Orthopedics

Feature Article 

Clinical Characteristics and Long-term Outcomes After Septic Arthritis of the Native Glenohumeral Joint: A 20-Year Retrospective Review

Matthew C. Sweet, BS; Gabriel J. Sheena, BS; Serena Liu, BS; Felicity E. Fisk, MD; Jonathan R. Lynch, MD; Stephanie J. Muh, MD

Abstract

Septic arthritis of the native glenohumeral joint is rare, and there is little information available regarding the natural progression and long-term joint outcomes of this pathology. The authors performed a retrospective analysis of 97 patients with culture-positive glenohumeral septic arthritis between 1995 and 2015 at their institution with a mean clinical follow-up of 83.1 months. Patient records were reviewed to document demographic and laboratory data, clinical presentation, postoperative complications, recurrences, and subsequent shoulder arthroplasty. Common comorbidities uncovered included 20 immunocompromised patients (20.6%), intravenous drug use among 27 patients (27.8%), diabetes mellitus among 40 patients (41.2%), and 18 patients (18.5%) receiving hemodialysis. Staphylococcus aureus was the most common pathogen identified (61 patients; 62.8%), followed by streptococcal species (17 patients; 17.2%). Hematogenous spread of infection was the most common etiology of shoulder sepsis (40.2%). Seven patients (7.2%) developed shoulder sepsis of undetermined etiology in the absence of established risk factors, and 16 patients (16.4%) developed recurrent glenohumeral septic arthritis at a mean of 40 months following initial eradication of infection. Three patients (3.0%) eventually underwent same-side shoulder arthroplasty at a mean of 18 months following septic arthritis, with none experiencing a periprosthetic joint infection. Glenohumeral septic arthritis is highly unlikely in the absence of medical risk factors. Long-term recurrence after clinically successful treatment is low (16.5%), and few patients undergo elective arthroplasty following shoulder septic arthritis. However, orthopedic surgeons can expect 30% to 40% of patients to require multiple trips to the operating room to successfully treat the initial joint infection, regardless of treatment method. [Orthopedics. 2019; 42(1):e118–e123.]

Abstract

Septic arthritis of the native glenohumeral joint is rare, and there is little information available regarding the natural progression and long-term joint outcomes of this pathology. The authors performed a retrospective analysis of 97 patients with culture-positive glenohumeral septic arthritis between 1995 and 2015 at their institution with a mean clinical follow-up of 83.1 months. Patient records were reviewed to document demographic and laboratory data, clinical presentation, postoperative complications, recurrences, and subsequent shoulder arthroplasty. Common comorbidities uncovered included 20 immunocompromised patients (20.6%), intravenous drug use among 27 patients (27.8%), diabetes mellitus among 40 patients (41.2%), and 18 patients (18.5%) receiving hemodialysis. Staphylococcus aureus was the most common pathogen identified (61 patients; 62.8%), followed by streptococcal species (17 patients; 17.2%). Hematogenous spread of infection was the most common etiology of shoulder sepsis (40.2%). Seven patients (7.2%) developed shoulder sepsis of undetermined etiology in the absence of established risk factors, and 16 patients (16.4%) developed recurrent glenohumeral septic arthritis at a mean of 40 months following initial eradication of infection. Three patients (3.0%) eventually underwent same-side shoulder arthroplasty at a mean of 18 months following septic arthritis, with none experiencing a periprosthetic joint infection. Glenohumeral septic arthritis is highly unlikely in the absence of medical risk factors. Long-term recurrence after clinically successful treatment is low (16.5%), and few patients undergo elective arthroplasty following shoulder septic arthritis. However, orthopedic surgeons can expect 30% to 40% of patients to require multiple trips to the operating room to successfully treat the initial joint infection, regardless of treatment method. [Orthopedics. 2019; 42(1):e118–e123.]

Although septic arthritis of the native glenohumeral joint is an infrequently encountered clinical entity, it can have a serious and potentially fatal outcome.1–5 Whereas native joint septic arthritis most commonly involves the knee and hip as opposed to the shoulder,2,6–8 Jiang et al9 recently reported an annual incidence of approximately 3200 cases of native shoulder septic arthritis in the United States, which accounts for 5% to 12% of all joint infections. Up to half of patients will have permanent, irreversible chondral damage and dysfunction, with worse outcomes noted in patients with rheumatoid arthritis or immunocompromised states.10,11 Risk factors for septic arthritis are well documented and include older age, underlying joint disease, low socioeconomic status, diabetes mellitus, and overlying skin infections.1,12–14 Recent studies have also explored the effects of body mass index,15 vitamin D,16 and hypothyroidism17 as possible risk factors for septic arthritis.

Various studies have compared treatment options for native shoulder septic arthritis, including open arthrotomy with debridement, arthroscopic irrigation and debridement, and serial aspirations.5,11,18 Recent literature has suggested that open arthrotomy is superior to arthroscopy in the treatment of shoulder septic arthritis, leading to lower reinfection rates.19 Post-infectious arthritis can be debilitating for patients. Arthroplasty for postinfectious glenohumeral arthritis has been described in small cohorts as an effective means of treatment.20,21 However, limited data exist assessing long-term outcomes in patients with a history of glenohumeral septic arthritis. The aims of this study were to (1) identify the etiology, patient characteristics, and presentation of glenohumeral septic arthritis and (2) report long-term joint outcomes, complications, and later need for arthroplasty in this population.

Materials and Methods

This study received institutional review board approval. Two hundred forty-eight cases of primary shoulder septic arthritis at a multicenter, academic hospital between 1995 and 2015 were retrospectively identified using the International Classification of Diseases, Ninth Revision, Clinical Modification code for native shoulder septic arthritis (711.01). An extensive, manual chart review was performed to ensure coding accuracy and to verify that all cases met the established diagnostic criteria for septic arthritis used at the authors' institution. One of three criteria had to be met: (1) greater than 50,000 white blood cells and greater than 90% polymorphonuclear neutrophils on joint aspirate; (2) at least 1 positive culture and/or Gram stain on joint aspirate or intraoperative culture; or (3) frankly purulent or cloudy fluid from joint aspirate.

One hundred thirty-seven cases found to be incorrectly coded or misdiagnosed were excluded. Ten patients died within 14 days postoperatively unrelated to surgery. One patient with glenohumeral septic arthritis confirmed by bacterial cultures who refused treatment and left against medical advice was excluded from review. Additionally, 1 patient who had a traumatic knife wound that penetrated the glenohumeral joint capsule, resulting in extensive soft tissue damage, was excluded. Patients younger than 16 years were excluded because the authors sought to evaluate septic arthritis in adults only. Two patients were found to have negative bacterial cultures and were excluded. The final cohort included 97 cases of culture-positive shoulder septic arthritis. All patients included in this study had isolated, native shoulder septic arthritis without any known previous shoulder arthroplasty or infection of the glenohumeral joint.

Patient demographics, comorbidities, laboratory results, and synovial fluid cultures were collected and recorded. All laboratory values were obtained either intraoperatively or at the time of joint aspiration prior to operative intervention. A detailed review of medical records, clinic notes, operative reports, and imaging studies was performed for all patients. The minimum postoperative follow-up was 1 month (mean, 83.1 months; range, 1–264 months).

The primary long-term outcome of interest included recurrence of septic arthritis necessitating secondary reoperation. Recurrence was defined as subsequent intraarticular infection involving the same joint more than 2 months after initial infection, on completion of the recommended antibiotic regimen. Secondary outcomes included the percentage of patients who went on to have shoulder arthroplasty as well as further postoperative complications.

Results

The mean age at infection was 58.2 years, with 58 patients being men (59.8%). Patients reported 2symptoms for a mean of 8.2 days (SD, 6.9 days; range, 1–35 days) prior to presentation. Patients took antibiotics for a mean of 38 days (range, 12–95 days), despite a recommended 6-week antibiotic regimen. The 97 patients had a heavy comorbidity burden, including 40 patients (41.2%) with diabetes mellitus and a mean hemoglobin A1c of 8.1 g/dL (SD, 2.3 g/dL; range, 4.7–13.3 g/dL). Eighteen patients (18.5%) were receiving hemodialysis at the time of diagnosis, 27 (27.8%) had a known history of intravenous drug use, and 26 (26.8%) had a previous diagnosis of chronic hepatitis C virus (Table 1). Additionally, 20 patients (20.6%) were immunocompromised, including all patients who were neutropenic as a result of active malignancy or immunosuppressive therapy (15 patients) as well as patients with human immunodeficiency virus (5 patients). Only 14 patients (14.4%) were considered to have no known risk factors for septic arthritis, with the only comorbidity in this group being hypertension.

Patient Demographics and Comorbidities (N=97)

Table 1:

Patient Demographics and Comorbidities (N=97)

Forty-eight patients (49.5%) were treated with open arthrotomy and debridement, 36 (37.1%) were treated with arthroscopic irrigation and debridement, and 13 (13.4%) underwent serial glenohumeral joint aspirations. A single joint aspiration was performed in all patients prior to receiving arthrotomy or arthroscopy to assess the gross appearance of synovial fluid and for laboratory studies.

Thirty-four patients (35.0%) required 2 or more joint procedures during their hospital admission for persistent clinical symptoms. A greater percentage of patients treated with arthroscopy (14 [38.9%]) required an additional joint washout compared with those who underwent arthrotomy (15 [31.3%]) and those with serial aspirations (5 [38.5%]).

Etiology of Glenohumeral Septic Arthritis

The most common identified etiology of glenohumeral septic arthritis was hematogenous spread from a confirmed primary source of infection (39 patients [40.2%]). Of these 39 cases, 9 (9.2%) had a primary subcutaneous abscess or cellulitis from drug administration, 6 (6.1%) had primary bacterial endocarditis, 6 (6.1%) had a primary catheter-related bloodstream infection (1 peripherally inserted central catheter and 5 dialysis access sites), 4 (4.1%) had a primary infected decubitus or chronic diabetic foot ulcer, and 14 (14.4%) had bacteremia from other sources.

Six patients (6.1%) developed septic arthritis after a documented intra-articular glenohumeral joint injection (5 from corticosteroid injections and 1 from a magnetic resonance imaging arthrogram). Five patients (5.1%) reported developing shoulder pain after a prior fall, without evidence of penetrating injury. One of these patients developed a hematoma that became infected. Four patients (4.1%) developed septic arthritis following previous arthroscopic rotator cuff repair at 3 weeks, 7 weeks, 8 weeks, and 8 months postoperatively. One patient (1.0%) developed postpartum group B Streptococcus sepsis, which was complicated by bilateral psoas abscesses and glenohumeral septic arthritis diagnosed by joint aspiration 8 days postpartum. The source of shoulder infection remained unknown in 42 (43.2%) patients. Of these, 35 had multiple risk factors for septic arthritis and 7 had no identifiable risk factors (hypertension only).

Preoperative Laboratory Results and Cultures

The mean white blood cell count on preoperative glenohumeral aspiration was 121,656 (SD, 93,862; range, 4364–495,042), with a mean differential of 92.6% neutrophils (SD, 6.7%; range, 62%–100%). Significant elevations in serum inflammatory markers were noted, with a mean erythrocyte sedimentation rate of 81.9 mm/h (range, 13–140 mm/h [normal reference range, 0–10 mm/h]) and C-reactive protein of 15.9 mg/dL (range, <0.5–36 mg/dL [normal reference range, <0.5 mg/dL]). The erythrocyte sedimentation rate was found to be elevated in all cases of glenohumeral septic arthritis, and C-reactive protein was elevated in all but 1 patient. The mean preoperative serum white blood cell count was 13.4×109/L (range, 3.9–29.7×109/L [normal reference range, 3.8–10.6×109/L]).

Positive synovial fluid cultures were obtained for all shoulders. Together, staphylococcal and streptococcal species represented more than 80% of all infectious pathogens identified (Table 2). Two shoulders had polymicrobial infections, and the remainder were positive for other various species (Table 2).

Results of Intraoperative Synovial Fluid Cultures in Native Glenohumeral Septic Arthritis (N=97)

Table 2:

Results of Intraoperative Synovial Fluid Cultures in Native Glenohumeral Septic Arthritis (N=97)

Recurrent Septic Arthritis and Postoperative Complications

Sixteen patients (16.4%) developed recurrent septic arthritis at a mean of 40 months (range, 4–96 months) following initial infection. Of the 48 patients originally treated with open arthrotomy, 8 (16.6%) developed recurrent infection. Of the 36 patients originally treated arthroscopically, 8 (22.2%) developed recurrent infection. There were no patients who developed recurrent septic arthritis after treatment with antibiotics and serial glenohumeral joint aspirations alone.

Thirteen patients died within 1 year postoperatively, unrelated to surgery, for a cumulative mortality rate of 13.4%. Two patients reported chronic shoulder pain at 6 months postoperatively. Two patients developed hematomas following open arthrotomy, 1 of whom required a second arthrotomy 23 days later for persistent infection. Additionally, 1 patient developed a hematoma years after the initial infection secondary to hypocoagulation, which successfully resolved. Two patients underwent future arthroscopic rotator cuff repair of the previously affected joint; 1 of these patients developed postoperative septic arthritis. Additionally, 1 patient developed a recalcitrant infection with a chronic draining wound requiring a total of 3 washouts during 9 months.

Glenohumeral Joint Arthroplasty

Three patients (3.0%) eventually underwent same-side shoulder arthroplasty for severe glenohumeral osteoarthritis, including 1 anatomic total shoulder arthroplasty and 2 reverse total shoulder arthroplasties (Figure 1). None of these patients developed a subsequent prosthetic joint infection. The mean time from initial shoulder infection to arthroplasty was 18 months (range, 8–28 months). Two of these patients underwent open arthrotomy and 1 underwent arthroscopic debridement of the original septic shoulder. Two cases of methicillin-sensitive Staphylococcus aureus and 1 case of Escherichia coli were identified. All 3 patients were 60 years or older (mean, 69.0 years) at initial infection. The mean prosthetic survival, determined by most recent documented follow-up, for these 3 patients was 66 months.

Radiologic progression of native glenohumeral septic arthritis in a single shoulder. Six standard anteroposterior views of a single left shoulder are shown. This 60-year-old woman underwent reverse total shoulder arthroplasty 2.3 years following glenohumeral septic arthritis. The prosthetic survival noted for this arthroplasty was 2 years, without complications. Left shoulder 1 month prior to glenohumeral septic arthritis. There is moderate degenerative change of the glenohumeral joint at baseline. There is an osteophyte at the anteroinferior aspect of the humeral head and asymmetric glenohumeral joint space narrowing (A). Left shoulder on day of diagnosis of septic arthritis showing pseudosubluxation of humeral head secondary to joint effusion (B). One week after open arthrotomy with irrigation and debridement of the septic shoulder, with wound staples seen (C). One year after infection showing further radiologic progression of glenohumeral arthritis, now with marked joint space narrowing and increasing size of the osteophyte (D). Left shoulder 2 months after reverse total shoulder arthroplasty. No periprosthetic lucency, fracture, or hardware loosening is seen (E). Thirteen months after reverse total shoulder arthroplasty. There is unchanged and acceptable alignment of the prosthesis without evidence of shaft osteolysis or fracture. There is no bony resorption around the screws of the glenoid component; however, there is inferior resorption of the calcar along the proximal aspect of the humeral component (F).

Figure 1:

Radiologic progression of native glenohumeral septic arthritis in a single shoulder. Six standard anteroposterior views of a single left shoulder are shown. This 60-year-old woman underwent reverse total shoulder arthroplasty 2.3 years following glenohumeral septic arthritis. The prosthetic survival noted for this arthroplasty was 2 years, without complications. Left shoulder 1 month prior to glenohumeral septic arthritis. There is moderate degenerative change of the glenohumeral joint at baseline. There is an osteophyte at the anteroinferior aspect of the humeral head and asymmetric glenohumeral joint space narrowing (A). Left shoulder on day of diagnosis of septic arthritis showing pseudosubluxation of humeral head secondary to joint effusion (B). One week after open arthrotomy with irrigation and debridement of the septic shoulder, with wound staples seen (C). One year after infection showing further radiologic progression of glenohumeral arthritis, now with marked joint space narrowing and increasing size of the osteophyte (D). Left shoulder 2 months after reverse total shoulder arthroplasty. No periprosthetic lucency, fracture, or hardware loosening is seen (E). Thirteen months after reverse total shoulder arthroplasty. There is unchanged and acceptable alignment of the prosthesis without evidence of shaft osteolysis or fracture. There is no bony resorption around the screws of the glenoid component; however, there is inferior resorption of the calcar along the proximal aspect of the humeral component (F).

Discussion

Septic arthritis of the glenohumeral joint is much less common than septic arthritis of the hip and knee joints and is rare in otherwise healthy patients.4 This investigation has provided a contemporary, detailed documentation of the presentation of septic shoulder and long-term outcomes in the largest known cohort of patients with septic arthritis of the native glenohumeral joint. To the authors' knowledge, this is the first study to investigate only cases with positive bacterial cultures and to report the incidence of subsequent shoulder arthroplasty. This information is critical for orthopedic surgeons, as it points to new outcomes in terms of management of glenohumeral septic arthritis. Specifically, most patients may be treated successfully and not develop severe arthritis requiring arthroplasty. Additionally, this study may help guide patient expectations, as orthopedic surgeons can reliably communicate the high likelihood for additional surgical interventions required to eradicate the infection.

In this study, 34 patients (35.0%) required a secondary procedure. This is similar to reoperation rates reported by Abdel et al5 (32%), Böhler et al19 (30.5%), Jeon et al4 (26%), and Memon et al22 (30%). Although the primary purpose of this investigation was not to compare treatment modalities for shoulder septic arthritis, the rates of reinfection for open arthrotomy (16.6%) and arthroscopy (22.2%) compare favorably with previously published outcomes.19 Overall, only 16.5% of patients had recurrence of their infection more than 2 months after initial treatment.

The most commonly identified causative organism in native shoulder septic arthritis was Staphylococcus aureus, followed by streptococcal species. The infectious organism differential of 37.1% methicillin-sensitive Staphylococcus aureus, 25.7% methicillin-resistant Staphylococcus aureus, and 17.2% streptococcal species (Table 2) was comparable to that reported by Jiang et al9: 39%, 21%, and 11%, respectively.

Although there are no specific ranges of laboratory values that can reliably exclude shoulder septic arthritis, elevations in inflammatory markers and white blood cell count, in the appropriate setting, increase clinical suspicion of a septic joint. The preoperative elevations in serum inflammatory markers and synovial fluid cell counts that the authors found compare favorably with ranges reported in other studies and provide an additional reference for clinicians suspecting glenohumeral septic arthritis.5,11,23

Previous research indicates that certain comorbidities, such as intravenous drug use, hemodialysis, hepatitis C, and immunocompromised states, increase the risk of septic arthritis.1,12–14 The authors' research compares favorably with prior literature, indicating the significant comorbidity burden that places this population at a higher risk for infectious arthritis. Interestingly, only 7 patients (7.2%) developed native glenohumeral septic arthritis without known risk factors or causative mechanism for infection.

In this study, few patients (3.0%) went on to have arthroplasty as a means to treat postinfectious arthritis. One viable explanation is that the patients were medically unfit for an elective procedure and at high risk for recurrent infection and postoperative complications. Second, for patients without significant comorbidities, the treating surgeon may have advised strongly against arthroplasty because of concern over subsequent postoperative infection. Finally, a subset of patients go on to function well following treatment of native septic arthritis and do not require further treatment.

There are recent studies suggesting that shoulder arthroplasty is a viable treatment option for native shoulder septic arthritis and may be performed with a low risk of reinfection.20,21 In a case series, Schoch et al20 documented periprosthetic joint infection in 2 of 23 cases following shoulder arthroplasty for postinfectious shoulder arthritis. In the current study, there were no subsequent prosthetic joint infections in the 66-month prosthetic survival period. Although this could be due to the small number of patients who underwent arthroplasty in this study, other studies report prosthetic joint infection rates varying from 0% to 5% in shoulders, hips, and knees24–29 and up to 15.4% in revision shoulder arthroplasties.30

This study had strengths. All included cases underwent extensive medical record review to ensure that each fulfilled strict septic arthritis diagnostic criteria and that there were no instances of prior shoulder infection. Additionally, several cases were incorrectly coded as septic shoulders but were ultimately determined to be inflammatory arthritis. This suggests that incorrect diagnoses may skew data in larger, national studies but were eliminated as a confounding factor in the current analysis.

This study had several limitations. One limitation was its retrospective nature and the potential for any of these patients to receive additional treatment at separate institutions or beyond the noted follow-up period. Additionally, because this study was retrospective, the authors were unable to implement a standard follow-up protocol at predetermined time points, and clinical outcome scores and postoperative range of motion data were not routinely documented for these patients. Due to changes in the electronic medical record system at the authors' institution during the past 20 years, radiographic follow-up was not available for all patients to determine the true incidence of postinfectious glenohumeral arthritis. Finally, there was a possibility that the initial infection was not completely eradicated in cases of recurrent septic arthritis. However, the authors' hospital follows current recommended guidelines using one of the treatment algorithms outlined above depending on the clinical picture for a particular patient. Isolating a single etiology for recurrence of infection for a particular case is difficult as the etiology is likely multi-factorial.

Conclusion

This contemporary study indicated the comorbidities and laboratory values associated with confirmed glenohumeral septic arthritis. The long-term recurrence of shoulder sepsis after clinically successful treatment remained relatively low, with only 16.5% of patients developing recurrent infections. Orthopedic surgeons can expect between 30% and 40% of patients to require multiple trips to the operating room to successfully treat the initial joint infection, regardless of treatment modality. Few patients with a history of shoulder sepsis ultimately undergo shoulder arthroplasty, which may be a viable means for long-term treatment in the correctly selected patient population.

References

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  27. Cochran AR, Ong KL, Lau E, Mont MA, Malkani AL. Risk of reinfection after treatment of infected total knee arthroplasty. J Arthroplasty. 2016;31(suppl 9):156–161. doi:10.1016/j.arth.2016.03.028 [CrossRef]
  28. Koh CK, Zeng I, Ravi S, Zhu M, Vince KG, Young SW. Periprosthetic joint infection is the main cause of failure for modern knee arthroplasty: an analysis of 11,134 knees. Clin Orthop Relat Res. 2017;475(9):2194–2201. doi:10.1007/s11999-017-5396-4 [CrossRef]
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Patient Demographics and Comorbidities (N=97)

CharacteristicValue
Age, mean±SD (range), y58.2±13.7 (27–93)
Sex, No.
  Male58 (59.8%)
  Female39 (40.2%)
Body mass index, mean±SD (range), kg/m229.2±6.6 (17.8–54.7)
Comorbidity
  Hemoglobin A1c, mean±SD (range), g/dL8.1±2.3 (4.7–13.3)
  Hypertension, No.70 (72.1%)
  Diabetes mellitus, No.40 (41.2%)
  Intravenous drug use, No.27 (27.8%)
  Hepatitis C virus, No.26 (26.8%)
  Immunocompromised, No.20 (20.6%)
  End-stage renal disease on hemodialysis, No.18 (18.5%)
  Coronary artery disease, No.16 (16.4%)
  Congestive heart failure, No.14 (14.4%)
  Hypothyroidism, No.10 (10.3%)
  Hepatitis B virus, No.7 (7.2%)
Inflammatory arthritis, No.
  Gout9 (9.2%)
  Calcium pyrophosphate deposition disease3 (3.0%)
  Rheumatoid arthritis3 (3.0%)

Results of Intraoperative Synovial Fluid Cultures in Native Glenohumeral Septic Arthritis (N=97)

Infectious OrganismNo. (%)
Staphylococcus aureus
  MSSA36 (37.1)
  MRSA25 (25.7)
Streptococcus pneumoniae5 (5.1)
Propionibacterium acnes5 (5.1)
Streptococcus agalactiae (group B)5 (5.1)
Pseudomonas aeruginosa5 (5.1)
Enterococcus faecalis4 (4.1)
Streptococcus pyogenes (group A)3 (3.0)
Polymicrobial2 (2.0)
Eikenella corrodens2 (2.0)
Streptococcus intermedius (group F)2 (2.0)
Group C Streptococcus1 (1.0)
Streptococcus viridans1 (1.0)
Escherichia coli1 (1.0)
Authors

The authors are from Wayne State University School of Medicine (MCS, SL) and the Department of Orthopaedic Surgery (GJS, FEF, JRL, SJM), Henry Ford Hospital, Detroit, Michigan.

The authors have no relevant financial relationships to disclose.

Correspondence should be addressed to: Stephanie J. Muh, MD, Department of Orthopaedic Surgery, Henry Ford Hospital, CFP-6, 2799 W Grand Blvd, Detroit, MI 48226 ( Smuh1@hfhs.org).

Received: June 01, 2018
Accepted: August 17, 2018
Posted Online: January 03, 2019

10.3928/01477447-20181227-01

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