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Infectious Disease Reports 2017; volume 9:7185

Native Propionibacterium septic Introduction Correspondence: Thomas Taylor, White River Propionibacterium species are anaer- Junction Veterans Affairs Regional Medical obes associated with normal flora, and Center, 215 N Main St. White River Jct. VT Thomas Taylor,1,2 Marcus Coe,3,4 05009, USA, cultures may be dismissed as contaminants. Ana Mata-Fink,5 Richard Zuckerman1,4 E-mail: [email protected] They are a less virulent but now well recog- 1 Department of Medicine, Geisel nized cause of following Key words: Propionibacterium, septic arthri- Medical School at Dartmouth, Hanover, surgery; and infection of orthopedic hard- tis, , anaerobe infection. NH; 2White River Junction VA Regional ware, vertebral osteomyelitis, endovascular Medical Center, VT; 3Department of devices, and cerebrospinal shunts. The Contributions: the authors contributed equally. , Geisel Medical course is indolent, often without typical Conflict of interest: the authors declare no School at Dartmouth, Hanover, NH; signs or symptoms of infection. Delayed anaerobic growth may contribute to falsely potential conflict of interest. The views 4Dartmouth-Hitchcock Medical Center, negative cultures, late diagnosis, and poor expressed herein do not necessarily represent Lebanon, NH; 5Department of outcomes. Delayed recognition of the views of the Department of Veterans Affairs or the US Orthopedics and Rehabilitation, Yale Propionibacterium follow- Government. Physician’s Building, New Haven, CT, ing shoulder has been well doc- USA 1 umented, but native joint septic arthritis Received for publication: 17 April 2017. may be under recognized, undiagnosed, and Revision received: 15 June 2017. consequently falsely attributed to orthope- Accepted for publication: 24 June 2017. dic surgery. Abstract This work is licensed under a Creative Propionibacterium species are associat- Commons Attribution-NonCommercial 4.0 ed with normal skin flora and cultures may Materials and Methods International License (CC BY-NC 4.0). be dismissed as contaminants. They are We present three cases of only©Copyright T. Taylor et al., 2017 increasingly recognized as a cause of septic Propionibacterium acnes septic arthritis in Licensee PAGEPress, Italy arthritis following shoulder arthroplasty and native , which exemplify chronic and Infectious Disease Reports 2017; 9:7185 . We identified three cases of atypical characteristics. The two septic knee doi:10.4081/idr.2017.7185 Propionibacterium septic arthritis in native joints were falsely considered to representuse joints mimicking atypical osteoarthritis and osteoarthritis. We did a search of the litera- (PVNS), other synovial tumor, and extent of review the literature, clinical course, and ture using PubMed citation septic arthritis treatment of 18 cases. Two cases of osteoarthritis. Synovial biopsies were nega- Propionibacterium for cases, and Clinical tive for PVNS, and cultures again grew P. Propionibacterium acne in native knee Key citation Propionibacterium for case acnes. The diagnosis of septic arthritis was joints and one in a sternoclavicular joint are series. Fifteen cases laid out in Table 1 confirmed by synovial pathology and he described. A literature search for alongside our case numbers 1-3 demon- received 6 weeks of IV ceftriaxone and Propionibacterium septic arthritis was per- strate similar presentations and outcomes with negative cultures. He formed. Clinical course, treatment, and out- (see supplemental references for cases suffered residual painful ambulation and come are reviewed for all cases. Our three reviewed from the literature). cases were combined with 15 cases from post infectious synovitis with recurrent ster- the literature. Fourteen cases showed few ile effusions. He will require future total joint arthroplasty, if cultures remain nega- signs of acute infection, slow culture commercialCase Report #1 growth, and delayed diagnosis. In 3 cases tive and post infectious synovitis subsides. A 56 year-old healthy male with moder- an early culture was dismissed as a contam- ate osteoarthritis of his right knee noted inant. Six cases were reported as caused by swelling and pain in the knee after a night recent arthrocentesis. Fifteen cases were Case Report #2 Non out with friends. Four years prior he had cured with antibiotics, although 5 of these repair of his right knee anterior cruciate lig- A 44 year-old healthy male presented 15 also required surgical intervention. Two ament, without residual hardware or staples. with tricompartment osteoarthritis. In 2001 patients were diagnosed while undergoing He suspected minor trauma superimposed he sustained a patellar rupture that was surgery for osteoarthritis. Four patients on his osteoarthritis and nursed the knee repaired primarily. He subsequently had a required arthroplasty and two of our over 4 months. He presented to Arthritis revision of the repair with xenograft. He patients will require arthroplasty for good Clinic with a large for consid- had persistent knee pain and was treated functional results. Propionibacterium as a eration of steroid injection. Arthrocentesis with hyaluronate derivatives, cortisone cause of septic arthritis in native joints yielded 60cc of mildly inflammatory and injections, and multiple knee . demonstrates few signs of acute infection, bloody . Analysis revealed no He presented to the Orthopedic Surgery presents with prolonged course, and is often crystals, many old RBCs, 2169 cells (30% clinic with a in August 2014 misdiagnosed or unsuspected. Anaerobic neutrophils, 40% macrophages, 30% lym- to pursue knee arthroplasty. At surgery in growth may be delayed or missed altogeth- phocytes). Culture became positive on the December 2014 the synovium was noted to er, and outcomes are consequently poor. 5th day with P. acnes which was considered be discolored with bloody, brown tinged Consider Propionibacterium septic arthritis to be a skin contaminant; given the long synovial fluid and yellow-brown colored in atypical osteoarthritis prior to arthroplas- duration of symptoms, low cell count, and with irregularities, fissuring, and ty. minimal pain. No steroid injections were full-thickness loss. Synovial samples were given, and he was referred for taken and the knee was irrigated and closed to assess for polyvillonodular synovitis without arthroplasty. Intra-operative syn-

[Infectious Disease Reports 2017; 9:7185] [page 87] Case Report

ovial fluid cultures were negative, but syn- ovial tissue culture became positive on the 7th day with P. acnes. He was started on Ceftriaxone and returned to the operating room for a . He completed a 6- week course of Ceftriaxone with cure, but prior poor functional status has not improved.

Case Report #3 A 60 year-old male with medical comorbidities including obesity, alcohol abuse, and cirrhosis developed pain and swelling at the left sternoclavicular joint in September 2014, while working as a mason, without skin break or direct trauma. He was prescribed prednisone and cyclobenzaprine, but a week later developed fever and was admitted to hospital and given a short course of antibiotics for possible pneumo- nia. CXR was suspicious for a lung nodule. CT and PET scan showed a metabolically active lung mass adjacent to the sternoclav- icular joint and manubrium. He left the hos- only pital without complete evaluation. In November 2014 a follow-up CT scan noted improvement in lung findings, but progres- sive erosion of the SC joint. In February use 2015 he returned to the admitting hospital where a CT guided biopsy revealed mild fibrosis and lymphoplasmacytic infiltrate, and culture grew P. acnes from thyoglyco- late broth only. He remained afebrile; CRP was 10.3. Given the chronic course and pos- sibility of skin contamination, a surgical biopsy was performed and confirmed P. acnes osteomyelitis with 3 of 4 positive tis- sue cultures. He was treated with 6 weeks of IV ceftriaxone followed by 3 weeks of PO moxifloxacin, with improvement in pain, commercial swelling, and function.

Results Non Insidious presenting courses occurred in 14 cases, most with predisposing trauma or arthritis, frequently osteoarthritis (OA). Multiple organisms isolated.

There were 4 acute presentations (cases 9, µ 10, 11, 12), all with likely unrecognized insidious courses. Case 9 presented with a OA 6 months None None Ceftriaxone Cure Good Cure Ceftriaxone None None 6 months OA hand abscess, acute Propionibacterium sep- § Burns osteomyelitis years resection None Vancomycin more bone resection Failure epithelioid sarcoma Poor sarcoma epithelioid Failure resection bone more None Vancomycin resection Bone years osteomyelitis Burns Trauma years Bone resection None Clindamycin arthrotomy Cure Poor Cure arthrotomy Clindamycin None resection Bone years Trauma OA 4 months ACL repair None Ceftriaxone arthroscopy Cure Poor Cure arthroscopy Ceftriaxone None repair ACL 4 months OA Hand abscess, sepsis 2 weeks None None Clindamycin Cure Good Cure Clindamycin None None 2 weeks sepsis abscess, Hand µ µ µ µ sis, and likely concomitant seeding of an § septic arthritis in joints. native osteoarthritic knee joint. This case was one of 3 polymicrobial (noted by µ). In the other two polymicrobial cases, multi-

ple organisms were isolated following pro- Initial culture discounted as contaminant; § longed presenting symptoms (cases 7 and 8). Case 10 was diagnosed as acute crystal

proven calcium pyrophosphate wrist arthri- Propionibacterium tis, but progressed slowly over 9 weeks before a synovectomy with multiple cul- dislocations Arthroplasty Arthroplasty cure arthroplasty, dislocations Gentamicin Gentamicin injections ? longer bone necrosis bone ? longer injections Moxifloxacin Moxifloxacin neck abscess abscess neck HLA-B-27+ Rifampicin Rifampicin HLA-B-27+ Girdelston Girdelston Synovectomy Synovectomy Rifampin Rifampin arthroplasty cure 17 46M Elbow Abrasion 5 months None None Amoxicillin Cure Good, arthroplasty Good, Cure Amoxicillin None None 5 months Abrasion Elbow 46M 17 15 17F , acne 17 month None None Amoxicillin Cure erosion Poor erosion Cure Amoxicillin None None month17 acne Arthritis, Shoulder 17F 15 3 60M Sternoclavicular 60M 3 5 65F Hip Trauma 6 months Fracture ORIF Pin failed removed Methicillin Cure Good arthroplasty Good Cure Methicillin removed failed Pin ORIF Fracture 6 months Trauma Hip 65F 5 11 10M Ankle* JIA, many ankle steroid 4 days Synovectomy None Penicillin clindamycin Cure, chronic Poor chronic Cure, clindamycin Penicillin None Synovectomy 4 days steroid ankle many JIA, Ankle* 10M 11 Good Cure Clindamycin None None 4 months RA Knee* 28F 13 9 71M Knee 71M 9 7 71M Elbow 71M 7 Case Age/Sex Site Risk Duration Prior surgery Hardware Treatment Outcome Function Outcome Treatment Hardware surgery Prior Duration Risk Site Case Age/Sex Poor CureKnee 56M Ceftriaxone 1 None repair Patellar ? months OA Bx synovial of culture Knee, 44M 2 stage two Good: Failure Clindamycin None Recurrent chronic OA Shoulder§ 71M 4 Good Cure Penicillin None Noneacne steroid 3 months arthritis, Reactive joint, 27M Sternomanubrial 6 Elbow 50M 8 Poor Cure Penicillin None None 9 weeks day) (1 CPPD Bx synovial Wrist* 42M 10 Good Cure Penicillin None None 3 days RA Knee* 52F 12 Good Cure Pristinamycin None 1 month RA Bx 70FSynovial of culture 14 Knee* stage two Good: spacer, Antibiotic Cefazolin resection bone None, None 6 months lymphoma sepsis; OA, Hip* 78F 16 rx sapho Poor, Failure Azithromycin None None months 14 vulgaris Acne Knee 51M 18 *Arthrocentesis associated; tures grew Propionibacterium. Case 11 had 1. Table

[page 88] [Infectious Disease Reports 2017; 9:7185] Case Report underlying Juvenile Inflammatory Arthritis arthritis, true to the nature of arthroplasty or surgery in a (JIA) and case 12 had underlying Propionibacterium arthritis and misdiag- native joint may be due to (RA). These two short nosed as various chronic arthritidies. Propionibacterium. Shoulder osteoarthritis presentations may have ignored longer All cases were cured of infection, is rare, because are non-weight courses attributed to the underlying inflam- except one complicated by adjacent epithe- bearing joints; this diagnosis particularly matory arthritis. The most common predis- lioid sarcoma (case 8), and one that failed to merits arthrocentesis with anaerobic culture posing condition for Propionibacterium respond but was not recultured (case 18). prior to arthroplasty. septic arthritis was underlying arthritis, and Propionibacterium is susceptible to most Propionibacteria form biofilms and only one patient (case 16) was immuno- antibiotics, with the notable exception of truly septic joints need to be cleared of compromised, with underlying lymphoma. metronidazole.7 All patients received at infection prior to insertion of hardware. Propionibacterium can be difficult to least six weeks of appropriate antibiotics. Cases 4 and 5, where arthroplasties were grow, and when cultures are positive skin Four patients required arthroplasty, and two retained, both failed cure with antibiotics contamination complicates interpretation. of our patients will require arthroplasty to alone. Propionibacterium septic prosthetic In at least three cases an earlier culture was achieve good functional outcome. joints may benefit from two stage revision positive for Propionibacterium and was dis- Outcomes in other patients were often com- arthroplasty (case 4), as debridement with missed as a contaminant (noted by §). plicated or poorly functional. retention or one stage arthroplasty is likely Propionibacterium are common skin flora; Two patients were diagnosed while to fail secondary to biofilms. it is difficult to discern true infection from undergoing surgery for OA. In our case Cultures taken at surgery can be inter- skin contamination. In our 3 cases, cultures number 2, arthroplasty was deferred. In preted as infection or as contamination. took 5 days to 7 days for growth. All cases case number 4, shoulder arthroplasty was Two studies cultured shoulders at multiple grew P. acnes except one which was P. performed, but failed and required subse- sites in the operating room just prior to total avidum. Species known to cause deep infec- quent two stage revision arthroplasty. Case shoulder arthroplasty utilizing anaerobic tion include P. acnes, P. avidum, and P. pro- 5 was also diagnosed from cultures taken thioglycolate broth held for at least 14 days; pionicum. Since many laboratories do not during hip arthroplasty; ORIF of an intra- 41.8% and 56% had at least one culture pos- speciate Propionibacterium, a request for capsular fracture failed with hip subluxa- itiveonly for P. acnes.4,8 Another perioperative speciation might help distinguish coloniza- tion. Cure required removal, culture study grew P. acnes in just 3.1% of tion from true infection. Girdelstone fixation, antibiotics and eventu- patients, but did not use thioglycolate broth Multiple cultures have been required al second stage arthroplasty. Six additional for their anaerobic culture, perioperative when this organism is sought following sep- patients (cases 7, 8, 10, 11, 15, 18) had poor antibiotics were given prior to culture, and tic shoulder arthroplasty.2 Cases 2, 10 and functional outcomes; one patient haduse bone shoulders were not considered infected by 14 grew only from synovial biopsy cultures; necrosis, another had severe joint erosion, histopathology.9 Early septic arthritis fol- synovial fluid cultures were negative. one required arthrotomy with debridement, lowing shoulder arthroplasty occurs in less Several cases were not suspected and dis- one required synovectomy with poor wrist than 1%, so are these culture positive preop- covered at surgery (cases 2, 4, 5, 7). Case 17 function, another required bone resection, erative shoulder joints infected or just colo- is unique in that after a synovial fluid cul- and case 18 failed azithromycin and was nized? The first study treated all culture ture grew P. acnes, a stored frozen synovial treated as SAPHO syndrome. One patient positive joints with one month of oral biopsy specimen from 4 months earlier was (case 6) suffered necrosis of the sterono- antibiotics following arthroplasty. Mook et retrospectively cultured anaerobically and manubrial joint, of little functional conse- al.10 tried to determine the rate of deep also grew P. acnes. This case documents at quence. The patient with acute septic arthri- meticulous culture growth from patients least a four month course of septic arthritis, tis due to hand abscess and sepsis had good undergoing open surgery of the gleno- diagnosed as and eventual- functional outcome of the secondary knee humeral joint. In patients without prior sur- ly treated as SAPHO syndrome (synovitis, commercialinfection. Three patients with RA (cases 12, gery, 18% had at least one positive culture, acne, pustulosis, hyperostosis, and osteitis) 13, 14) underwent relatively early diagnos- 93% of which grew P. acnes. None were with poor outcome. tic arthrocentesis for monoarticular arthritis considered infected, but an accompanying Although arthrocentesis associated sep- and had good outcomes. Propionibacterium editorial reviewed other studies and con- tic arthritis is very rare, 6 cases Nonwere report- arthritis was curable in this series; but grad- cluded the management of painful shoulder ed as possibly caused by recent arthrocente- ual onset, few hallmarks of acute infection, arthroplasty remains highly variable.11 sis (noted by *). These cases do not report and delayed diagnosis often resulted in poor SAPHO syndrome represents a constel- concurrent cultures from incident arthro- function. lation of synovitis, acne, palmo-plantar pus- centesis. Since Propionibacterium are tulosis, hyperostosis, and osteitis. The well- known to colonize normal skin, it is possi- known association with P. acnes is exempli- ble the organism was introduced by injec- Discussion and Conclusions fied by a study confirming 14 of 21 patients tion. Shoulders have been shown to harbor Propionibacteria are anaerobes of low with culture positive needle biopsies of more Propionibacterium seated in anaero- virulence and part of our normal flora; but osteitis lesions, and their response to antibi- bic deep sweat glands and hair follicles than isolates at sterile sites, positive Gram stain, otics.12 Previously considered a form of other anatomic locations,3 accounting for pure growth of Propionibacterium species reactive arthritis, could SAPHO represent septic complication following shoulder acne, and indolent monoarticular arthritis in insidious Propionibacterium infection, or arthroplasty.4 However, joint infection fol- native joints may all indicate true infection. autoimmunity initiated by such infection? lowing arthrocentesis or injection varies Arthrocentesis and culture including anaer- Diagnosis of atypical osteoarthritis syn- between 0.007% and 0.037%.5,6 Given the obic broth should be considered for joints dromes, such as Milwaukee Shoulder, rarity of needle induced septic arthritis, it is with chronic inflammatory arthritis prior to SAPHO syndrome, and Chronic Recurrent more likely the 6 cases thought to be arthro- steroid injection or joint arthroplasty. The Multifocal Osteitis (CRMO)13 should all be centesis associated were actually previously shoulder is heavily colonized with reconsidered in this context. infected cases of insidious onset septic Propionibacerium.3 Infection after joint

[Infectious Disease Reports 2017; 9:7185] [page 89] Case Report

A. Septic arthritis in Iceland 1990- strict specimen collection technique. J References 2002: increasing incidence due to iatro- Shoulder Elbow Surg 2015;24:1206-11. 1. Kanafani ZA, Sexton DJ, Pien BC, et al. genic infections. Ann Rheum Dis 10. Mook WR, Klement MR, Green CL, et Postoperative joint infections due to 2008;67:638-43. al. The incidence of Propionibacterium Propionibacterium species: a case-con- 6. Hollander J. Intrasynovial corticos- acnes in open : a con- teroid therapy in arthritis. MD State trol study. Clin Infect Dis 2009;49: trolled diagnostic study. J Bone Joint Med J 1969;19:62. 1083-5. Surg Am 2015;97:957-63. 7. Roberts SA, Shore KP, Paviour SD, et 2. Dodson CC, Craig EV, Cordasco FA, et 11. Hasan SS, Ricchetti ET. When is a pos- al. Antimicrobial susceptibility of al. Propionibacterium acnes infection itive culture in shoulder surgery not an anaerobic bacteria in New Zealand: infection? J Bone Joint Surg Am 2015; after shoulder arthroplasty: a diagnostic 1999-2003. J Antimicrob Chemother 97:e51. challenge. J Shoulder Elbow Surg 2006;57:992-8. 12. Assmann G, Kueck O, Kirchhoff T, et 2010;19:303-7. 8. Sethi PM, Sabetta JR, Stuek SJ, et al. 3. Patel A, Calfee RP, Plante M, et al. Presence of Propionibacterium acnes in al. Efficacy of antibiotic therapy for Propionibacterium acnes colonization primary shoulder arthroscopy: results of SAPHO syndrome is lost after its dis- of the human shoulder. J Shoulder aspiration and tissue cultures. J continuation: an interventional study. Elbow Surg 2009;18:897-902. Shoulder Elbow Surg 2015;24:796-803. Arthritis Res Ther 2009;11:R140. 4. Levy PY, Fenollar F, Stein A, et al. 9. Maccioni CB, Woodbridge AB, 13. Wipff J, Costantino F, Lemelle I, et al. A Propionibacterium acnes postoperative Balestro JC, et al. Low rate of large national cohort of French patients shoulder arthritis: an emerging clinical Propionibacterium acnes in arthritic with chronic recurrent multifocal entity. Clin Infect Dis 2008;46:1884-6. shoulders undergoing primary total osteitis. Arthritis Rheumatol 2015;67: 5. Geirsson AJ, Statkevicius S, Vikingsson surgery using a 1128-37. only use

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