Orthopedics

Feature Article Supplemental Data

Clinical Characteristics and Outcomes of Staphylococcus lugdunensis Prosthetic Joint Infections: A Multicenter Retrospective Analysis

Komal Masood, MD; Roberta E. Redfern, PhD; Joan M. Duggan, MD, AAHIVS; Gregory M. Georgiadis, MD; Geehan Suleyman, MD

Abstract

Staphylococcus lugdunensis has been increasingly recognized as a cause of serious infections, particularly prosthetic joint infections (PJIs). The aim of this study was to describe the clinical characteristics, treatments, and outcomes of S lugdunensis PJIs. This was a retrospective multicenter study of consecutive adult patients with S lugdunensis PJIs from January 2007 through December 2017; 28 patients met inclusion criteria. The knee was the most commonly affected joint (67.9%), followed by the hip (25%). Clinical and microbiologic characteristics, treatment modalities, and outcomes were evaluated. Thirteen (46.4%) patients had two-stage revision, 9 (32.1%) had debridement with or without revision, 5 (21.4%) had no surgical intervention, and 1 (3.6%) had one-stage revision. Twenty-four (85.7%) patients had monomicrobial infection with S lugdunensis, whereas 4 had polymicrobial. Two patients had concomitant bacteremia. All isolates, except 1, were susceptible to oxacillin. Three patients with no surgical intervention received oral antibiotics, 2 were not treated, and 1 was discharged to hospice. Relapse was observed in 2 of 13 (15%) patients who had two-stage revision, 4 of 9 (44%) who had debridement, and 6 of 6 (100%) who had no surgical intervention or one-stage revision regardless of antibiotic treatment regimen. There was a significant difference in cure rate for patients who underwent two-stage revision compared with other treatment modalities (85% vs 33%, P=.009). Appropriate management of S lugdunensis PJI includes both aggressive surgical treatment and a prolonged course of antibiotics and is associated with excellent clinical response. Regardless of route or duration of antibiotic therapy, relapse is high for patients not treated with two-stage revision. [Orthopedics. 2020;43(6):345–350.]

Abstract

Staphylococcus lugdunensis has been increasingly recognized as a cause of serious infections, particularly prosthetic joint infections (PJIs). The aim of this study was to describe the clinical characteristics, treatments, and outcomes of S lugdunensis PJIs. This was a retrospective multicenter study of consecutive adult patients with S lugdunensis PJIs from January 2007 through December 2017; 28 patients met inclusion criteria. The knee was the most commonly affected joint (67.9%), followed by the hip (25%). Clinical and microbiologic characteristics, treatment modalities, and outcomes were evaluated. Thirteen (46.4%) patients had two-stage revision, 9 (32.1%) had debridement with or without revision, 5 (21.4%) had no surgical intervention, and 1 (3.6%) had one-stage revision. Twenty-four (85.7%) patients had monomicrobial infection with S lugdunensis, whereas 4 had polymicrobial. Two patients had concomitant bacteremia. All isolates, except 1, were susceptible to oxacillin. Three patients with no surgical intervention received oral antibiotics, 2 were not treated, and 1 was discharged to hospice. Relapse was observed in 2 of 13 (15%) patients who had two-stage revision, 4 of 9 (44%) who had debridement, and 6 of 6 (100%) who had no surgical intervention or one-stage revision regardless of antibiotic treatment regimen. There was a significant difference in cure rate for patients who underwent two-stage revision compared with other treatment modalities (85% vs 33%, P=.009). Appropriate management of S lugdunensis PJI includes both aggressive surgical treatment and a prolonged course of antibiotics and is associated with excellent clinical response. Regardless of route or duration of antibiotic therapy, relapse is high for patients not treated with two-stage revision. [Orthopedics. 2020;43(6):345–350.]

Staphylococcus lugdunensis is a coagulase-negative Staphylococcus (CNS) that was first identified in 1988 and is considered part of the normal skin flora, widely distributed in the inguinal and perineal areas.1 Prior to advances in diagnostic laboratory techniques, this organism was often misdiagnosed as S aureus.2,3 Unlike S aureus, S lugdunensis is generally widely susceptible to methicillin and oxacillin and other antimicrobial agents, including daptomycin, rifampin, clindamycin, vancomycin, and linezolid; however, some strains have shown resistance to common antistaphylococcal agents.4,5

Furthemore, S lugdunensis is a unique CNS in that it closely resembles S aureus in pathogenicity with the propensity to cause severe infection with multiple relapses. It has emerged as a major human pathogen capable of causing significant infections at many sites, including prosthetic joints.6 Other serious infections include bacteremia, endocarditis, diskitis/osteomyelitis, and abscesses of virtually every organ. Several factors add to its pathogenicity, including its ability to promote tissue interaction by binding proteins located within the host tissue, causing easy attachment to synthetic surfaces. It is also lysozyme resistant, which prevents activation of the immune system.7 Finally, S lugdunensis produces biofilm similar to other CNS, which contributes to its predilection for prosthetic joint infections (PJIs). This biofilm protects the organism from the immune system while allowing it to grow and thrive, especially on the prosthetic joint material.8 This often leads to difficulty in achieving cure without surgical debridement and antimicrobial treatment.2

Joint replacement is a common procedure performed in the United States. In 2010, approximately 332,000 total hip and 719,000 total knee arthroplasties were performed, and these numbers are projected to increase to 850,000 and 1,921,000, respectively, by 2030.9,10 Between 1% and 3% of patients who undergo knee or hip joint replacement surgery encounter an infection,1 and these values are expected to increase to 6.8% and 6.5%, respectively, by 2030.11 Given the expected increase in the number of joint replacements and PJIs during the next decade, the economic impact of this complication is significant and appropriate management is crucial. However, S lugdunensis is not a commonly reported causative organism in PJIs.1 This retrospective analysis was undertaken to examine the clinical characteristics and outcomes of S lugdunensis PJIs based on different treatment modalities, including surgical techniques and antimicrobial therapy, and to provide guidance to support clinicians in making appropriate decisions regarding the management of this potentially devastating complication.

Materials and Methods

This was an observational retrospective multicenter study involving consecutive adult patients from 9 hospitals throughout Northwest Ohio and Southeast Michigan with laboratory evidence of S lugdunensis infection. Patients were identified by query of the hospitals' electronic laboratory database for infections occurring from January 1, 2007, through December 31, 2017. Research staff performed a manual review of medical records of patients identified with a culture positive for S lugdunensis. Patients 18 years or older with previous joint replacement and those with infected fracture fixation devices were eligible for inclusion. Definitions used during chart review and for data analysis are listed in Table 1. These are consistent with the definition of PJI from the Musculoskeletal Infection Society.12

Definitions of Staphylococcus lugdunensis Prosthetic Joint Infection, Treatment Success, and Treatment Failure

Table 1:

Definitions of Staphylococcus lugdunensis Prosthetic Joint Infection, Treatment Success, and Treatment Failure

Variables of interest included baseline and demographic characteristics, including age, sex, and comorbidities. Clinical information, including date and site of original procedure, clinical signs and symptoms, blood and joint cultures, and medical and surgical interventions, was collected. Outcomes, including relapse, cure, and death, were noted with last known date of contact to determine the length of follow-up. Institutional review board approval was obtained prior to data collection; written informed consent was waived due to the retrospective nature of the study.

Statistical Analysis

Descriptive statistics were used to describe demographic and baseline patient characteristics. Median with range was reported for continuous variables, which were compared using the Mann– Whitney U test, while categorical variables were analyzed using Fisher's exact test. Post hoc analysis of event-free survival was examined using the Kaplan– Meier method; log rank test was used to compare the outcomes of patients as a function of treatment with or without surgical intervention. Event-free survival was calculated from the end of definitive treatment to relapse. Two-tailed P<.05 was considered statistically significant. All analyses were performed using statistical software R, version 3.5.1 (The R Foundation for Statistical Computing, Vienna, Austria) and SPSS Statistics for Windows, version 25.0 (IBM, Armonk, New York).

Results

A total of 695 consecutive adult patients with S lugdunensis infection were initially screened for inclusion in the study. Of these, 28 (4.0%) patients were found to have PJIs caused by S lugdunensis and were included in the analysis. Demographics, comorbid conditions, and clinical characteristics of the patients are presented in Table 2. The majority of identified prostheses were implanted during elective knee or hip joint replacement; these were primary knee and hip replacement surgeries. Three prostheses (10.7%) were implanted as a result of trauma or injury: 1 femoral neck fracture, 1 tibial pilon fracture, and 1 rotator cuff tear.

Baseline Clinical Characteristics of Patients With Staphylococcus lugdunensis Prosthetic Joint InfectionBaseline Clinical Characteristics of Patients With Staphylococcus lugdunensis Prosthetic Joint Infection

Table 2:

Baseline Clinical Characteristics of Patients With Staphylococcus lugdunensis Prosthetic Joint Infection

All patients were white. Fifteen (53.6%) patients were female, and the median age was 68.5 years. The most common presentations were pain (27 of 28 patients), reduced movement (27 of 28 patients), and swelling of the joint (20 of 28 patients). Two patients were found to have associated S lugdunensis bacteremia, 1 of whom had a concomitant pacemaker lead endocarditis. The knee (n=19) was the most commonly involved joint, followed by the hip (n=7). Median duration between initial joint replacement and index PJI was 1043 days (range, 12–5459 days), representing late PJI (>10 weeks postoperatively as previously defined)13 in 96.4% of this cohort; 9 (32%) patients developed PJI within 2 years of the procedure, and 16 (57%) patients developed infection 5 years after surgery.

One patient was discharged from the hospital to hospice without antibiotic treatment and was excluded from the outcome analysis. Two other patients died 5 months and 9 years after initial infection; however, the deaths appeared to be unrelated to infection.

Most patients (24 of 28) had monomicrobial infection with S lugdunensis (Table 2). Four patients had infection with additional microorganisms, including 2 with other CNS (S capitis and S haemolyticus), 1 with Enterococcus faecalis (susceptible to ampicillin and vancomycin), and 1 with multiple organisms, including Pseudomonas aeruginosa, methicillin-resistant S aureus, and Escherichia coli in addition to S lugdunensis.

Treatment Data

Surgical Management. Twenty-three (82.1%) patients underwent surgical intervention for their PJIs. Thirteen (46.4%) underwent a two-stage revision, 9 (32.1%) had debridement with or without polyethylene exchange, and 1 (3.6%) had one-stage revision. Overall, 14 patients had removal of infected hardware as part of initial surgery and 13 patients received an antibiotic cement spacer (containing vancomycin and tobramycin). Conversely, 5 (17.9%) patients had no surgical intervention (Table A, available in the online version of the article).

Comparison of clinical characteristics and intervention of patients with Staphylococcus lugdunensis prosthetic joint infection (PJI) who relapsed compared to those who did not

Table A:

Comparison of clinical characteristics and intervention of patients with Staphylococcus lugdunensis prosthetic joint infection (PJI) who relapsed compared to those who did not

Antimicrobial Therapy. Antimicrobial treatment course and duration varied. The majority of patients (25 of 28) received intravenous (IV) antibiotics on admission. Of the 25 patients who received IV antibiotics during their hospitalization, 22 (88.0%) were discharged with IV therapy, 1 (4.0%) with oral treatment, and 2 (8.0%) without antibiotics (Table A). Oral antibiotics were continued for 2 patients after discharge and discontinued for 1 patient. One patient was discharged to hospice without treatment and not included in the outcome analysis.

All of the 13 (100%) patients who underwent two-stage revision received at least 6 weeks of IV antibiotics. Four (31%) received suppressive therapy with doxycycline (75%) and amoxicillin and clavulanic acid (25%). Eight (89%) of 9 patients who had debridement were discharged with IV antibiotics, 6 (75%) of whom received at least 6 weeks of treatment, followed by suppressive therapy for 5 (83%) patients. One was discharged without therapy. The patient with one-stage revision received 4 weeks of IV therapy, followed by suppressive doxycycline. Of the 5 (18%) patients who had no surgical intervention, only 3 were discharged with therapy. One patient received a 6-week course of oral cephalexin, and the other 2 patients received an unknown duration of oral cephalexin and linezolid.

The most commonly prescribed IV antibiotics at discharge included beta-lactams (n=15) and vancomycin (n=8). Of the beta-lactams, cefazolin (n=7) and ceftriaxone (n=3) were more frequently used. Twenty-one (95%) of 22 patients received more than 4 weeks of IV antibiotics, and 2 (67%) of 3 patients received less than 4 weeks of oral therapy. Most patients tolerated antibiotics well, except for 2 patients; 1 was switched from IV vancomycin to IV daptomycin due to acute kidney injury. Another patient developed daptomycin-induced eosinophilic pneumonia and was switched to IV vancomycin for completion of therapy.

Treatment Outcomes

Of the 28 patients, only 16 (57%) achieved clinical cure, as defined in Table 1. Eleven (69%) of these had a two-stage revision and 5 (31%) had debridement with or without polyethylene liner exchange. Overall, there was a statistically significant difference in cure rates based on type of surgical intervention (Table A; P=.003) as well as for those who underwent two-stage revision compared with other treatment modalities (85% vs 33%, P=.009). Relapse was observed in 2 of 13 (15%) patients who had two-stage revision compared with 4 of 9 (44%) who had debridement with or without polyethylene liner exchange and 6 of 6 (100%) who had no surgical intervention or one-stage revision at any time during follow-up. Comparison of event-free survival by treatment suggested that relapse occurred less often in those treated with two-stage revision, with longer overall event-free survival compared with all other interventions as evidenced by Kaplan–Meier curve with log rank test (P=.019; Figure 1).

Kaplan–Meier event-free survival of patients for whom two-stage surgical revision was used vs any other treatment (including one-stage revision and nonsurgical treatments). Comparison by log rank test showed significantly improved event-free survival with two-stage revision treatment of Staphylococcus lugdunensis prosthetic joint infection (P=.019).

Figure 1:

Kaplan–Meier event-free survival of patients for whom two-stage surgical revision was used vs any other treatment (including one-stage revision and nonsurgical treatments). Comparison by log rank test showed significantly improved event-free survival with two-stage revision treatment of Staphylococcus lugdunensis prosthetic joint infection (P=.019).

The clinical and baseline characteristics of patients who relapsed are compared with those who did not in Table A. Receipt and duration of definitive antibiotics trended toward significance, with those who relapsed having shorter antibiotic therapy and being less likely to have received definitive antibiotic therapy, irrespective of surgical treatment. However, the choice of antibiotics did not affect outcome.

Discussion

These findings suggest that S lugdunensis can potentially cause serious delayed-onset PJIs with a high relapse rate. Additionally, these data suggest a significant difference in cure rates between patients who underwent two-stage revision compared with other treatment modalities. Furthermore, patients treated with a longer duration of antibiotics (>4 weeks) had higher cure rates, although this was not statistically significant.

Staphylococcus lugdunensis has recently been recognized as a common cause of bone and joint infection.14 The first large cohort of patients with S lugdunensis PJI in the United States was described by Shah et al15 in 2010. Previous studies of the organism have provided results similar to those reported in the current study. In several reports, PJIs with S lugdunensis occurred most often in the knees compared with the hips or other joints.5,15 Moreover, the time from index surgery to infection varies and has been reported to range from 3 weeks to 10 years, with one study involving fracture fixation device infections reporting the majority (87%) of cases being delayed or late onset.13,16 In this cohort, 1 infection was diagnosed in the early period (12 days), while the remainder occurred in a delayed or late-onset period. Interestingly, 9 of 28 (32.1%) patients presented with infection more than 10 years after the index procedure, 2 of whom were more than 20 years after implantation of prosthesis.

The current results highlight the importance of aggressive surgical intervention in the treatment of S lugdunensis PJIs. Comparing those patients with any surgical intervention with those patients with antibiotic therapy alone indicated significantly improved event-free survival, even if surgical intervention was only irrigation and debridement rather than revision surgery. The cure rate in this cohort who underwent surgical intervention was similar to that of previous reports. Importantly, it has been observed that the combination of surgical intervention and antimicrobial treatment is associated with higher relapse-free survival.13 Early reports suggested that treatment failures were common in the absence of surgical removal of the prostheses.17 Some authors have suggested high rates of relapse regardless of the use of surgical intervention,5 while others have suggested that thorough debridement is sufficient in the context of prolonged antibiotic therapy.4

The type of surgical intervention was associated with the risk of relapse in this study. While both one- and two-stage revision have been used to treat infected total joints,18–20 patients who were treated with two-stage revision achieved better control of infection compared with patients with other or no interventions.21,22 Moreover, those who received prolonged antibiotic therapy with two-stage revision had the best chance of cure (P=.003). This can be explained by the removal of the infected prosthetic joint, which acts as the nidus of infection, followed by sterilization of the joint space with prolonged antibiotic administration before placing new hardware.

Although the organism is virulent, it is highly susceptible to a range of antimicrobial agents, including oxacillin.20,23 In this study, 97% of isolates were susceptible to oxacillin and 100% to vancomycin, similar to previous reports.1,4,5,15 Surprisingly, the current analysis indicated that patients who were treated with antistaphylococcal beta-lactams had cure rates similar to those with other agents, including vancomycin. Previous studies have demonstrated that glycopeptides have inferior staphylococcal killing when compared with the standard antistaphylococcal beta-lactams (eg, nafcillin or cefazolin).24 However, all of the agents used for the current patients provided some antistaphylococcal activity. Thus, these findings highlight the importance of adequate source control. Nonetheless, treatment with the standard antistaphylococcal beta-lactams (eg, cefazolin) is preferred to vancomycin and is associated with fewer side effects. No patients receiving beta-lactams had any major adverse effects. Conversely, 1 patient receiving IV vancomycin and another receiving IV daptomycin developed acute renal failure and eosinophilic pneumonia, respectively, requiring change of antibiotics, which is similar to previous studies.3,5,15

The authors also noted that patients treated with a prolonged course of IV antibiotics (≥4 weeks) had a lower rate of relapse (P=.004), regardless of surgical treatment. In previous studies, those with observed high cure rates also reported long-term treatment with antibiotics.9,13 A recently published randomized controlled trial indicated that oral antibiotics were noninferior to IV therapy when used during the first 6 weeks for bone and joint infections, including PJIs.25

This study had several limitations. Due to its retrospective nature, it was not possible to determine cause-and-effect relationships rather than associations between treatment approaches and outcomes. In addition, the quality of clinical documentation may have had an effect, as some data may have been missing or inaccurate, as in any retrospective analysis. Also, there may have been changes in clinical practice over time that could have impacted results in a manner that could not be captured in this study. Finally, the sample available for inclusion in this analysis was small and may not have been powered to detect differences in treatment or patient types. This study was exploratory in nature, and hypotheses to guide sample size requirements were not completed. However, the authors included more than a decade of results from 9 hospitals within a large geographic area; thus, these results are expected to be somewhat generalizable.

Conclusion

Although S lugdunensis is a CNS, it is a virulent pathogen and should not be disregarded as a contaminant. If clinical suspicion is high for PJI, it is necessary to identify the species of CNS to guide treatment because S lugdunensis is more aggressive than other CNS. In this series, relapse was high for patients treated without two-stage revision, regardless of route or duration of antibiotic therapy. Although there was a relatively small sample, the results indicate that the optimal therapeutic approach for S lugdunensis PJIs includes aggressive surgical management with two-stage revision and a prolonged course of IV antibiotics to achieve the best cure rate. However, larger prospective studies are needed to confirm these results.

References

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Definitions of Staphylococcus lugdunensis Prosthetic Joint Infection, Treatment Success, and Treatment Failure

S lugdunensis prosthetic joint infection definition:    S lugdunensis isolate from at least 1 periprosthetic tissue or joint fluid culture with:

Purulence around prosthesis at time of surgery or aspiration

Acute inflammation consistent with infection on histopathology

Presence of sinus tract on examination or during surgery

Treatment success/remission: Absence of symptoms or signs of infection evaluated at least 12 months after the end of definitive antimicrobial therapy Treatment failure/relapse: Occurrence of prosthetic joint infection caused by S lugdunensis or any other organism at any time after completion of definitive antimicrobial therapy

Baseline Clinical Characteristics of Patients With Staphylococcus lugdunensis Prosthetic Joint Infection

VariableValue
Age, median (range), y67.9 (42 to 87)
Body mass index, median (range), kg/m230.7 (22.3 to 63.6)
Sex, No. (%)
  Male13 (46.4)
  Female15 (53.6)
Comorbid condition, No. (%)
  Coronary artery disease/myocardial infarction11 (39.3)
  Diabetes mellitus10 (35.7)
  Chronic obstructive pulmonary disease6 (21.4)
  Cancer3 (10.7)
  Rheumatoid arthritis2 (7.1)
Smoking, No. (%)8 (28.6)
Alcohol use, No. (%)5 (17.9)
Intravenous drug use, No. (%)0 (0)
Involved joint, No. (%)
  Ankle1 (3.6)
  Hip7 (25.0)
  Knee19 (67.9)
  Shoulder1 (3.6)
Presenting sign or symptom, No. (%)
  Joint pain27 (96.4)
  Reduced movement27 (96.4)
  Joint swelling20 (71.4)
  Joint erythema11 (39.3)
  Drainage5 (17.9)
  Sinus tract formation3 (10.7)
  Fever3 (10.7)
  Wound dehiscence2 (7.1)
  Bacteremia2 (7.1)
  Endocarditis1 (3.6)
Time from initial joint replacement to prosthetic joint infection, median (range), d1043 (12 to 5459)
Microorganism recovered, No. (%)
  Monomicrobial S lugdunensis prosthetic joint infection24 (85.7)
  Polymicrobial S lugdunensis prosthetic joint infection4 (14.3)
Definitive antibiotic treatment, No. (%)
  No antibiotics3 (10.7)
  Vancomycin8 (28.6)
  Cefazolin7 (25.0)
  Third-generation cephalosporina4 (14.3)
  Cephalexin2 (7.1)
  Daptomycin1 (3.6)
  Ampicillin/sulbactam1 (3.6)
  Nafcillin plus rifampin1 (3.6)
  Linezolid1 (3.6)

Comparison of clinical characteristics and intervention of patients with Staphylococcus lugdunensis prosthetic joint infection (PJI) who relapsed compared to those who did not

VariableCured n=16Relapsed n=12p-value
Median age, years (range)68.5 (42 – 81)68.5 (43 – 87)0.78
Median BMI, kg/m2 (range)31.8 (25.1 – 52.2)25.5 (22.3 – 63.6)0.03
Median time from initial joint replacement to384 (12 – 5459)1690 (284 – 4377)0.37
PJI, days
Median length of stay, days6.5 (2 – 14)3.0 (0 – 19)0.06
Gender, n (%)
  Male8 (50)5 (41.7)0.72
  Female8 (50)7 (58.3)
Comorbidities, n (%)
  Active smoking within 6 weeks4 (25)4 (33.3)0.69
Coronary artery disease/myocardial infarction2 (12.5)9 (75)0.001
  Congestive heart failure2 (12.5)3 (25)0.62
  Chronic kidney disease2 (12.5)3 (25)0.62
  Chronic obstructive pulmonary disease2 (12.5)4 (33.3)0.35
  Dementia0 (0)1 (8.3)0.43
  Diabetes mellitus6 (37.5)4 (33.3)1.0
  End-stage renal disease1 (6.2)0 (0)1.0
  Alcohol use2 (12.5)3 (25)0.62
  Neurologic disorder2 (12.5)2 (16.7)1.0
  Solid tumor3 (18.8)0 (0)0.24
  Peripheral vascular disease1 (6.2)0 (0)1.0
Location, n (%)
  Ankle0 (0)1 (8.3)0.63
  Hip5 (31.2)2 (16.7)
  Knee10 (62.5)9 (75.0)
  Shoulder1 (6.2)0 (0)
Antibiotic treatment, n (%)
  No antibiotics0 (0)3 (100)0.004
  Intravenous antibiotics (>4 weeks)15 (71)6 (29)
  Intravenous antibiotics (<4 weeks)1 (100)0 (0)
  Oral antibiotics (> 4 weeks)0 (0)1 (100)
  Oral antibiotics (< 4 weeks)0 (0)2 (100)
Definitive antibiotics, n (%)16 (100)9 (75)0.07
Choice of antibiotics, n (%)
  Anti-staphylococcal β-lactam agent*7 (44)4 (33)0.973
  Non-antistaphylococcal β-lactam agent+9 (56)5 (67)
Definitive antibiotic duration, days44.6 ± 9.730.2 ± 22.00.06
Surgical intervention, n (%)
  2-stage revision11 (84.6)2 (15.4)0.003
  Polyethylene exchange5 (55.6)4 (44.4)
  1-stage revision0 (0)1 (100)
  No surgery0 (0)5 (100)
Authors

The authors are from the Department of Infectious Diseases (KM, JMD), University of Toledo College of Medicine, and the Research Department (RER) and the Department of Orthopaedic Surgery (GMG), ProMedica Toledo Hospital, Toledo, Ohio; and the Department of Infectious Diseases (GS), Henry Ford Hospital, Detroit, Michigan.

The authors have no relevant financial relationships to disclose.

Correspondence should be addressed to: Geehan Suleyman, MD, Department of Infectious Diseases, Henry Ford Hospital, 2799 W Grand Blvd, CFP 305, Detroit, MI 48202 ( GSULEYM2@hfhs.org).

Received: October 14, 2019
Accepted: June 18, 2020
Posted Online: October 01, 2020

10.3928/01477447-20200923-03

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