Key Points
Question
What are the clinical characteristics and outcomes of patients with Cutibacterium acnes endocarditis?
Findings
In this case series including 105 patients, C acnes endocarditis was seen predominantly among male patients with prosthetic heart valves and was characterized by absence of fever, close to normal inflammatory markers, and a prolonged time to positive blood culture results. Surgical treatment was required in a high proportion of patients.
Meaning
This study suggests that C acnes endocarditis is difficult to diagnose because typical endocarditis features are often absent; it is recommended to extend blood culturing for male patients with new-onset prosthetic valve dysfunction, peripheral embolization, or signs of heart failure.
Abstract
Importance
It is suggested that patients with Cutibacterium acnes endocarditis often present without fever or abnormal inflammatory markers. However, no study has yet confirmed this statement.
Objective
To assess the clinical characteristics and outcomes of patients with C acnes endocarditis.
Design, Setting, and Participants
A case series of 105 patients presenting to 7 hospitals in the Netherlands and France (4 university hospitals and 3 teaching hospitals) with definite endocarditis according to the modified Duke criteria between January 1, 2010, and December 31, 2020, was performed. Clinical characteristics and outcomes were retrieved from medical records. Cases were identified by blood or valve and prosthesis cultures positive for C acnes, retrieved from the medical microbiology databases. Infected pacemaker or internal cardioverter defibrillator lead cases were excluded. Statistical analysis was performed in November 2022.
Main Outcomes and Measures
Main outcomes included symptoms at presentation, presence of prosthetic valve endocarditis, laboratory test results at presentation, time to positive results of blood cultures, 30-day and 1-year mortality rates, type of treatment (conservative or surgical), and endocarditis relapse rates.
Results
A total of 105 patients (mean [SD] age, 61.1 [13.9] years; 96 men [91.4%]; 93 patients [88.6%] with prosthetic valve endocarditis) were identified and included. Seventy patients (66.7%) did not experience fever prior to hospital admission, nor was it present at hospitalization. The median C-reactive protein level was 3.6 mg/dL (IQR, 1.2-7.5 mg/dL), and the median leukocyte count was 10.0 × 103/µL (IQR, 8.2-12.2 × 103/µL). The median time to positive blood culture results was 7 days (IQR, 6-9 days). Surgery or reoperation was indicated for 88 patients and performed for 80 patients. Not performing the indicated surgical procedure was associated with high mortality rates. Seventeen patients were treated conservatively, in accordance with the European Society of Cardiology guideline; these patients showed relatively high rates of endocarditis recurrence (5 of 17 [29.4%]).
Conclusions and Relevance
This case series suggests that C acnes endocarditis was seen predominantly among male patients with prosthetic heart valves. Diagnosing C acnes endocarditis is difficult due to its atypical presentation, with frequent absence of fever and inflammatory markers. The prolonged time to positivity of blood culture results further delays the diagnostic process. Not performing a surgical procedure when indicated seems to be associated with higher mortality rates. For prosthetic valve endocarditis with small vegetations, there should be a low threshold for surgery because this group seems prone to endocarditis recurrence.
This case series assesses the clinical characteristics and outcomes of patients with Cutibacterium acnes endocarditis.
Introduction
Cutibacterium acnes is a gram-positive bacterium, most known for its role in acne vulgaris. C acnes is generally considered nonpathogenic, and positive blood culture results are often regarded as contaminated.1 In recent years, more attention has been paid to C acnes as a cause of infective endocarditis (IE). Experienced clinicians hypothesize that patients with C acnes endocarditis are difficult to diagnose because typical IE features, such as fever and high levels of inflammatory markers, are often absent. However, these statements are supported only by case reports or small case series.2,3 Therefore, the aim of this study is to examine the clinical characteristics and outcomes of patients with C acnes IE in a large cohort of more than 100 patients.
Methods
We performed a retrospective case series in 7 hospitals in the Netherlands and France (4 university hospitals and 3 teaching hospitals). Patients with a diagnosis of definite IE according to the modified Duke criteria4 between January 1, 2010, and December 31, 2020, were included. Cases with an isolated infected pacemaker or internal cardioverter defibrillator lead cases were excluded because we were interested only in valve endocarditis. Cases were identified by positive blood or valve and prosthesis culture results, retrieved from the medical microbiology databases. The Medical Ethics Review Committee Leiden The Hague Delft waived the need for consent because of the retrospective nature of this study in which participants are not subjected to any form of action. In addition, data were deidentified. Recurrence of IE was defined as IE relapse and/or a new episode of C acnes IE after initial treatment. Data are presented following the reporting guideline for case series.5
Statistical Analysis
Statistical analysis was performed in November 2022 using IBM SPSS Statistics, version 27 (IBM Corp). Normally distributed variables were reported as mean (SD) values, and nonnormally distributed variables are displayed as median (IQR) values. Frequencies and percentages were calculated. There were no statistical tests performed.
Results
A total of 105 patients (mean [SD] age, 61.1 [13.9] years; 96 men [91.4%]) with C acnes IE were identified and included. Most patients (94 [89.5%]) had previous cardiac surgery, which in most cases concerned previous valve surgery (93 [88.6%]). Baseline characteristics, including the types of previous cardiac surgical procedures, are presented in Table 1. The median time between index surgery and hospital presentation was 35.0 months (IQR, 15.5-71.5 months). There were 12 cases (11.4%) of native valve endocarditis: 5 aortic valve, 3 mitral valve, 1 combined aortic valve and mitral valve, and 3 tricuspid valve cases. The 3 patients with tricuspid valve native valve endocarditis had pacemaker leads. Tricuspid valve plasty was required for 1 patient with severe tricuspid valve regurgitation. For other native valve endocarditis cases, there was no underlying predisposition.
Table 1. Baseline Characteristics of the Total Cohort.
| Characteristic | Total cohort, No. (%) (N = 105) |
|---|---|
| Sex | |
| Male | 96 (91.4) |
| Female | 9 (8.6) |
| Age, mean (SD), y | 61.1 (13.9) |
| Atrial fibrillation | 40 (38.1) |
| Previous cerebrovascular disease | 35 (33.3)a |
| Previous stroke | 17 (16.2) |
| Previous transient ischemic attack | 21 (20.0) |
| Left ventricular ejection fraction | |
| Good | 83 (79.0) |
| Moderate | 19 (18.1) |
| Poor | 3 (2.9) |
| Immunocompromised | 0 |
| Previous Cutibacterium acnes endocarditis | 2 (1.9) |
| Previous cardiac surgery | 94 (89.5) |
| Aortic valve replacement | 66 (62.9) |
| Bentall procedure | 17 (16.2) |
| Mitral valve replacement | 7 (6.7) |
| Mitral and tricuspid valve repair with annuloplasty ring | 1 (1.0) |
| Isolated ascending aorta replacement | 2 (1.9) |
| Isolated coronary artery bypass grafting | 1 (1.0) |
Five patients had a history of both stroke and transient ischemic attack.
At presentation, 70 patients (66.7%) did not report having experienced fever (defined as a measured temperature >38.0 °C) prior to hospital admission, nor was it present on physical examination (Table 2). The most frequently observed symptoms were dyspnea (38 [36.2%]), malaise (26 [24.8%]), and stroke (20 [19.0%]). Most patients (43 [41.0%]) experienced symptoms for 1 to 2 weeks prior to hospital admission. Five patients (4.8%) with prosthetic valve endocarditis (PVE) were asymptomatic, but routine echocardiography revealed new-onset prosthetic valve dysfunction. The median C-reactive protein (CRP) level at presentation was 3.6 mg/dL (IQR, 1.2-7.5 mg/dL (reference range, <0.1 mg/dL [to convert to milligrams per liter, multiply by 10.0]).6 Moreover, the CRP level was not suspected for a bacterial infection (≤1.0 mg/dL) for 23 patients (21.9%). The median leukocyte count was within the reference range (10.0 × 103/µL [IQR 8.2-12.2 × 103/µL] [to convert to ×109/L, multiply by 0.001]). Laboratory test results at hospital admission are presented in Table 2. Blood cultures were performed for 87 patients, of whom 76 patients had at least 1 positive blood culture result. The median time to positive blood cultures was 7 days (IQR, 6-9 days), and 25.0% (19 of 76) became positive within 5 days. In total, 477 sets of blood cultures were obtained, of which 191 (anaerobic) cultures (40.0%) became positive.
Table 2. Admission Parameters of the Total Cohort.
| Parameter | Total cohort, No. (%) (N = 105) |
|---|---|
| Onset of symptoms | |
| ≤2 wk | 43 (41.0) |
| 2-4 wk | 18 (17.1) |
| 5 wk to 3 mo | 18 (17.1) |
| >3 mo | 26 (24.8) |
| Symptoms | |
| Fever | 35 (33.3) |
| Stroke | 20 (19.0) |
| Myocardial infarction | 3 (2.9) |
| Major arterial emboli | 3 (2.9) |
| Malaise | 26 (24.8) |
| Chills | 38 (36.2) |
| Dyspnea | 38 (36.2) |
| Weight loss | 14 (13.3) |
| Newly diagnosed cardiac murmur | 13 (12.4) |
| Splinter hemorrhage | 2 (1.9) |
| Asymptomatic | 8 (7.6) |
| Hemoglobin level, median (IQR), g/dL | 7.6 (6.8-8.3) |
| MCV, median (IQR), µm3 | 86.0 (83.0-90.0) |
| CRP, median (IQR), mg/dL | 3.6 (1.2-7.5) |
| CRP ≤1.0 mg/dL | 23 (21.9) |
| Leukocyte count, median (IQR), ×103/µL | 10.0 (8.2-12.2) |
| eGFR, median (IQR), mL/min/1.732 | 64.0 (59.0-87.0) |
Abbreviations: CRP, C-reactive protein; eGFR, estimated glomerular filtration rate; MCV, mean corpuscular volume.
SI conversion factors: To convert hemoglobin to grams per liter, multiply by 10.0; MCV to femtoliters, multiply by 1.0; CRP to milligrams per liter, multiply by 10.0; and leukocytes to ×109/L, multiply by 0.001.
In total, 64 patients were classified as having definite IE according to the modified Duke criteria.4 A positive blood culture result was a major criterion for 54 patients, and echocardiography findings were positive for all of these patients. The minor criterion observed most frequently was cardiac predisposition (63 of 64 [98.4%]). Peripheral embolization was observed for 30 of 64 patients (46.9%). Cardiac computed tomography (CT) was performed for 28 patients, with positive results for 26 patients (92.9%). 18Fluorodeoxyglucose positron emission tomography or CT (18FDG PET-CT) was performed for 35 patients, with positive results for 32 patients (91.4%). Thirty of 105 patients were classified as having possible IE by the modified Duke criteria because of positive echocardiography findings combined with at least 1 minor criterion. Cardiac CT was performed for 9 patients, with positive findings for 8 patients (88.9%). 18FDG PET-CT was performed for 2 patients, with positive findings for 1 patient (50.0%). In this possible IE group, IE was yet confirmed as definite by surgical findings combined with positive (prosthetic) valve culture results (27 of 30), polymerase chain reaction testing (2 of 30), or obduction (1 of 30).
Eleven of 105 patients were not suspected to have IE, but they underwent cardiac surgery with intraoperative confirmation of definite IE by the pathologic criteria. Surgery was performed for the following reasons: native valve regurgitation (n = 5), native aortic valve stenosis (n = 2), and prosthesis degeneration (n = 4). Infective endocarditis was suspected for these patients because of valvular perforations and the presence of vegetations. In all 11 patients, at least 2 cultures had positive results (2 valve cultures or a valve culture combined with a culture of a vegetation or a postoperative blood culture). Preoperatively, cardiac CT was performed for 3 patients, but none had positive findings for IE. An overview of the major and minor IE criteria are presented in Table 3.
Table 3. Major and Minor Criteria for Patients With Definite and Possible Endocarditis.
| Criterion | Total cohort, No. (%) (N = 105) |
|---|---|
| Total cohort | |
| Definite IE according to diagnostic criteria | 64 (61.0) |
| 2 Major criteria | 54 (51.4) |
| 1 Major criterion and 3 minor criteria | 10 (9.5) |
| 5 Minor criteria | 0 |
| Major criteria | |
| Blood culture results positive for IE | 54 (51.4) |
| Echocardiography positive for IE | 64 (61.0) |
| Vegetation | 43 (41.0) |
| >1 cm | 14 (13.3) |
| ≤1 cm | 29 (27.6) |
| Abscess | 22 (21.0) |
| Pseudoaneurysm | 4 (3.8) |
| Valvular perforation or new-onset prosthetic valve dysfunction (partial dehiscence or severe regurgitation) | 18 (17.1) |
| Minor criteria | |
| Predisposition | 63 (60.0) |
| Fever | 28 (26.7) |
| Total vascular phenomena | 32 (30.5) |
| Stroke | 19 (18.1) |
| Myocardial infarction | 3 (2.9) |
| Major arterial emboli | 3 (2.9) |
| Splinter hemorrhage | 3 (2.9) |
| Silent emboli | |
| Brain | 2 (1.9) |
| Spleen | 2 (1.9) |
| Immunologic phenomena | 0 |
| Microbiological evidence not meeting a major criterion | 11 (10.5) |
| Preoperative classified as possible IE and confirmed by culture, histologic examination, or PCR of vegetation, (prosthetic) valve, or abscess | 30 (28.6) |
| Possible IE | |
| 1 Major criterion and 1 minor criterion | 15 (14.3) |
| 1 Major criterion and 2 minor criteria | 15 (14.3) |
| Major criteria | |
| Blood culture results positive for IE | 30 (28.6) |
| Echocardiography positive for IE | 30 (28.6) |
| Vegetation | 12 (11.4) |
| >1 cm | 6 (5.7) |
| ≤1 cm | 6 (5.7) |
| Abscess | 11 (10.5) |
| Pseudoaneurysm | 2 (1.9) |
| Valvular perforation or new-onset prosthetic valve dysfunction (partial dehiscence or severe regurgitation) | 22 (21.0) |
| Minor criteria | |
| Predisposition | 29 (27.6) |
| Fever | 5 (4.8) |
| Total vascular phenomena | 1 (1.0) |
| Stroke | 1 (1.0) |
| IE preoperatively not suspected but diagnosed by pathologic criteria and intraoperative confirmation (culture, histologic examination of vegetation, or [prosthetic] valve or abscess) | 11 (10.5) |
Abbreviations: IE, infective endocarditis; PCR, polymerase chain reaction.
Surgery or reoperation was indicated (class I or IIa5) for 88 patients but performed for 80 patients (76.2%). Perioperatively, the most frequently observed findings were (aortic root) abscesses (37 of 80 [46.3%]), prosthetic valve dehiscence (32 of 80 [40.0%]), and vegetations (26 of 80 [32.5%]). Complex anatomical repair of the left ventricular outflow tract, aortic root, or the aortomitral continuity was required for 11 of 80 patients (13.8%). The indications for surgery as well as the types of surgery performed are presented in Table 4. The postoperative 30-day mortality rate was 15.0% (12 of 80), and the 1-year mortality rate was 22.5% (18 of 80). Six of 80 patients (7.5%) who underwent surgery experienced IE recurrence.
Table 4. Indications for Surgery and the Types of Surgical Procedures Performed.
| Indication and type | Patients receiving surgery, No. (%) (n = 80) |
|---|---|
| Indication | |
| Heart failure due to (prosthetic) valve dysfunction | 22 (27.5) |
| Uncontrolled infection (abscess, pseudoaneurysm, fistula, or enlarging vegetation) | 52 (65.0) |
| Prevention of embolism | 6 (7.5) |
| Surgery type | |
| Aortic valve replacement | 38 (47.5) |
| Bentall procedure | 20 (25.0) |
| Mitral valve replacement | 7 (8.8) |
| Mitral valve plasty | 2 (2.5) |
| Aortic replacement plus mitral valve replacement | 1 (1.3) |
| Aortic valve replacement plus mitral valve plasty | 3 (3.8) |
| Aortic valve replacement plus mitral valve replacement plus tricuspid valve plasty | 2 (2.5) |
| Mitral valve replacement plus tricuspid valve plasty | 1 (1.3) |
| Mitral valve replacement plus ascending aorta replacement | 1 (1.3) |
| Bentall procedure plus mitral valve plasty | 2 (2.5) |
| Bentall procedure plus mitral valve replacement | 1 (1.3) |
| Tricuspid valve plasty | 1 (1.3) |
| Isolated ascending aorta replacement | 1 (1.3) |
Twenty-five of 105 patients were treated conservatively. Despite the indication for surgery, a surgical procedure was not performed for 8 of 25 patients due to comorbidity. Three of these 8 patients died within 30 days after hospital presentation. All 3 had a poor prognosis because of an endocarditis-related stroke. Moreover, 1 of 8 patients in this group experienced PVE recurrence, subsequently requiring surgery because of a stroke. In the other 17 of 25 patients who received conservative treatment, there was no indication for a surgical procedure. No patients in this group died within 1 year after hospital admission, and 5 of 17 patients (29.4%) experienced IE recurrence. These patients had left-sided PVE with small vegetations. Mortality rates as well as C acnes recurrence rates are presented in Table 5.
Table 5. Mortality and Cutibacterium acnes Infective Endocarditis Recurrence Rates for Patients Treated Surgically and Conservatively Across the Indications for Surgery.
| Outcome | Patients, No. (%) | ||
|---|---|---|---|
| Surgery indicated and performed (n = 80) | Surgery indicated but not performed (n = 8) | Surgery not indicated; only antibiotic treatment (n = 17) | |
| 30-d Mortalitya | 12 (15.0) | 3 (37.5) | 0 |
| 1-y Mortalitya | 18 (22.5) | 0 | 0 |
| C acnes recurrence | 6 (7.5) | 1 (12.5) | 5 (29.4) |
| Timeline of recurrence | |||
| During admission | 0 | 0 | 1 (5.9) |
| 30 d to 3 mo After discharge | 2 (2.5) | 0 | 2 (11.8) |
| 3-6 mo After discharge | 2 (2.5) | 1 (12.5) | 0 |
| 6 mo to 1 y After discharge | 0 | 0 | 1 (5.9) |
| ≥1 y After discharge | 2 (2.5) | 0 | 1 (5.9) |
For surgically treated patients, postoperative mortality rates are presented. For patients treated conservatively, mortality rates after hospital admission are presented.
All but 1 patient received empirical and, when susceptibility results were available, targeted antibiotic therapy after diagnosis as advised by the European Society of Cardiology guideline.7 The latter patient had a severe stroke at presentation with an unfavorable prognosis. The administered intravenous antibiotic regimens included benzylpenicillin, 12 million units/d (71 [67.6%]); benzylpenicillin, 18 million units/d (11 [10.5%]); vancomycin, 2 to 3 g/d (11 [10.5%]); amoxicillin, 12 g/d (6 [5.7%]); and ceftriaxone, 2 to 4 g/d (3 [2.9%]). All 12 patients who experienced C Acnes IE recurrence were treated with benzylpenicillin, 12 million units/d. Nineteen patients (18.1%) received additional rifampicin; only 1 of these patients experienced IE recurrence. In accordance with the European Society of Cardiology guideline, intravenous antibiotics were given for at least 6 weeks after the last positive blood or tissue culture result. Two patients (1.9%) did not receive intravenous antibiotic therapy because of patient preference and a chronically infected ascending aorta prosthesis. Clindamycin and amoxicillin, respectively, were given.
Discussion
To our knowledge, this study is the world’s largest case series of C acnes IE. It confirms the hypothesis that the clinical presentation of patients with C acnes IE differs significantly from that of other bacterial causative agents. In our study, C acnes IE was characterized by absence of fever (66.7%) and close to normal CRP levels. In contrast, in the EURO-ENDO (European Endocarditis) registry, 77% of patients with IE had fever, and the median CRP level was 6.5 mg/dL.8 Aside from the diagnostic challenges inherent to PVE,9 the diagnostic process in C acnes IE is further impaired by the prolonged time to positive blood culture results. So, for male patients with prosthetic heart valves presenting with signs of heart failure or peripheral embolization, there should be a low threshold for performing blood cultures (>5 days’ incubation period). Echocardiography remains the criterion standard in detecting IE, but additional cardiac CT or 18FDG PET-CT is useful in suspected PVE with periannular extension.9,10 For cardiac CT and 18FDG PET-CT, we observed a sensitivity of 85.0% and 89.2%, respectively. Thus, the high glucose uptake in PET-CT does not match the assumed low virulence of C acnes IE.
We hypothesize that C acnes IE occurs mostly among male patients because the sebaceous glands, where C acnes predominates,11 proliferate under stimulation of androgens.12 Because the male chest is rich with sebaceous glands, we suggest the surgical wound is contaminated with C acnes during index (valve) surgery. Subsequently, we assume the low virulence and slow growth of C acnes13 results in patients presenting several years after index surgery. We hypothesize that additional preoperative measures, such as topical agents, can be effective in C acnes IE prevention for patients with acne on the thorax. However, further research is needed on this topic.
Although levels of inflammatory markers are generally low at presentation, the high share of aortic root abscesses emphasizes the indolent but not innocent nature of C acnes IE. If surgery is indicated,7 it should be offered to patients because mortality is high when it is indicated but not performed.14,15 In accordance with the current guideline, conservative treatment should be performed in right-sided IE or native valve IE without uncontrolled infection, heart failure, or large vegetations. In PVE with small vegetations, however, antibiotic treatment alone seems insufficient to eradicate C acnes, considering the relatively high rates of short-term IE recurrence. More research is needed on the optimal antibiotic therapy, with or without adding rifampicin. Moreover, further research should explore the effectiveness of chronic oral suppression therapy in C acnes IE. For PVE with small vegetations, we suggest a new class IIa indication for surgery for this group.
Limitations
Our study has several limitations. First, the retrospective design of our study creates the risk of information bias. Although we comprehensively assessed all patients’ records to and from referring hospitals, we cannot rule out possible inaccuracies in the provided data. Second, because we opted not to perform statistical analysis because of the small sample size, we cannot provide the best antibiotic regimen (with or without adding rifampicin) to treat C acnes IE and to minimize the risk of IE recurrence. Also, although we observed a trend of higher C acnes IE recurrence rates after conservative treatment, we must look at this finding in the light of a lack of underlying statistical evidence. Third, C acnes is a known skin contaminant, so blood or tissue culture results could have been false positive. Nevertheless, all included cases had multiple positive blood or tissue culture results, combined with positive echocardiography findings and/or surgical evidence, which means that all cases were definite IE by C acnes.
Conclusions
In this case series, we found that C acnes endocarditis was seen predominantly among male patients with prosthetic heart valves. Diagnosing C acnes endocarditis is difficult due to its atypical presentation, with frequent absence of fever and inflammatory markers. The prolonged time to positivity of blood culture results further delays the diagnostic process. Not performing surgery when indicated seems to be associated with higher mortality rates. However, each patient’s operability must always be taken into account. For patients with PVE with small vegetations, there should be a low threshold for surgery because these patients seem to be prone to short-term endocarditis relapse.
Data Sharing Statement
References
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Data Sharing Statement