UW Shoulder and Elbow Academy: Propionibacterium and the shoulder

Here is a review of some of the important things we think we know about Propionibacterium and the shoulder.

I. It is now recognized that, rather than being a barrier that keeps bacteria out of the body; the skin is a veritable garden containing viruses, fungi, and bacteria (including Propionibacterium). This microbiome varies in different cutaneous ecosystems. Propionibacterium are particularly prominent in the oily skin of the chest and back (including the areas of incision for shoulder surgery), rather than in the damp axillary area as previously thought. It is possible that the presence of Propionibacterium in the complex healthy microbiome contributes to the resistance of the shoulder to more aggressive organisms, such as Staph Aureus and Streptococcus.

Belkaid, Y. and J. A. Segre (2014). "Dialogue between skin microbiota and immunity." Science 346(6212): 954-959.

Chehoud, C., et al. (2013). "Complement modulates the cutaneous microbiome and inflammatory milieu." Proc Natl Acad Sci U S A 110(37): 15061-15066.

Chen, Y. E. and H. Tsao (2013). "The skin microbiome: current perspectives and future challenges." J Am Acad Dermatol 69(1): 143-155.

Findley, K., et al. (2013). "Topographic diversity of fungal and bacterial communities in human skin." Nature 498(7454): 367-370.

Grice, E. A. (2014). "The skin microbiome: potential for novel diagnostic and therapeutic approaches to cutaneous disease." Semin Cutan Med Surg 33(2): 98-103.

Grice, E. A., et al. (2009). "Topographical and temporal diversity of the human skin microbiome." Science 324(5931): 1190-1192.

Grice, E. A. and J. A. Segre (2011). "The skin microbiome." Nat Rev Microbiol 9(4): 244-253.

Grice, E. A. and J. A. Segre (2012). "The human microbiome: our second genome." Annu Rev Genomics Hum Genet 13: 151-170.

Grice, E. A., et al. (2008). "A diversity profile of the human skin microbiota." Genome Res 18(7): 1043-1050.

Grice, E. A. and J. A. Segre (2012). "Interaction of the microbiome with the innate immune response in chronic wounds." Adv Exp Med Biol 946: 55-68.

Findley, K. and E. A. Grice (2014). "The skin microbiome: a focus on pathogens and their association with skin disease." PLoS Pathog 10(10): e1004436.

Kong, H. H., et al. (2012). "Temporal shifts in the skin microbiome associated with disease flares and treatment in children with atopic dermatitis." Genome Res 22(5): 850-859.

Misic, A. M., et al. (2014). "The Wound Microbiome: Modern Approaches to Examining the Role of Microorganisms in Impaired Chronic Wound Healing." Adv Wound Care (New Rochelle) 3(7): 502-510.

Naik, S., et al. (2012). "Compartmentalized control of skin immunity by resident commensals." Science 337(6098): 1115-1119.

Nakatsuji, T., et al. (2013). "The microbiome extends to subepidermal compartments of normal skin." Nat Commun 4: 1431.

Oh, J., et al. (2014). "Biogeography and individuality shape function in the human skin metagenome." Nature 514(7520): 59-64.

Patel, A., et al. (2009). "Propionibacterium acnes colonization of the human shoulder." J Shoulder Elbow Surg 18(6): 897-902.

SanMiguel, A. and E. A. Grice (2014). "Interactions between host factors and the skin microbiome." Cell Mol Life Sci.

II. Propionibacterium has the ability to form a biofilm on hair follicles, metal and plastic implants and on suture, enabling it to durably resist host defenses and antibiotics and to live in a relatively anaerobic environment from which it can exert its effects on bone resorption (osteolysis) and joint stiffness over months and years.

Achermann, Y., et al. (2014). "Propionibacterium acnes: from commensal to opportunistic biofilm-associated implant pathogen." Clin Microbiol Rev 27(3): 419-440.

Al-Ahmad, A., et al. (2014). "Antibiotic resistance and capacity for biofilm formation of different bacteria isolated from endodontic infections associated with root-filled teeth." J Endod 40(2): 223-230.

Aubin, G. G., et al. (2014). "Propionibacterium acnes, an emerging pathogen: from acne to implant-infections, from phylotype to resistance." Med Mal Infect 44(6): 241-250.

Bayston, R., et al. (2007). "Biofilm formation by Propionibacterium acnes on biomaterials in vitro and in vivo: impact on diagnosis and treatment." J Biomed Mater Res A 81(3): 705-709.

Bayston, R., et al. (2007). "Antibiotics for the eradication of Propionibacterium acnes biofilms in surgical infection." J Antimicrob Chemother 60(6): 1298-1301.

Coenye, T., et al. (2007). "Biofilm formation by Propionibacterium acnes is associated with increased resistance to antimicrobial agents and increased production of putative virulence factors." Res Microbiol 158(4): 386-392.

Furustrand Tafin, U., et al. (2012). "Role of rifampin against Propionibacterium acnes biofilm in vitro and in an experimental foreign-body infection model." Antimicrob Agents Chemother 56(4): 1885-1891.

Jahns, A. C. and O. A. Alexeyev (2014). "Three dimensional distribution of Propionibacterium acnes biofilms in human skin." Exp Dermatol 23(9): 687-689.

Portillo, M. E., et al. (2013). "Propionibacterium acnes: an underestimated pathogen in implant-associated infections." Biomed Res Int 2013: 804391.

Ramage, G., et al. (2003). "Formation of Propionibacterium acnes biofilms on orthopaedic biomaterials and their susceptibility to antimicrobials." Biomaterials 24(19): 3221-3227.

Sampedro, M. F., et al. (2010). "A biofilm approach to detect bacteria on removed spinal implants." Spine (Phila Pa 1976) 35(12): 1218-1224.

Tebruegge, M., et al. (2014). "Invasive Propionibacterium acnes infections in a non-selective patient cohort: clinical manifestations, management and outcome." Eur J Clin Microbiol Infect Dis.

Tunney, M. M., et al. (2007). "Biofilm formation by bacteria isolated from retrieved failed prosthetic hip implants in an in vitro model of hip arthroplasty antibiotic prophylaxis." J Orthop Res 25(1): 2-10.

Tunney, M. M., et al. (1999). "Detection of prosthetic hip infection at revision arthroplasty by immunofluorescence microscopy and PCR amplification of the bacterial 16S rRNA gene." J Clin Microbiol 37(10): 3281-3290.

III. Propionibacterium in surgical wounds may originate from the dermis, which is not sterilized by surgical skin preparation.

Matsen, F. A., 3rd, et al. (2013). "Origin of Propionibacterium in surgical wounds and evidence-based approach for culturing Propionibacterium from surgical sites." J Bone Joint Surg Am 95(23): e1811-1817.

Lee, M. J., et al. (2014). "Propionibacterium persists in the skin despite standard surgical preparation." J Bone Joint Surg Am 96(17): 1447-1450.

IV. Propionibacterium can recovered from shoulders without prior surgery. It is not clear if these organisms are seeded from the overlying dermis or hematogenously from distant sources, such as the mouth.

Bunker, T., et al (2014) “Association between Propionibacterium acnes and frozen shoulder: a pilot study.” Shoulder & Elbow October 2014 vol. 6 no. 4 257-261

Hudek, R., et al. (2014). "Propionibacterium acnes in shoulder surgery: true infection, contamination, or commensal of the deep tissue?" J Shoulder Elbow Surg 23(12): 1763-1771.

Levy, O., et al. (2013). "Propionibacterium acnes: an underestimated etiology in the pathogenesis of osteoarthritis?" J Shoulder Elbow Surg 22(4): 505-511.

Matsen, F. A., 3rd, et al. (2014). "Propionibacterium can be isolated from deep cultures obtained at primary arthroplasty despite intravenous antimicrobial prophylaxis." J Shoulder Elbow Surg. Published Online: December 26, 2014

Schaeverbeke, T., et al. (1998). "Propionibacterium acnes isolated from synovial tissue and fluid in a patient with oligoarthritis associated with acne and pustulosis." Arthritis Rheum 41(10): 1889-1893.

Sethi, P. M., et al. (2014). "Presence of Propionibacterium acnes in primary shoulder arthroscopy: results of aspiration and tissue cultures." J Shoulder Elbow Surg.

V. In the past the presence of Propionibacterium in failed shoulder arthroplasty has probably been overlooked because appropriate number and type of specimens were not taken and because the necessary culturing methods were not used when revision shoulder arthroplasty was performed in cases of prosthetic failure without clinical evidence of infection (such as apparently aseptic loosening of the glenoid).

Butler-Wu, S. M., et al. (2011). "Optimization of periprosthetic culture for diagnosis of Propionibacterium acnes prosthetic joint infection." J Clin Microbiol 49(7): 2490-2495.

Pottinger, P., et al. (2012). "Prognostic factors for bacterial cultures positive for Propionibacterium acnes and other organisms in a large series of revision shoulder arthroplasties performed for stiffness, pain, or loosening." J Bone Joint Surg Am 94(22): 2075-2083.

Schafer, P., et al. (2008). "Prolonged bacterial culture to identify late periprosthetic joint infection: a promising strategy." Clin Infect Dis 47(11): 1403-1409.

Tebruegge, M., et al. (2014). "Invasive Propionibacterium acnes infections in a non-selective patient cohort: clinical manifestations, management and outcome." Eur J Clin Microbiol Infect Dis.

VI. Not all the Propionibacterium recovered from failed arthroplasties are P. Acnes

Butler-Wu, S. M., et al. (2011). "Genome sequence of a novel species, Propionibacterium humerusii." J Bacteriol 193(14): 3678.

VII. Propionibacterium was isolated from failed arthroplasties without clinical evidence of infection as early as 2007. Subsequently there have been many reports of the recovery of Propionibacterium from failed shoulder surgeries. It appears that almost half of failed arthroplasties are culture positive for Propionibacterium. In that the role of Propionibacterium in prosthetic failure remains to be clarified, it is preferable to speak of the culture results, rather than trying to come up with a definition of ‘true infection’. Speaking of the number of positive cultures is not meaningful without indicating the source and number of specimens submitted and how they were cultured. Thus the preferred terminology is ‘failed arthroplasty with 4 out of 5 tissue and explant positive for Propionibacterium-specific cultures’.

Franta, A. K., et al. (2007). "The complex characteristics of 282 unsatisfactory shoulder arthroplasties." J Shoulder Elbow Surg 16(5): 555-562.

Achermann, Y., et al. (2014). "Propionibacterium acnes: from commensal to opportunistic biofilm-associated implant pathogen." Clin Microbiol Rev 27(3): 419-440.

Achermann, Y., et al. (2013). "Characteristics and outcome of 16 periprosthetic shoulder joint infections." Infection 41(3): 613-620.

Achermann, Y., et al. (2010). "Improved diagnosis of periprosthetic joint infection by multiplex PCR of sonication fluid from removed implants." J Clin Microbiol 48(4): 1208-1214.

Athwal, G. S., et al. (2007). "Deep infection after rotator cuff repair." J Shoulder Elbow Surg 16(3): 306-311.

Athwal, G. S., et al. (2007). "Acute deep infection after surgical fixation of proximal humeral fractures." J Shoulder Elbow Surg 16(4): 408-412.

Beekman, P. D., et al. (2010). "One-stage revision for patients with a chronically infected reverse total shoulder replacement." J Bone Joint Surg Br 92(6): 817-822.

Berthelot, P., et al. (2006). "Outbreak of postoperative shoulder arthritis due to Propionibacterium acnes infection in nondebilitated patients." Infect Control Hosp Epidemiol 27(9): 987-990.

Bonnevialle, N., et al. (2010). "Bilateral clavicle fracture external fixation." Orthop Traumatol Surg Res 96(7): 821-824.

Cheung, E. V., et al. (2007). "Reimplantation of a glenoid component following component removal and allogenic bone-grafting." J Bone Joint Surg Am 89(8): 1777-1783.

Cheung, E. V., et al. (2008). "Revision shoulder arthroplasty for glenoid component loosening." J Shoulder Elbow Surg 17(3): 371-375.

Cheung, E. V., et al. (2008). "Infection associated with hematoma formation after shoulder arthroplasty." Clin Orthop Relat Res 466(6): 1363-1367.

Crane, J. K., et al. (2013). "Antimicrobial susceptibility of Propionibacterium acnes isolates from shoulder surgery." Antimicrob Agents Chemother 57(7): 3424-3426.

Dilisio, M. F., et al. (2014). "Arthroscopic tissue culture for the evaluation of periprosthetic shoulder infection." J Bone Joint Surg Am 96(23): 1952-1958.

Dodson, C. C., et al. (2010). "Propionibacterium acnes infection after shoulder arthroplasty: a diagnostic challenge." J Shoulder Elbow Surg 19(2): 303-307.

Erickson, B. J., et al. (2014). "Acute infection with Propionibacterium acnes after a Latarjet coracoid transfer procedure: a case report." Knee Surg Sports Traumatol Arthrosc.

Foruria, A. M., et al. (2013). "Clinical meaning of unexpected positive cultures (UPC) in revision shoulder arthroplasty." J Shoulder Elbow Surg 22(5): 620-627.

Franceschini, V. and C. Chillemi (2013). "Periprosthetic shoulder infection." Open Orthop J 7: 243-249.

Grosso, M. J., et al. (2012). "Reinfection rates after 1-stage revision shoulder arthroplasty for patients with unexpected positive intraoperative cultures." J Shoulder Elbow Surg 21(6): 754-758.

Hattrup, S. J. and K. J. Renfree (2010). "Two-stage shoulder reconstruction for active glenohumeral sepsis." Orthopedics 33(1): 20.

Herrera, M. F., et al. (2002). "Infection after mini-open rotator cuff repair." J Shoulder Elbow Surg 11(6): 605-608.

Horneff, J. G., et al. (2014). "Propionibacterium acnes infections in shoulder surgery." Orthop Clin North Am 45(4): 515-521.

Hou, C. et al “How do revised shoulders that are culture positive for Propionibacterium differ from those that are not?” J Shoulder Elbow Surg 2015.

Ince, A., et al. (2005). "One-stage exchange shoulder arthroplasty for peri-prosthetic infection." J Bone Joint Surg Br 87(6): 814-818.

Kelly, J. D., 2nd and E. R. Hobgood (2009). "Positive culture rate in revision shoulder arthroplasty." Clin Orthop Relat Res 467(9): 2343-2348.

Khassebaf, J., et al. (2014). "Antibiotic susceptibility of Propionibacterium acnes isolated from orthopaedic implant-associated infections." Anaerobe 32C: 57-62.

Kim, S. J. and J. H. Kim (2014). "Unexpected positive cultures including isolation of Propionibacterium acnes in revision shoulder arthroplasty." Chin Med J (Engl) 127(22): 3975-3979.

Klatte, T. O., et al. (2013). "Single-stage revision for peri-prosthetic shoulder infection: outcomes and results." Bone Joint J 95-B(3): 391-395.

Levy, P. Y., et al. (2008). "Propionibacterium acnes postoperative shoulder arthritis: an emerging clinical entity." Clin Infect Dis 46(12): 1884-1886.

McGoldrick, E., et al. (2015). "Substantial cultures of Propionibacterium can be found in apparently aseptic shoulders revised three years or more after the index arthroplasty." J Shoulder Elbow Surg 24(1): 31-35.

Millett, P. J., et al. (2011). "Propionibacterium acnes infection as an occult cause of postoperative shoulder pain: a case series." Clin Orthop Relat Res 469(10): 2824-2830.

Mirzayan, R., et al. (2000). "Management of chronic deep infection following rotator cuff repair." J Bone Joint Surg Am 82-A(8): 1115-1121.

Mook, W. R. and G. E. Garrigues (2014). "Diagnosis and Management of Periprosthetic Shoulder Infections." J Bone Joint Surg Am 96(11): 956-965.

Portillo, M. E., et al. (2013). "Prosthesis failure within 2 years of implantation is highly predictive of infection." Clin Orthop Relat Res 471(11): 3672-3678.

Richards, J., et al. (2014). "Patient and procedure-specific risk factors for deep infection after primary shoulder arthroplasty." Clin Orthop Relat Res 472(9): 2809-2815.

Sabesan, V., et al. (2013). "Clinical and radiographic outcomes of total shoulder arthroplasty with bone graft for osteoarthritis with severe glenoid bone loss." J Bone Joint Surg Am 95(14): 1290-1296.

Saltzman, M. D., et al. (2011). "Infection after shoulder surgery." J Am Acad Orthop Surg 19(4): 208-218.

Singh, J. A., et al. (2012). "Periprosthetic infections after shoulder hemiarthroplasty." J Shoulder Elbow Surg 21(10): 1304-1309.

Singh, J. A., et al. (2012). "Periprosthetic infections after total shoulder arthroplasty: a 33-year perspective." J Shoulder Elbow Surg 21(11): 1534-1541.

Topolski, M. S., et al. (2006). "Revision shoulder arthroplasty with positive intraoperative cultures: the value of preoperative studies and intraoperative histology." J Shoulder Elbow Surg 15(4): 402-406.

Updegrove, G. F., et al. (2014). "Preoperative and intraoperative infection workup in apparently aseptic revision shoulder arthroplasty." J Shoulder Elbow Surg.

Walter, G., et al. (2014). "Bone and joint infections due to anaerobic bacteria: an analysis of 61 cases and review of the literature." Eur J Clin Microbiol Infect Dis 33(8): 1355-1364.

Wang, B., et al. (2013). "A 7-year retrospective review from 2005 to 2011 of Propionibacterium acnes shoulder infections in Ottawa, Ontario, Canada." Diagn Microbiol Infect Dis 75(2): 195-199.

Zeller, V., et al. (2007). "Propionibacterium acnes: an agent of prosthetic joint infection and colonization." J Infect 55(2): 119-124.

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