Hemiarthroplasty (HA) and total shoulder arthroplasty (TSA) have been increasingly performed for the treatment of several osteoarticular conditions such as osteoarthritis, humeral head avascular necrosis and proximal humeral fractures following traumas.1,2 Indeed, the annual number of HA and TSA performed in the United States is growing faster, reaching more than 50,000 shoulder replacements per year.3 The incidence of periprosthetic shoulder infections (PSI) appears to be less than that of periprosthetic hip (THA) and knee (TKA) infections, though there have been reports of higher rates in the surgery literature.4,5 Periprosthetic shoulder infections, nonetheless, remain challenging as they increase morbidity as well as raise costs.6 The rate of infectious complication following primary shoulder arthroplasties appears to be as lower as the rates associated with primary hip and knees arthroplasties, while few single-center studies have demonstrated higher rates of PSI.1,4–6

There have been few previous studies analyzing risk factors for PSI.7–9 Patient related-factors and comorbidities such as male gender, younger age, diabetes, morbid obesity, rheumatoid arthritis, and other types of immunosuppression including tumors, have already been implicated.7,10 Surgical-related factors such as peri-operative hematomas and prior surgeries, especially in the trauma setting, increase the incidence of infection after primary shoulder arthroplasty.1,7,11

In addition, the role of biofilm-forming bacteria, such as Propionibacterium acnes, but also Staphylococcus, and Streptococcus in the pathogenesis of orthopedic implant-associated infections, particularly PSI has been widely accepted.12–16 Although uncommonly implicated in PSI, Pseudomonas is an aerobic Gram-negative bacillus expressing the ability to form complex biofilm structures on the surfaces of orthopedic implants.17,18 In one large study addressing Gram-negative prosthetic joint infections, Pseudomonas aeruginosa was by far the most frequently (40%) isolated pathogen.19

We herein sought to identify pre- and intra-operative risk factors predisposing subjects to develop deep infections following HA and TSA, and evaluate causative microorganisms associated with PSI.

There have been few studies describing the epidemiology of periprosthetic joint infection (PJI) after shoulder arthroplasty, including microbial etiology, incidence, and predisposing factors. We aimed to investigate the risks of PJI as well as to understand the underlying microbiological aspects in a cohort of subjects who underwent HA and PSA over 25-year period, 1987–2012. While the rates of PJI following TKA and THA seems to be increasing,10 PSI remains relatively stable according to a large US database survey.6 Interestingly, in our study the rate of PSI reached 12.4% during the first 12-year period of 1987–1999, but dropped to 4.8% in the subsequent 13-year period of 2000–2012, although this difference was not statistically significant. Many reasons may have been associated with the reduction of PSI rate over time, but we argue that an improvement in the pre- and intra-operative management of trauma patients in our urban tertiary teaching center may have played a role.

We sought to identify potential risk factors for PSI, and when examining specifically pre-operative variables, such as demographic data and underlying medical comorbidities, no significant association with PSI was found. Conversely, previous studies have associated younger male patients and PSI, possibly due to local trauma and surgical procedures performed for fractures,6,7 while others studies showed PSI to be significantly associated with chronic diseases, including diabetes and rheumatoid arthritis.1 We identified higher rates of proximal humeral acute fractures as the main reason for shoulder arthroplasty; however, we could not find an association with infection.

Compared to HA, TSA is associated with increased difficulty, increased need for blood transfusions, and longer operative times, though recently published studies show superior outcomes with equivalent postoperative complications, including PSI.1,2,7 In the present study, 6.2% of TSA became infected, even though TSA was not statistically associated with PSI. In contrast, we identified a statistically significant association between PSI and patients presenting ASA grade III or higher, which was confirmed on multivariate analysis. In fact, patients presenting ASA grade three or higher had 4.74-fold higher risk of PSI. To the best of our knowledge, no previous studies have identified significant association of ASA grade particularly with shoulder arthroplasty infection. A retrospective cohort study of patients undergoing TSA or reverse TSA with an ASA score grade III or higher found greater risk of surgical complications, including nerve damage and perioperative fracture, but not higher incidence of surgical site infections.21 Composite risk scores aggregate different factors into one and ASA is a six-point scale frequently applied pre-operatively to assess patient's global health and risks for postoperative complications.22 Furthermore, an elevated ASA grade has been shown to increase the rate of infectious complications after orthopedic surgeries, including PJI following THA and TKA and spinal surgeries.10,22 Additionally, in the current study the presence of hematoma formation soon after shoulder arthroplasty was found to be a potential risk of PSI, showing a 7.10-fold higher risk of PSI on univariate analysis, though it did not reach statistical significance likely secondary to the low incidence of PSI in our study. Cheung et al.23 have previously showed an association of postoperative large hematoma formation requiring reoperation and PJI after primary or revision shoulder arthroplasty, in which hematoma formation after PSA was frequently associated with positive intraoperative cultures.

The presence of hair follicles and sebaceous glands do not increase the adherence of bacteria; this is an inherent property of the bacterium. Rather, they likely harbor bacteria that cannot be adequately sterilized with routine peri-operative sterilization procedures.

Studies have associated PSI with higher frequency of chest bacterial colonization, especially the adherence of anaerobic-aerotolerant Gram-positive bacilli such as P. acnes and other colonizers of human skin like Staphylococcus, Streptococcus, and Pseudomonas spp.12–14 Indeed, an increasingly amount of recent data have demonstrated the predominance of P. acnes in PSI.7,10,12–16 Importantly, our microbiological findings added new information to the epidemiology of PSI as GNB were identified in half of periprosthetic cultures. Notwithstanding, because no P. acnes was recovered from our PSI cases, we have modified the microbiological protocol for the diagnosis of PJI in our Institution. Since 2009 we included sonication technique of the retrieved implants, tissue, and synovial fluid culture incubation on thioglycolate broth for up to 14 days. These findings may reflect the fact that in the majority of our PSI cases presented as early-onset, and local trauma had been the main reason for primary shoulder arthroplasty. Hsieh et al., identified 15% of GNB-PJI after THA and TKA, occurring mainly in the early postoperative period, in which P. aeruginosa was the principal pathogen.19 Reasons for the high frequency of GNB-PSI in our study may include: (1) previous use of broad-spectrum systemic antibiotics such as cephalosporin in trauma patients may have selected more naturally resistant pathogens; (2) since 2011 we started applying sonication culture method for the microbial diagnosis of PJI, thus increasing microbial identification of biofilm-forming sessile pathogens. The presence of S. aureus and S. epidermidis in a quarter of our PSI patients was not surprising, in contrast to the 12.5% detection of Enterococcus faecalis. Much like GNB, enterococci are more commonly associated with early postoperative PJI and as part of polymicrobial infection.10 Since previous studies have associated the P. acnes with PSI,13,24 we have then applied sonication cultures for the microbial diagnosis of different orthopedic implant-associated infections, and prolonged the culture incubation period to 14 days. So far, we have isolated many fastidious and difficult-to-grow bacteria, but not P. acnes.25 Unfortunately, we have been unable to understand why P. acnes shows no growth after plating sonication fluid and tissue samples onto solid culture media and liquid broth under anaerobic condition, and incubating for at least 14 days. Perhaps, its growth may be hampered by the concomitant presence of others pathogens on polymicrobial infections.12 As previously speculated by Singh et al., we also believe that many of the culture-negative results on clinically diagnosed PSI cases would have been caused by P. acnes.7

We are aware that our study has several important limitations, of course due to its retrospective design and a small number of PSI cases (type II error), thus limiting the performance of multivariate analysis to many important associations with PSI such as presence of hematoma and type of fracture. Interpretation by readers of odds ratio calculation using only binominal logistic regression should be made with caution, because it may overestimate the true effect if the variables analyzed are common. The study was carried out in a large urban public teaching center located in a developing country crowded mega-city which offers a specialized orthopedic care for the local population. Studies addressing PSI risk factors among different populations may not reproduce these results, thus the generalizability of our conclusions should be seen with caution. On the other hand, one important strength of our study is that we performed an active surveillance among all subjects submitted to HA and TSA for at least two years after surgery. Another strength was the large number of trauma patients included in the analysis, thus generating a good epidemiological data among this frequent reason for shoulder arthroplasty.

Despite these limitations, our study revealed higher rates of PSI after HA and TSA, estimated at 9.5% over a 25-year period. PSI was mainly associated with an underlying diagnosis of local trauma, and on multivariate analysis, only ASA grade three or higher was associated with increased risk of PSI. Conversely, controlling for individual patient comorbidity, we found no increased association with PSI. Gram-negative bacilli, especially P. aeruginosa was an important cause of infection and P. acnes was neither detected in periprosthetic tissues nor on sonication fluid cultures. Since 2013, PSI rates after shoulder arthroplasty have reduced dramatically in our center, by applying infection control measures especially on trauma patients requiring HA or PSA, which improved the quality of care. Prospective studies including larger number of patients are needed to examine potential risk factor for PSI after HA and TSA.

The authors declare no conflicts of interest.