Orthopedics

Feature Article 

Incidence and Characteristics of Osteoarticular Infections in Patients With Infective Endocarditis

Hiba K. Anis, MD; Evan M. Miller, BA; Jaiben George, MBBS; Nabin K. Shrestha, MD; Alison K. Klika, MS; Atul F. Kamath, MD; Maja Babic, MD; Carlos A. Higuera, MD

Abstract

Osteoarticular infections (OAIs) in the setting of infective endocarditis (IE) are uncommon. Although morbidity and mortality have been widely studied, details of the characteristics of patients with concurrent IE and OAI are limited. Therefore, the purpose of this study was to determine the (1) incidence, (2) mortality, (3) clinical features, and (4) microbiological profiles of OAIs in the setting of IE. A retrospective review was conducted of 1280 IE cases at a large academic institution between 2009 and 2015. Patients were categorized according to the following OAI types: spondylodiskitis, large joint septic arthritis, other site infections, or multiple affected joints. Inpatient mortality rates, clinical findings, and microbiological characteristics were compared between OAI types. Overall, the incidence of OAI among IE patients was 6.8% (n=87). The in-hospital mortality rate was 9.2% (n=8) and was not significantly associated with OAI type (P=.801). Eighteen patients had multiple affected joints resulting in a total of 114 infected sites. Of these, 39% (n=44) were spondylodiskitis, 29% (n=33) were large joint septic arthritis, and 32% (n=37) were infections of smaller joints. Back pain was most common among patients with spondylodiskitis (P<.001), whereas fever and general fatigue were most common with septic arthritis (P<.001). Of the available bone/ joint cultures, 69% were positive. Overall, Staphylococcus aureus was the most common IE pathogen in patients with both IE and OAI (63%). Clinicians should maintain a high suspicion for OAI in patients with IE caused by Staphylococcus aureus, particularly spondylodiskitis among those presenting with back pain. [Orthopedics 2020; 4X(X):xx–xx.]

Abstract

Osteoarticular infections (OAIs) in the setting of infective endocarditis (IE) are uncommon. Although morbidity and mortality have been widely studied, details of the characteristics of patients with concurrent IE and OAI are limited. Therefore, the purpose of this study was to determine the (1) incidence, (2) mortality, (3) clinical features, and (4) microbiological profiles of OAIs in the setting of IE. A retrospective review was conducted of 1280 IE cases at a large academic institution between 2009 and 2015. Patients were categorized according to the following OAI types: spondylodiskitis, large joint septic arthritis, other site infections, or multiple affected joints. Inpatient mortality rates, clinical findings, and microbiological characteristics were compared between OAI types. Overall, the incidence of OAI among IE patients was 6.8% (n=87). The in-hospital mortality rate was 9.2% (n=8) and was not significantly associated with OAI type (P=.801). Eighteen patients had multiple affected joints resulting in a total of 114 infected sites. Of these, 39% (n=44) were spondylodiskitis, 29% (n=33) were large joint septic arthritis, and 32% (n=37) were infections of smaller joints. Back pain was most common among patients with spondylodiskitis (P<.001), whereas fever and general fatigue were most common with septic arthritis (P<.001). Of the available bone/ joint cultures, 69% were positive. Overall, Staphylococcus aureus was the most common IE pathogen in patients with both IE and OAI (63%). Clinicians should maintain a high suspicion for OAI in patients with IE caused by Staphylococcus aureus, particularly spondylodiskitis among those presenting with back pain. [Orthopedics 2020; 4X(X):xx–xx.]

The annual incidence of infective endocarditis (IE) is estimated to be 3 to 9 cases per 100,000 individuals in industrialized nations, making it the third or fourth most common life-threatening infection syndrome.1,2 In-hospital mortality rates range from 15% to 22%, with a 5-year mortality rate of 40%, and these mortality rates vary among specific subgroups of patients, such as those with native valves or comorbidities.1 The epidemiology of IE has recently evolved to include not only relatively young patients with valvular disease, but now also older adults, even those without prior valvular disease and especially following surgery.3 In this older population, important complications of IE to consider include heart failure, uncontrolled infection, acute renal failure, rheumatic complications, myocarditis, and systemic embolism. Specifically, embolic events are frequent and life-threatening complications caused by the migration of cardiac vegetations, with an overall incidence of 20% to 50%.3–5 Frequent sites of embolism in left-sided IE include the brain and spleen, while pulmonary embolism is frequent in native right-sided and pacemaker lead IE.4

Infected valves also act as a continuous source of bacteremia and may lead to seeding of microorganisms causing infections in other sites of the body, including bones, joints, and vertebral disks.3 Although musculoskeletal symptoms are reported in 19% to 44% of these cases, the diagnosis of a bone or joint infection is less common.6 Because current literature on osteoarticular infections (OAIs) among IE patients is limited to case reports and small retrospective case series, the incidence and characteristics of the disease process are unclear. The management of patients with concomitant OAI and IE typically involves surgeries for both the OAI and the IE in addition to medical treatment. However, the correct type and sequence of management remain an area of uncertainty.

The epidemiology of IE has been evolving during the past decade. The management of OAI in patients with IE is particularly challenging. To effectively treat these patients, it is important to first understand the extent and nature of the disease process. Therefore, the purpose of this study was to determine the (1) incidence, (2) inpatient mortality, (3) clinical features, and (4) microbiological profiles of OAIs in the setting of IE.

Materials and Methods

Study Design

Following institutional review board approval, a retrospective review was conducted of IE cases at a large academic institution between 2009 and 2015. The database used for the study was an institutional infectious endocarditis registry. Data regarding patient demographics, clinical findings, and laboratory findings were manually collected from electronic medical records.

A total of 1280 patients admitted with confirmed IE were identified.7 The electronic medical records of these patients were queried using International Classification of Diseases, 9th Revision, Clinical Modification (ICD-9-CM) diagnosis codes denoting any musculoskeletal involvement. The following ICD-9-CM codes were used: 711.00-99 for pyogenic arthritis, 916.40-99 for arthropathy, 719.01-09 for joint effusion, 730.00-99 for osteomyelitis, and 996.67 for infection due to an internal device, an implant, or a graft. Members of the clinical research team manually reviewed medical records of these patients to identify those with an OAI. An OAI was defined as the presence of septic arthritis or osteomyelitis of any bone or joint during the admission.

Osteoarticular Infections

Patients were separated into cohorts according to the following OAI types: spondylodiskitis, large joint septic arthritis (shoulder, knee, or hip), other sites, or multiple affected sites. The diagnosis of spondylodiskitis was made based on radiological findings (destructive changes on magnetic resonance imaging and/or computed tomography scan) with positive results on blood cultures or biopsies.8,9 Patients with suspected vertebral involvement but negative results on blood cultures and biopsies were excluded. A diagnosis of septic arthritis required either isolation of organisms from the affected joint or, in the setting of previously administered antibiotics, typical clinical symptoms and joint aspirated fluid.10,11Table 1 lists the other OAI sites.

Location of 114 Bone and Joint Infections in 87 Patients

Table 1:

Location of 114 Bone and Joint Infections in 87 Patients

Study Variables

Data on the following were collected and recorded by 2 reviewers (E.M.M., J.G.): patient age, sex, body mass index (BMI), comorbidities, valve affected, pathogen, treatment of IE, Duke criteria, intravenous drug abuse, presence of OAI, OAI type, date of onset of bone and joint symptoms, pathogen causing OAI, treatment of OAI, complications, reoperation, readmission, serum inflammatory markers, synovial fluid analysis results, histology/microbiology results, and in-hospital mortality.

Statistical Analysis

The incidence of OAI in the setting of IE was calculated by dividing the number of patients with a concomitant infection of 1 or more bones and joints by the total number of patients collected from the IE database. Univariate analyses were performed to compare patient demographics, clinical findings, and microbiological characteristics between different types of OAI. Chi-square test or Fisher's exact test was used to compare the categorical variables, while t test or analysis of variance was used to compare the continuous variables. The threshold for statistical significance was maintained at P<.05. Statistical analysis was performed using Excel (Microsoft Corp, Redmond, Washington) and R statistical software (R Core Team, Vienna, Austria).

Results

Incidence

Overall, the incidence of OAI among patients with IE was 6.8% (n=87). Specifically, 2.8% (n=36) of the patients with IE had spondylodiskitis of native vertebra, 1.2% (n=15) had large joint septic arthritis, 1.4% (n=18) had an OAI of other sites, and 1.4% (n=18) had multiple joints affected.

Because some (of the 87) patients had multiple affected joints, there were 114 sites of OAI in total. Of these 114 sites, 39% (n=44) were diagnosed as spondylodiskitis, 29% (n=33) were large joint septic arthritis (n=7 shoulders, n=6 hips, and n=20 knees), and 32% (n=37) were of other smaller sites (Table 1).

Mortality

The in-hospital mortality rate overall among patients admitted for IE with concomitant OAI was 9.2% (n=8). Inpatient mortality rates between OAI types were not found to be significantly different. The mortality rate was 6% (n=2) with spondylodiskitis, 13% (n=2) with large joint septic arthritis, 11% (n=2) with other site infections, and 11% (n=2) with multiple affected joints (P=.801).

Clinical Features

Injection drug users (IDUs) made up 16% (n=14) of the patients with both IE and OAI. Compared with the other OAI types in which 20% to 22% of patients were IDUs, fewer patients with spondylodiskitis were IDUs (8%, n=3). However, this difference was not found to be statistically significant (P=.439).

Overall, approximately one-fourth of all patients (26%, n=23) had prosthetic valve infections and three-fourths had native valve infections (74%, n=64). There was no significant association between OAI type and valve type (P=.319). Additionally, compared with the other heart valves, mitral valves were most commonly affected overall (47%, n=41), as well as within the different OAI types.

Patients with spondylodiskitis more commonly presented with back pain compared with patients with the other OAI types (P<.001). Fever and general fatigue were most common among those with large joint septic arthritis (P<.001) (Table 2).

Demographic Characteristics of 87 Patients With an Osteoarticular Infection Complicating Infective Endocarditis

Table 2:

Demographic Characteristics of 87 Patients With an Osteoarticular Infection Complicating Infective Endocarditis

Microbiological Profiles

Overall, Staphylococcus aureus was the most common pathogen causing IE and was isolated from 63% (n=55) of all patients with both IE and OAI. Streptococcus species were the next most common pathogens responsible for IE, affecting 19 patients (22%). Other microorganisms responsible for IE were Enterococcus faecalis (9%, n=8), coagulase-negative staphylococci (3%, n=3), and Candida albicans (2%, n=2). No associations were observed between causative organism for IE and the OAI type (P=.076) (Table 2).

Overall, 43% (n=49) of the 114 OAI sites were not biopsied: 3% (n=1) of the large joints, 30% (n=11) of the other sites, and 84% (n=37) of the spondylodiskitis sites. Therefore, bone and joint cultures were available for 57% (n=65) of all of the affected OAI sites. Of these available bone and joint cultures, 69% (n=45) had positive results. Similar to the organisms causing IE, of all of the positive cultures, the most common organism isolated from the OAI sites was Staphylococcus aureus (51%, n=33) (Table 3).

Organisms Isolated From Biopsy of 114 Sites of Bone and Joint Infections in 87 Patients With Infective Endocarditis

Table 3:

Organisms Isolated From Biopsy of 114 Sites of Bone and Joint Infections in 87 Patients With Infective Endocarditis

In the majority of the positive cultures obtained from the OAI sites, the same pathogen was isolated from both the OAI and the IE sites. Of the 65 positive OAI cultures, 58% (n=38) were consistent with the IE cultures. The following organisms were found in both the IE and the OAI sites: Staphylococcus aureus (n=31), Streptococcus species (n=5), Staphylococcus aureus and Streptococcus species (n=1), and Staphylococcus aureus and Pseudomonas aeruginosa (n=1).

Discussion

Patients with IE who present with bone and joint infections are challenging to manage, particularly when determining the type and sequence of treatment. The first step in addressing this unusual challenge is to carefully characterize patients. Although most recent studies on this topic have focused on spondylodiskitis in the setting of endocarditis, there are other bone and joint infections underrepresented among single case reports in the literature. To the authors' knowledge, this is the largest cohort of patients with bone and joint infections complicating IE. In this study, the authors found that OAIs were present in approximately 7% of patients with IE. Spondylodiskitis was the most common OAI. The majority of patients with concomitant OAI and IE were infected with Staphylococcus aureus.

This study is consistent with previous literature and found that the occurrence of OAI in patients with IE is rare.6,12,13 Important limitations of the primary literature include the small number of available series and the absence of uniform criteria when evaluating patients with endocarditis and bone infections.14 The incidence in the current study was higher than that reported previously by Lamas et al,15 which was observed to be 4.3% (30 of 693 IE patients). In their study, of the 30 reported cases of bone and joint infections complicating IE, 30% (n=10) involved the vertebrae and 29% (n=14) involved large joints, similar to the current authors' observations.

Back pain was found to be most commonly reported in cases of spondylodiskitis with IE. Similarly, Tamura16 performed a retrospective analysis of 58 patients with IE and found that all 11 patients diagnosed with spondylodiskitis reported back pain. One clinical challenge for spondylodiskitis is a delay in diagnosis; pathologic spinal changes are observed 3 to 5 days after the onset of infection on magnetic resonance imaging and at 2 to 4 weeks on plain radiographs.17,18 As symptoms for spondylodiskitis are largely nonspecific, current guidelines published through the Infectious Diseases Society of America recommend suspicion of a spinal infection if local pain, fever, elevated erythrocyte sedimentation rate and C-reactive protein, sepsis with Staphylococcus aureus, new neurologic symptoms, and, notably, IE with new local pain exist.19 In the current study, magnetic resonance imaging was the predominant modality used for the diagnosis of vertebral osteomyelitis. Although isolated spondylodiskitis was the most common OAI in the setting of IE, it is possible that it may not have been diagnosed in some patients because not every patient receives imaging of the spine. However, almost half of the patients without spondylodiskitis (45%, 23 of 51) also had imaging of the spine, which suggests a low likelihood of missed vertebral infections.

Among the 87 patients with IE, Staphylococcus aureus was the most common causative pathogen. Only gram-positive cocci or fungal microorganisms were isolated from blood cultures, which is consistent with prior studies.15,20 Vlahakis et al6 reported that among 9 separate case series including 1312 patients with IE and musculoskeletal manifestations, only 4 cases of IE due to Enterococcus species were reported. In the current study, there were 8 patients with E faecalis, and all presented with vertebral osteomyelitis. Additionally, among the bone and joint cultures with positive results, the vast majority yielded gram-positive cocci or fungal microorganisms, with only 1 culture of a gramnegative rod. In the case of vertebral osteomyelitis, specific specimens obtained by either percutaneous biopsy or open surgery were unavailable in 82% of these infections (36 of 44), and antibiotic selection was based on blood culture results, which agrees with the therapeutic approach found in prior studies on vertebral infections.21 In the current study, a wider microbiological profile was observed among the OAIs of smaller bones and joints, which emphasizes the importance of evaluating these types of infections in IE patients; previous studies have underrepresented OAIs of other smaller sites and tended to focus primarily on spondylodiskitis.6,13–16,21

The current authors found that 16% of patients with both IE and OAI were documented as IDUs, which conflicts with a previous study by Sapico et al.13 That study evaluated 104 patients with IE and found that of patients who had concomitant OAI and IE, all 15 (100%) were documented as being IDUs. No bone and joint infections occurred among the IE patients who were not IDUs. Of note, the study by Sapico et al13 was limited in the number of cases and the data were collected between 1989 and 1993 from a cardiology service in Los Angeles county, which may explain the discrepancy.

There were some limitations to this study. Patients from the IE registry database were screened for possible OAI with ICD-9-CM codes. This screening is subject to coding inaccuracies. Although several codes were used to identify those with OAI, it is possible that some patients with OAI may not have been identified. Additionally, a referral bias is possible because this study was conducted at a referral center. Therefore, the incidence of OAI in this study may not be generalizable to other centers. In terms of analysis, patient characteristics and variables within the study only allow for the formation of a reasonable descriptive study. Clinical characteristics and diagnostic variables were collected through manual reviews of medical records. Thus, the accuracy by which these are represented in patient charts and records is variable. Current diagnostic recommendations for OAIs and IE also limited specific information pertaining to their onset as musculoskeletal symptoms can often be the earliest signs.6 Due to the retrospective nature of this study, it was difficult to establish whether these OAIs were a result of seeding from the infected valves, or if the OAIs led to IE. An ideal study would also have cultures available for all OAIs; however, in this study, there were some patients who did not have biopsies of their OAI. Despite these limitations, the authors were able to determine the characteristics of a consecutive set of patients with IE who had concomitant bone and joint infections.

Conclusion

This study found that OAI is an uncommon presentation in patients with IE, having an incidence of 7%. In this large contemporary series of IE patients, spondylodiskitis was the most common bone or joint infection, and almost all patients with concomitant IE and spondylodiskitis reported back pain. Therefore, clinicians should have a low threshold to investigate vertebral infections in patients with IE, especially in the presence of back pain. Because the majority of patients with concomitant OAI and IE had cultures positive for Staphylococcus aureus, there should be a high suspicion for OAI when Staphylococcus aureus is isolated as the causative IE pathogen. Findings from this study provide an overview of OAI in the setting of IE and may help with the challenging management of such patients. Further research is needed to evaluate predictors of morbidity and mortality as well as to assess the optimal management in these patients.22,23

References

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Location of 114 Bone and Joint Infections in 87 Patients

SiteNo.
Spondylodiskitis44 (39%)
Large joint septic arthritis33 (29%)
  Shoulder7
  Hip6
  Knee20
Other site37 (32%)
  Acromioclavicular joint2
  Ankle4
  Body of the sternum1
  Calcaneus1
  Cranium1
  Elbow3
  Iliac bone1
  Metatarsal4
  Phalanges12
  Sacroiliac joint4
  Wrist4

Demographic Characteristics of 87 Patients With an Osteoarticular Infection Complicating Infective Endocarditis

VariableTotal OAI (N=87)Spondylodiskitis (n=36)Septic Arthritis of Large Joints (n=15)Other OAIs (n=18)Multiple OAIs (n=18)P
Age, mean, y57.960.154.053.361.5.274
Male, No.542571012.430
BMI, mean, kg/m229.029.329.528.828.4.960
Age-adjusted Charlson Comorbidity3.94.42.73.93.8.314
Index, mean
Injective drug user, No.143 (8.3%)3 (20.0%)4 (22.2%)4 (22.2%).439
Clinical feature, No.
  Back pain53 (60.9%)35 (97.2%)4 (26.7%)7 (38.8%)7 (38.8%)<.001
  Fever52 (59.8%)13 (36.1%)15 (100%)14 (77.8%)10 (55.6%)<.001
  General fatigue57 (67.8%)17 (47.2%)15 (100%)17 (94.4%)10 (55.6%)<.001
Type of IE, No..319
  Prosthetic23 (26.4%)12 (33.3%)5 (33.3%)4 (22.2%)2 (11.1%)
  Native valve64 (73.6%)24 (66.7%)6 (40.0%)18 (100%)16 (88.9%)
Valve affected, No..250
  Mitral41 (47.1%)16 (44.4%)10 (66.7%)7 (38.9%)8 (44.4%)
  Aortic8 (9.2%)13 (36.1%)2 (13.3%)3 (16.7%)5 (27.8%)
  Other/multiple23 (26.4%)7 (19.5%)3 (20.0%)8 (44.4%)5 (27.8%)
Organism causing IE, No..076
   Staphylococcus aureus55 (63.2%)17 (47.2%)11 (73.3%)13 (72.2%)14 (77.8%)
  Non-Staphylococcus aureus
  Coagulase-negative staphylococci3 (3.4%)2 (5.6%)001 (5.6%)
   Enterococcus faecalis8 (9.2%)8 (22.2%)000
   Streptococcus species19 (21.8%)8 (22.2%)4 (26.7%)4 (22.2%)3 (16.7%)
   Candida albicans2 (2.3%)1 (2.8%)01 (5.6%)0

Organisms Isolated From Biopsy of 114 Sites of Bone and Joint Infections in 87 Patients With Infective Endocarditis

MicroorganismNo.

Spondylodiskitis (N=44)Septic Arthritis of Large Joints (N=33)Other Site Infections (N=37)
Gram positive
   Staphylococcus aureus5 (12%)16 (48%)12 (32%)
  Coagulase-negative staphylococci01 (3%)3 (8%)
   Enterococcus faecalis001 (3%)
   Streptococcus species02 (6%)3 (8%)
Gram negative
   Klebsiella pneumoniae01 (3%)0
Other microorganism
   Candida albicans001 (3%)
No growth2 (5%)12 (36.4%)6 (16%)
No biopsy37 (84%)1 (3%)11 (30%)
Authors

The authors are from the Department of Orthopaedic Surgery, Cleveland Clinic Foundation, Cleveland, Ohio.

Dr Anis, Mr Miller, Mr George, Dr Shrestha, Ms Klika, and Dr Babic have no relevant financial relationships to disclose. Dr Kamath is on the speaker's bureau of and is a paid consultant for DePuy Synthes and Zimmer Biomet. Dr Higuera has received grants from KCl, Stryker, Zimmer Biomet, Orthogenics, Orthofix, Ferring Pharmaceuticals, Cymedica, and Cempra.

Correspondence should be addressed to: Alison K. Klika, MS, Department of Orthopaedic Surgery, Cleveland Clinic Foundation, 9500 Euclid Ave/A41, Cleveland, OH 44195 ( klikaa@ccf.org).

Received: July 18, 2019
Accepted: September 12, 2019
Posted Online: November 06, 2019

10.3928/01477447-20191031-02

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