinomycosis is frequently associated with surgery, trauma or the long-term use of IUDs [14,15]. In the present case, however, no IUD had been implanted, and the patient did not experience surgery or major trauma before the onset of the infection. Absence of these risk
Table 1 The susceptibilities of the isolate to 12 antimicrobial agents. Agent
MIC(mg/ml)
Penicillin Ceftriaxone Ceftazidime Imipenem/cilastatin Sulbactam/ampicillin Amikacin Clarithromycin Clindamycin Minocycline Levofloxacin Sulfamethoxazole/trimethoprim Vancomycin
<0.016 <0.016 4 <0.002 <0.016 32 <0.016 <0.016 0.5 0.25 >32 2
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factors may have suggested the causative agents to be microorganism other than A. israelii in this case. While the precise route of infection remains unclear, the present case indicates that an immunocompetent patient without surgery, trauma or the use of an IUD may also be subject to abdominal infection by P. propionicum. The diagnosis of infection due to P. propionicum remains challenging for routine practice in clinical laboratories. The organism is relatively slow-growing, grows optimally under anaerobic conditions, and may be easily missed if antibiotics are administered. In addition, P. propionicum and A. israelii are difficult to differentiate, because both bacteria are microaerophilic to anaerobic and produce “spider-form” microcolonies [3]. While P. propionicum differs from A. israelii in its growth rate (18 h vs. 7 days for colony formation), it eventually forms molar tooth colonies that are indistinguishable from A. israelii by prolonged incubation. It also gives biochemical reactions that are essentially the same as those of A. israelii and Actinomyces naeslundii. The prominent difference between P. propionicum and Actinomyces spp. is that the former produces propionic acid from the fermentation of glucose, does not require carbon dioxide for either aerobic or anaerobic growth, and the major component of the cell wall of P. propionicum is diaminopimelic acid [12]. However, these features are not evaluable by routine microbial tests currently available in clinical laboratories. Consequently, 16S rRNA gene sequencing is the most reliable method to discriminate these two species in the clinical setting, as experienced in the present case. Since A. israelii has been the best known species for producing “spider-form” colonies, P. propionicum may have been misidentified as A. israelii before genetic analyses became widely available. We consider that 16S rRNA sequencing is essential to correctly identify P. propionicum when spider-form colonies are detected. In addition, once filamentous bacteria are detected by Gram staining, an anaerobic culture should be performed to obtain the best growth of these bacteria. While Actinomycosis requires long-term antimicrobial administration for successful treatment [14], standard treatment for actinomycosis-like disease by microorganism other than A. israelii has yet been established. Studies have demonstrated that Actinomyces species and P. propionicum are commonly susceptible to many antibiotics, including the majority of the b-lactams, clindamycin, vancomycin and fluoroquinolones, but are generally resistant to aminoglycosides and metronidazole [13]. No acquisition of resistance has been recognized after prolonged administration of antibiotics. In the present case, we first used imipenem and amikacin, because nocardiosis could not be ruled out at that time.
Following the identification of P. propionicum as a causative agent, long-term administration of one of the sensitive antibiotics (minocycline) was successful for the treatment. Once infection by P. propionicum or Actinomyces is suspected based on the formation of spider-form colonies by the isolates from the lesion, starting empiric treatment with antibiotics, particularly b-lactams, would be recommended in combination with surgical treatment. After the drug sensitivity of the isolates is verified, long-term treatment with a narrow-spectrum antimicrobial agent should lead to a successful outcome. Conflict of interest None declared. References [1] Brock DW, Georg LK, Brown JM, Hicklin MD. Actinomycosis caused by Arachnia propionica: report of 11 cases. Am J Clin Pathol 1973;59:66e77. [2] Novak A, Brütsch P. Case report of actinomycosis caused by Arachnia propionica. Infection 1980;8:S209e11. [3] Wunderink HF, Lasshley EELO, van Poelgeest MIE, Gaarenstroom KN, Claas ECJ, Kuijper EJ. Pelvic actinomycosis-like disease due to Propionibacterium propionicum after hysteroscopic removal of an intrauterine device. J Clin Microbiol 2011;49:466e8. [4] Pine L, Hardin H. Actinomyces israelii, a cause of lacrimal canaliculitis in man. J Bacteriol 1959;78:164e70. [5] Buchanan L. Characterization of a propionic acid producing actinomycete, Actinomyces propionicus, sp. nov. J Gen Microbiol 1962;28:305e23. [6] Albright L, Toczek S, Brenner VJ, Ommaya AK. Osteomyelitis and epidural abscess caused by Arachnia propionica. Case report. J Neurosurg 1974;40: 115e9. [7] Charfreitag O, Stackebrandt E. Inter- and intrageneric relationships of the genus Propionibacterium as determined by 16S rRNA sequences. J Gen Microbiol 1989;135:2065e70. [8] Cummins CS, Moss CW. Fatty acid composition of Propionibacterium propionicum (Arachnia propionica). Int J Syst Bacteriol 1990;40:307e8. [9] Brazier JS, Hall V. Propionibacterium propionicum and infections of the lacrimal apparatus. Clin Infect Dis 1993;17:892e3. [10] Miglets AW, Branson D. Arachnia propionica (Actinomyces propionicus) as an unusual agent in tympanomastoiditis. Arch Otolaryngol 1983;109:410e2. [11] Riley TV, Ott AK. Brain abscess due to Arachnia propionica. Br Med J 1981;282: 1035. [12] Gerencser MA, Slack JM. Isolation and characterization of Actinomyces propionicus. J Bacteriol 1967;94:109e15. [13] Siqueira JF. Periapical actinomycosis and infection with Propionibacterium propionicum. Endod Top 2003;6:78e95. [14] Vyas JM, Kasmar A, Chang HR, Holden J, Hohmann E. Abdominal abscesses due to actinomycosis after laparoscopic cholecystectomy: case reports and review. Clin Infect Dis 2007;44:e1e4. [15] Filipovic B, Milinic N, Nikolic G, Ranthelovic T. Primary actinomycosis of the anterior abdominal wall: case report and review of the literature. J Gastroenterol Hepatol 2005;20:517e20.