Diagnosing the presence of Cutibacterium in shoulder arthroplasty: how many cultures need to be taken at revision shoulder arthroplasty?

Cutibacterium (formerly known as Propionibacterium) is the commonest organism causing shoulder periprosthetic infections (PJI). Evaluating failed arthroplasties for PJI is essential for guiding treatment. Diagnosing Cutibacterium PJI requires multiple deep tissue and explant samples, special culturing protocols and prolonged periods of observation. 

The topic of detecting Cutibacterium at revision arthroplasty was addressed by the authors of Origin of propionibacterium in surgical wounds and evidence-based approach for culturing propionibacterium from surgical sites who studied the presence of this organism on the skin and in the surgical wounds of patients who underwent revision arthroplasty for reasons other than clinically obvious infection. Specimens were cultured in broth and on aerobic and anaerobic media.

Propionibacterium grew in twenty-three of thirty cultures of specimens obtained preoperatively from the unprepared epidermis over the area where a skin incision was going to be made for a shoulder arthroplasty; males had a greater average degree of positivity than females. 

Twelve of twenty-one male subjects and zero of twenty female subjects who had cultures of dermal specimens obtained during revision shoulder arthroplasty had positive findings for Propionibacterium. 

Twelve of twenty male subjects and only one of twenty female subjects had positive deep cultures.. 

The positivity of dermal cultures for Propionibacterium was significantly associated with the positivity of deep cultures for this organism.

If Propionibacterium was present in deep tissues, it was likely that it would be recovered by culture if four different deep specimens were obtained and cultured for a minimum of seventeen days on three different media: aerobic, anaerobic, and broth.

Evaluating the presence of Cutibacterium in primary shoulder arthroplasty was explored by the authors of Minimal number of cultures needed to detect Cutibacterium Acnes in primary reverse shoulder arthroplasty. A prospective study

They studied 160 primary RSAs (128 females and 32 males, mean age 74 years), excluding patients with obvious infection or an invasive shoulder procedure in the prior 6 months. 

In 90 cases, 11 cultures were obtained.  10 cultures were obtained in the other 70 cases (culture #10 was a sterile sponge to detect false positives). To determine the minimum number of cultures needed to detect Cutibacterium

Two out of the 70 sterile sponges cultured turned out to be positive for Cutibacterium, giving a false positive rate of 2.8%.

There were 42 patients with positive cultures: 20/32 of the males (69%) and 22/128 of the females (17%).

When considering the the 23% of patients with positive deep tissue cultures, the sensitivity to detect Cutibacterium in relation to the number of specimens is shown in the chart below

Comment: The second study above demonstrates that Cutibacterium can be recovered from a subtantial percentage of patients having primary reverse total shoulder arthroplasty. This study of older predominantly female patients needs to be considered in light of the fact that younger male patients are substantially more likely to have positive deep cultures. 

It is not clear why cultures were obtained in these primary arthroplasties - was there a suspicion of infection?. It is not clear at what point in the procedure the specimens were obtained - the beginning, middle or end. And it not clear whether these patients had ipsilateral shoulder surgery prior to their reverse total shoulder. The post from earlier today (see this link) is of interest in that regard. 

While the number of positive cultures is of relevance, recent evidence indicates that the degree of positivity is of greater importance in interpreting the results of deep cultures for Cutibacterium. The authors of Characterizing the Propionibacterium Load in Revision Shoulder Arthroplasty A Study of 137 Culture-Positive Cases  reported on 137 revision shoulder arthroplasties from which a minimum of 4 specimens had been submitted for culture and at least 1 was positive for Propionibacterium. Standard microbiology procedures were used to assign a semiquantitative value (0.1, 1, 2, 3, or 4), called the Specimen Propi Value, to the amount of growth in each specimen. The sum of the Specimen Propi Values for each shoulder was defined as the Shoulder Propi Score, which was then divided by the total number of specimens to calculate the Average Shoulder Propi Score.

The number and percentage of positive specimen specific cultures of material obtained from the stem explant, head explant, glenoid explant, humeral membrane, collar membrane, other soft tissue, fluid per shoulder ranged from 1 to 6 and 14% to 100%. 

A high percentage of specimens (mean, 43%; median, 50%) from the culture-positive shoulders showed no growth. 

Only 32.6% of the fluid cultures were positive in comparison with 66.5% of the soft-tissue cultures and 55.6% of the cultures of explant specimens. 

The average Specimen Propi Value (and standard deviation) for fluid specimens (0.35 ± 0.89) was significantly lower than those for the soft-tissue (0.92 ± 1.50) and explant (0.66 ± 0.90) specimens (p < 0.001). 

The Shoulder Propi Score was significantly higher in men (3.56 ± 3.74) than in women (1.22 ± 3.11) (p < 0.001). Similarly, men had a significantly higher Average Shoulder Propi Score (0.53 ± 0.51) than women (0.19 ± 0.43) (p < 0.001).

This investigation suggests that Propionibacterium is unevenly distributed within culture-positive revised shoulders. As a result, the number of specimens and their source (explant, soft tissue, or fluid) have major influences on the culture results for a revised shoulder arthroplasty.

We have subsequently learned to identify patients at high risk for positive deep cultures at revision for failed arthroplasty: young male patients with highly positive preoperative cultures of the skin overlying the intended skin incision and having high serum levels of testosterone who develop shoulder pain and stiffness after an initial "honeymoon" period of good comfort and function. In  these patients multiple deep tissue and explant specimens are sent for culture while wound prophylaxis (Betadine lavage, topic antibiotics), prosthesis exchange, and antibiotic treatment are considered for managing a likely infection pending the results of the cultures.

When seeking Cutibcaterium at revision arthroplasty, out current practice is to take 5 deep tissue or explant specimens and culture them on aerobic, anaerobic and broth media for at least 14 days.

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Here are some videos that are of shoulder interest

Shoulder arthritis - what you need to know (see this link).

How to x-ray the shoulder (see this link).

The ream and run procedure (see this link).

The total shoulder arthroplasty (see this link).

The cuff tear arthropathy arthroplasty (see this link).

The reverse total shoulder arthroplasty (see this link).

The smooth and move procedure for irreparable rotator cuff tears (see this link).

Shoulder rehabilitation exercises (see this link).

To diagnose Cutibacterium periprosthetic infection, don't forget to culture explants.

 Culturing Explants for Cutibacterium at Revision Shoulder Arthroplasty: An Analysis of Explant and Tissue Samples at Corresponding Anatomic Sites

Making the diagnosis of a Cutibacterium periprosthetic shoulder infection is difficult because the patient is typically not ill, the peripheral blood typically does not show WBC, C-reactive protein or sedimentation rate evidence of inflammation and because histology on frozen section is often unremarkable (see this link for an example). Thus the diagnosis depends on the results of cultures of multiple deep specimens obtained at revision arthroplasty, submitting these specimens for aerobic, anaerobic and broth cultures and observing the cultures for 2 to 3 weeks.

While submitting deep tissue samples tissue is commonplace, the value of culturing explanted components has not been well-described. Culturing explants may enhance detection of Cutibacterium in revised shoulders because these bacteria tend to become sequestered in biofilms on the surface of prosthetic components and to be less prevalent in samples of tissue or fluid.

This study sought to answer the following questions: 

1) How does the culture positivity of explant cultures compare to that of deep tissue cultures? 

2) How often are explant cultures positive when tissue cultures are not, and vice versa? 

3) How does the bacterial density in explant cultures compare to that in tissue cultures?

The authors reviewed 106 anatomic arthroplasties revised over a 7-year period. 

Explant (humeral head, humeral stem, glenoid) and tissue (collar membrane, humeral canal tissue, periglenoid tissue) specimens were sent for semiquantitative Cutibacterium culture. 

Tissue samples were placed in a stomacher with saline, and the saline was streaked onto three different anaerobic and aerobic media and observed for 21 days. 

Explanted components were vortexed with saline, and the saline was streaked in a similar fashion.

The authors compared culture positivity and bacterial density when cultures of an explant and tissue adjacent to the implant were both available.

They found that explants had positive cultures at a higher rate than the adjacent tissue specimens for most anatomic sites. 

Of the shoulders that had Cutibacterium growth, a higher proportion of explants were culture positive when tissue samples were negative (23-43%) than vice versa (0-21%). 

 

The load of Cutibacterium was higher in explants than in tissues. 

Inclusion of explant samples almost doubled the number of revised shoulders meeting the author's criteria for treatment for Cutibacterium periprosthetic infection. Considering only the results of tissue samples, 16% of the shoulders met this threshold  (≥2 positive cultures); however, with the inclusion of the results for explant cultures an additional 14% of cases –for a total of 30% - met the criteria for infection treatment.

They concluded that in this group of patients, culturing explants in addition to deep tissue samples increased the sensitivity for detecting Cutibacterium in revision shoulder arthroplasty.

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Here are some videos that are of shoulder interest

Shoulder arthritis - what you need to know (see this link).

How to x-ray the shoulder (see this link).

The ream and run procedure (see this link).

The total shoulder arthroplasty (see this link).

The cuff tear arthropathy arthroplasty (see this link).

The reverse total shoulder arthroplasty (see this link).

The smooth and move procedure for irreparable rotator cuff tears (see this link).

Shoulder rehabilitation exercises (see this link).

Understanding the results of cultures for Cutibacterium

What do Positive and Negative Cutibacterium Culture Results in Periprosthetic Shoulder Infection Mean? A Multi-Institutional Control Study

This group of authors from 11 different institutions sought two evaluate the accuracy of cultures for Cutibacterium using positive control (PC) and negative control (NC) samples. Each institution was sent 12 blinded samples (10 PC and 2 NC). The 10 PC samples included 2 sets of 5 different dilutions of a Cutibacterium strain isolated from the humeral canal tissue of a failed total shoulder arthroplasty with a periprosthetic infection with five out five positive cultures for Cutibacterium. This particular isolate was hemolytic with a subtype IB by traditional subtyping and H1 by single locus sequence typing (SLST)

Ten serial dilutions were performed such that the lowest dilution contained approximately 0.1 colony forming units per 100 ul of culture solution. A set of internal control specimens were cultured and sequenced to ensure that there was no contamination during the dilution process.

Five dilutions were selected; the middle of which had a bacterial load that matched that in the original clinical sample, referred to as the 1 dilution. Two dilutions were more concentrated (10 and 100) and two dilutions were less concentrated (0.1 and 0.01) completed the set of five PC samples. 

Negative control (NC) isolates contained sterile saline solution. 

Each culture solution was combined with a 10mm x 10mm piece of gauze to replicate a tissue sample and frozen for transport. At each institution the samples were handled as if they were received from the operating room. The culturing protocols were standardized among the institutions.

100% of specimens at the 4 most concentrated dilutions were positive for Cutibacterium. 

The least concentrated dilution was positive in 91% of samples.

The NC samples grew Cutibacterium in 3 of 22 samples (14%) at two of the 11 institutions. The other 9 institutions detected no growth in the negative control (NC) samples. 

Cutibacterium grew in PC samples at an average of 

4.0 +/- 1.3 days, and all grew within 7 days. 

Time to positivity was significantly shorter (mean 4.0 days) in true positive cultures compared to that for  false positive cultures (8.3 p<0.001)

Strength of culture positivity was recorded as the number of the four quadrants showing growth in a culture plate streaked using the standard method. 

As shown below, the strength of positivity (number of quadrants with growth) was linearly related to the concentration of the dilution.

The 11 different institutions reported highly consistent rates of culture positivity for samples with higher bacterial loads; with lower bacterial loads the results were somewhat less consistent.

False positive cultures were not noted for most of the 11 sites. False positive cultures were characterized by low bacterial loads and longer times to culture positivity (see NC points in the graph above). 

Comment: This study shows that a standardized approach to specimens culturing can lead to reproducible results among institutions. This inter-institution consistency is critical to comparing treatment protocols and clinical outcomes among institutions.

The study shows that the rate of false positive cultures among these institutions is low. 

Even with the most dilute test solution, 91% of the institutions were able to detect Cutibacterium.

In that 

(a) the basic definition of a periprosthetic infection is the demonstration of bacteria doing harm, and 

(b) in that Cutibacterium is the most common bacteria causing periprosthetic infections (often with a stealth presentation), 

a robust and reproducible approach to detecting this bacterium in shoulder wounds is essential for determining diagnosis and treatment.

This approach most include the harvesting of multiple deep tissue and explant specimens for culture and a standardized approach for culturing the specimens as well as for reporting and understanding culture results as described in this article.

You can support cutting edge shoulder research that is leading to better care for patients with shoulder problems, click on this link.

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Here are some videos that are of shoulder interest

Shoulder arthritis - what you need to know (see this link).

How to x-ray the shoulder (see this link).

The ream and run procedure (see this link).

The total shoulder arthroplasty (see this link).

The cuff tear arthropathy arthroplasty (see this link).

The reverse total shoulder arthroplasty (see this link).

The smooth and move procedure for irreparable rotator cuff tears (see this link).

Shoulder rehabilitation exercises (see this link).

Culturing for Cutibacterium at revision surgery

The role of implant sonication in the diagnosis of periprosthetic shoulder infection

These authors spought to investigate the value of implant sonication fluid cultures in the diagnosis of shoulder periprosthetic joint infection (PJI) compared with tissue culture. They conducted a retrospective case-control study analyzing all patients who underwent a revision surgery for any kind of suspected septic or aseptic event due to failed shoulder arthroplasty.

Of the 72 patients, a total of 28 (38.9%) were classified as infected. Of the 28 infected patients, 20 (71.4%) had an identified organism by tissue cultures.


Of all infected patients, 71.4% (20/28 patients) had an identified organism by tissue cultures, and C acnes was the most commonly isolated pathogen, in 13/28 patients (46%), followed by coagulase-negative staphylococci (5/28, 17.9%), Staphylococcus aureus (2/28, 7%), Finegoldia magna (1/28, 3.6%), Streptococcus agalactiae (1/28, 3.6%), Enterococcus faecalis (1/28, 3.6%), and Peptoniphilus asaccharolyticus (1/28, 3.6%).

The sensitivities of sonicate fluid (50 CFU/mL) and periprosthetic tissuebculture for the diagnosis of periprosthetic shoulder infection were 36% and 61% (P . .016), and the specificities were 97.7% and 100%, respectively. If no cutoff value was used in sonication culture, the sensitivity increased to 75% whereas the specificity dropped to 82%. Although there was no significant difference in sensitivity between tissue culture and the no-cutoff sonication fluid culture (61% vs. 75%), the specificity of tissue culture was significantly higher (100% vs. 82%,).

The authors concluded that tissue culture showed a higher sensitivity and specificity than implant sonication in the diagnosis of shoulder PJI and should remain the gold standard for microbiological diagnosis of shoulder PJI.

Comment: It is not a question of either explant or tissue cultures. We have found that both tissue and explant cultures are of importance in the detection of a periprosthetic infection. In their study it is possible that the authors missed the opportunity to recover bacteria in over 25% of their cases because in some cases they only submitted two specimens to the laboratory.

Because Cutibacterium are not evenly dispersed throughout an infected shoulder it is critical that five deep specimens be submitted for culture, in that even if the shoulder is infected, some specimens may show no growth. Recall that titanium alloy provides a surface that is attractive for Cutibacterium biofilm formation; this in some cases the explant cultures are positive while the tissue cultures are negative.

Our routine is to culture synovium, collar membrane, humeral membrane, and all explanted prostheses. Explants are vortexed in 3 cc of saline to remove the biofilm, but sonication has not been shown to be of added value.

Here is a relevant poster from a recent American Shoulder and Elbow Surgeons meeting

Should Explants Be Cultured at Revision Shoulder Arthroplasty?

Background:Surgeons revising a failed arthroplasty need to know whether or not bacteria are present around the implanted components.  The specimen harvesting and culturing practices used to recover bacteria at revision surgery vary among surgeons, some including only tissue and others including both tissue and removed component explants. Culturing explants has the potential benefit of revealing organisms residing in biofilms on their surface that might otherwise be overlooked. The purpose of this study was to assess the added value of culturing explants in seeking evidence of Propionibacteriumat revision arthroplasty. We sought to answer three questions:

1. Does culturing of explants (in addition to tissue cultures) facilitate the recovery of Propionibacteriumfrom revised shoulder arthroplasties?

2. In Propionibacteriumculture-positive shoulders, how does the Propionibacteriumload from explant cultures compare with the load from tissue cultures?

3. In Propionibacteriumculture-positive shoulders, are some anatomic areas more likely to have positive cultures?

Methods:From December 2015 until March 2018, 122 revision arthroplasties were consented for inclusion in a revision shoulder arthroplasty database. Specimens were submitted for standardized Propionibacterium culturing of tissue from the collar membrane, humeral canal, and periglenoid area as well as explants of the humeral head, humeral stem, and glenoid components. In this analysis we included only those shoulders that had both tissue and explant culture results from three anatomically similar locations: 1) HEAD region: collar membrane tissue and humeral head explant (n=86), 2) STEM region: humeral canal tissue and humeral stem explant (n=58), or 3) GLENOID region: periglenoid tissue and glenoid explant (n=45). Tissue samples were placed in a stomacher with saline, and the saline was streaked onto three different anaerobic and aerobic media and observed for 21 days. Explanted components were vortexed with saline, and the saline was streaked in a similar fashion. Semiquantitative culture results were reported for each specimen as the Specimen Propi Value (SpPV). We analyzed the results for two threshold values: SpPV>0 and for SpPV≥1. 

Results:For both thresholds, inclusion of explant cultures increased the percentages of cultures that were positive. 

Importantly, explants were culture positive in shoulders in which the tissue specimens were negative in 6 of 30 (20%) HEAD specimens, 8 of 24 (33%) STEM specimens, and 9 of 19 (47%) GLENOID specimens. The PropionibacteriumSpPVs were similar between positive explant and tissue specimens in the HEAD region (tissue 1.0 ± 0.8 vs. explant 1.5 ± 1.1, p=0.144), STEM region (tissue 1.2 ± 1.0 vs. explant 1.3 ± 1.1, p=0.873), and GLENOID region (tissue 1.0 ± 0.6 vs. explant 0.8 ± 0.8). The percentage of positive tissue or explant specimens were similar between anatomic sites: the HEAD specimens were positive in 30 of 86 (35%) samples, STEM 24 of 58 (41%), and GLENOID 19 of 45 (42%). 

Conclusion:In this study, inclusion of explant cultures increased the percentages of cultures positive for Propionibacteriumat each of three anatomic sites. These findings suggest that the identification of Propionibacterium in revision arthroplasty is more likely if removed implants are submitted for culture. This increase may be due to the detection of bacteria in implant biofilms in cases where it was not detectable in tissue samples.  

And here are some related studies

Performance of implant sonication culture for the diagnosis of periprosthetic shoulder infection

Sonication versus Vortexing of Implants for Diagnosis of Prosthetic Joint Infection

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What is the significance of positive cultures at re-implantation in a two-stage treatment of a prosthetic joint infection?

Positive Culture During Reimplantation Increases the Risk of Subsequent Failure in Two-Stage Exchange Arthroplasty

These authors retrospectively reviewed the data of 259 patients who met the Musculoskeletal Infection Society criteria for periprosthetic joint infection (PJI) and who underwent both stages of 2-stage exchange arthroplasty from 1999 to 2013.

Most spacers contained 3 g of vancomycin and 3 g of tobramycin. At the time of reimplantation, between 3 and 6 samples were obtained for culture.
Among these patients were 267 PJIs (186 knees and 81 hips); 33 (12.4%) had ≥1 positive culture result at re-implantation.

The microorganism isolated at re-implantation was frequently different from that isolated at the time of the initial infection. Furthermore, the organism isolated at the time of subsequent infection was also frequently different from that of the initial infection and the re-implantation.

Treatment failure was defined at a minimum one year follow-up as: (1) failed infection eradication, characterized by a sinus tract, drainage, pain, or infection recurrence caused by the same organism strain; (2) subsequent surgical intervention for infection after reimplantation surgery; or (3) PJI-related mortality.

 The failure rate was
21% for those with negative cultures at re-implantation
50% for those with 1 positive culture at re-implantation and
35% for those with ≥ 2 positive cultures at re-implantation

Comment: This study points out how confusing is the current state of affairs is for diagnosing and managing cases of 'periprosthetic joint infections'.  In this study, when spacers were used at the first stage of a two-stage procedure, cultures were positive at the time of the second stage in over 10% of the cases. The rate of cases meeting a definition of 'failure' was over 20%, even if the cultures were negative at the time of the second stage. Although many authors dismiss a single positive culture as a 'contaminant', one positive culture at the time of re-implantation was associated with the highest rate of failure (50%).  When there was recurrent infection, it was often with different organisms than those cultured at the prior surgery.

It is obvious that we've got a lot to learn. Consistency in culturing practices will do a lot to clarify the situation. We know that the numbers of positive cultures and the types of organisms cultured depend on the number and types of specimens submitted for culture, the media on which they are cultured, and the time these cultures are observed. We also know that recurrence of infection is difficult to define because not infrequently these recurrences are clinically subtle and often become apparent at longer than expected intervals after surgery.

Stay tuned!
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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.

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.

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.

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.

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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