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Comparison of bloodstream infections due to Corynebacterium striatum, MRSA, and MRSE

BMC Infectious Diseases volume 24, Article number: 988 (2024) Cite this article

Abstract

Background

Corynebacterium striatum (C. striatum), a common skin and mucosal colonizer, is increasingly considered as an opportunistic pathogen causing bloodstream infections (BSIs). This study aims to investigate the clinical features and outcomes of C. striatum-BSI.

Methods

We included hospitalized cases with C. striatum-positive blood cultures from January 2014 to June 2022 and classified them into C. striatum-BSI group and contamination group; Clinical characteristics, treatments, and outcomes were compared between the C. striatum-BSI group and contamination group, Methicillin-resistant Staphylococcus aureus (MRSA)-BSI and Methicillin-resistant Staphylococcus epidermidis (MRSE)-BSI.

Results

Fifty-three patients with positive C. striatum blood cultures were identified. Among them, 25 patients were classified as C. striatum-BSI, with 21 as contamination cases. And 62 cases of MRSA-BSI and 44 cases of MRSE-BSI were identified. Compared to the contaminated group, the C. striatum-BSI group had a shorter time to positivity of blood cultures (27.0 h vs. 42.5 h, P = 0.011). C. striatum-BSI group had a longer time to positivity (27 h) when compared to both the MRSA (20 h) and MRSE groups (19 h) (p < 0.05). Appropriate therapy within 24 h of BSI onset was significantly lower in the C. striatum group (28%) compared to the MRSA (64.5%) and MRSE (65.9%) groups (p < 0.005). The 28-day mortality was higher in the C. striatum group (52.0%) compared to the MRSA (25.8%) and MRSE (18.2%) groups. 

Conclusions

Given the distinct characteristics of C. striatum-BSI, including a longer time to positivity than other Gram-positive bacteria and higher mortality rates, we suggest prescribing early appropriate antibiotics if C. striatum-BSI is suspected.

Peer Review reports

Background

Corynebacterium striatum (C. striatum), like Staphylococcus epidermidis, is a commensal organism of normal human skin and mucosal membranes [1,2,3]. Historically, C. striatum has been regarded by clinicians as a contaminant in blood cultures [4]. Increasingly, it is being recognized as a potential pathogen that can cause a variety of infections in both immunocompromised and immunocompetent hosts [5,6,7]. Furthermore, C. striatum frequently exhibits multidrug resistance, resulting in empirical antibiotic treatment failure [2, 8]. Among the true infections, bloodstream infections (BSIs) have been associated with significant mortality and morbidity up to 34% [9, 10].

Current literature on this topic primarily consisted of case reports or case series describing infections at various sites instead of solely focusing on bloodstream infections [11,12,13,14]. In addition, previous studies have mainly delineated the microbiological characteristics and resistance profiles of C. striatum infections [15, 16], with limited data available on the clinical features and prognosis in real-world clinical settings.

When C. striatum is isolated from blood cultures, this finding is usually considered contamination rather than a true infectious pathogen. Clinicians have limited knowledge about positive C. striatum blood cultures, including the time to positivity and the usage of antibiotics. The aim of this study was to investigate the clinical characteristics, treatments and outcomes of C. striatum BSIs. We compared C. striatum BSIs with Methicillin-resistant Staphylococcus aureus (MRSA) BSIs and Methicillin-resistant Staphylococcus epidermidis (MRSE) BSIs since they are also common skin commensals with similar antibiotic susceptibilities. We aimed to improve the understanding of bloodstream infection caused by this organism and assist clinicians in making clinical decisions.

Methods

Study population and design

A retrospective study of adult hospitalized patients with blood cultures positive for C. striatum was conducted at Peking Union Medical College Hospital, a tertiary-care hospital in Beijing, China, between January 2014 and June 2022. A blood culture set consists of one aerobic and one anaerobic blood culture bottle; the amount of blood drawn from patients was about 8 ml (see Supplemental file 1). Coinfection was excluded from the study.

Using electronic medical records, the following data were collected: demographic characteristics, underlying diseases, immunosuppressive status, source of BSI, laboratory tests on the onset of BSI, organ support therapies, antimicrobial therapies, survival time, and outcomes within 28 days from onset of BSI. Charlson comorbidity index score and Pitt bacteremia score were calculated as previous researches [17]. Two qualified physicians looked over patients’ medical records to guarantee data consistency.

This study was approved by the Research Ethics Committee of Peking Union Medical College Hospital (PUMCH, K23C1014). As the study was no-interventional and retrospective in nature with anonymized data, the written informed consent and informed consent had been waived.

Definitions

The contaminant group was defined as only one blood culture set that turned positive. Bacteremia was defined as if at least two blood culture sets taken at the same time turned out positive for the same species or when one blood culture specimen and another clinically relevant sample taken from another site yielded positive results. This criteria was applied to C. striatum-BSI and MRSE groups due to their characteristics of common skin contaminant [18, 19]. For the MRSA group, patients were categorized as BSI if at least one blood culture set turned out positive. Coinfection was defined as a C. striatum-BSI (or MRSE-BSI or MRSA-BSI) with positive blood culture for mixed organisms (bacterial, mycobacterial, or fungal) at the same time.

The onset of BSI was defined as the date of collection of the first blood culture yielded index pathogen. Nosocomial and Intensive care unit (ICU) BSI was defined as the occurrence of BSI in 48 h or more after admission [20]. Neutropenia was defined as an absolute neutrophil count lower than 500/ml at the onset of BSI. Immunosuppressive therapy was defined as a daily dose of ≥ 10 mg prednisolone-equivalent steroids, monoclonal antibodies, antimetabolite drugs, or T-cell inhibitors within 30 days before BSI onset. The source of BSI was determined based on an active infection site, and the isolation of the organism from that site coincided with the onset of BSI. The unknown source of infection was BSIs without positive cultures of other body fluids or swab specimens during this infection. Antimicrobial therapy was considered appropriate if at least one active antimicrobial agent, determined by in vitro susceptibility testing, was administered within 24 h after the onset.

Identification and antibiotic susceptibility testing of Corynebacterium striatum

C. striatum was identified by matrix-assisted laser desorption/ionization time-of-flight mass spectrometry (MALDI-TOF MS). Drug susceptibility testing was conducted using the broth microdilution method according to the Clinical and Laboratory Standards Institute guidelines. The antibiotics tested were clindamycin, linezolid, levofloxacin, tigecycline, teicoplanin, penicillin, erythromycin, gentamicin, rifampicin, tetracycline, and vancomycin. For each antibiotic, six dilutions were performed including break points recommended by the CLSI standard and corresponding to the genus Corynebacterium according to the latest edition every year.

Statistical analysis

Data are presented as frequency and percentages for categorical variables and as mean ± standard deviation (SD) or median with interquartile range (IQR) for continuous variables. Categorical variables were compared using either the Chi-square test or Fisher's exact test, while continuous variables were compared using the Mann–Whitney U test. A p-value below 0.05 was considered statistically significant. Data were analyzed using SPSS version 21.0.1. Figures were designed using Prism version 9.0.

Results

Between January 2014 and June 2022, a total of 53 episodes for positive blood culture of C. striatum were detected, and 21 cases of these were contaminated and 32 patients were identified as C. striatum-BSI. At 32 cases of C. striatum infection, 7 cases of these were with coinfection of other microorganisms (Fig. 1). As for the control group, 62 patients with MRSA-BSI, and 44 patients with MRSE-BSI were identified based on the criteria (Fig. 1).

Fig. 1
figure 1

The study selection of flowchart

Full size image

Clinical characteristics of C. striatum-BSI group and contaminated group

As shown in Table 1, we observed no significant differences in gender, age, Charlson Comorbidity Index, and underlying health conditions between C. striatum-BSI and contaminated group. The time to positivity of blood culture in the contaminated group (42.5 h) was significantly longer (p = 0.011) than C. striatum-BSI group (27 h). C. striatum group was in more severe clinical condition according to Pitt bacteremia score (score of 5 vs 3 in median), septic shock (52.0% vs 33.3%), and usage of invasive mechanical ventilation (IMV) (64.0% vs 16.7%) than the contaminated group. The 28-day mortality was higher (p = 0.057) in C. striatum group (52%) than contaminated group(22.2%).

Table 1 Patient characteristics of the C. striatum-BSI group and contaminated group
Full size table

Clinical characteristics of patients with C. striatum-BSI

The main characteristics of C. striatum-BSI were in (Table 2). C. striatum-BSI occurred more frequently in males (70.0%), and the average age of patients was 60 years old. 56.0% of patients were nosocomial infections. The proportion of ICU infection was 20% in C. striatum-BSI, 16.1% in MRSA, and 13.6% in MRSE. It was found that the time to BSI onset from hospital admission was longer in C. striatum-BSI (14.0 days) than in MRSA (4.0 days) and MRSE groups (6.0 days). We also found that all groups mostly could not find infective sources (64% in C. striatum, 43.5% in MRSA, 47.7% in MRSE). As for sources that could be detected, the vascular catheter was the most common site in the C. striatum group (16.0%), as well as MRSE (31.8%), and the MRSA group was skin and soft tissue (22.6%). C. striatum group (4.0) had a higher (P = 0.007) Carlson Comorbidity Index compared to the MRSA group (2.0). The proportion of immunocompromised status was 60.0% without statistical difference compared to control groups.

Table 2 Clinical characteristics, treatment and outcome of C. striatum-BSI, MRSA-BSI and MRSE-BSI groups
Full size table

The C. striatum group (27.0 h) had a longer time to positivity of blood culture compared to MRSA (20.0 h, P = 0.002) and MRSE (19.0 h, P < 0.001) groups. Overall, the clinical condition of the C. striatum group (5.0) appeared to be more severe than other groups, as evidenced by a higher Pitt's score compared to the MRSA group (1.0, P < 0.001) and the MRSE group (1.0, P < 0.001). Additionally, the C. striatum group had normal WBC counts (8.9 X 109/L) but lower platelet counts (78.0 X 109/L) and a higher incidence of shock (52.0%) compared to control groups. The C. striatum group (64%) also had higher utilization of invasive mechanical ventilation than the MRSA (27.4%) and MRSE (25.0%) groups.

Antimicrobial therapy and outcomes of patients with C. striatum-BSI

As shown in Table 2, there was a significantly different proportion of appropriate therapy within 24 h in C. striatum-BSI (28.0%) compared to MRSA (64.5%) and MRSE (65.9%) groups (p < 0.05). Table 3 demonstrated the antibiotics susceptibility. C. striatum was mainly susceptible to linezolid, tigecycline, teicoplanin, and vancomycin, consistent with MRSA and MRSE. As shown in Fig. 2, 57.1% (4/7), 44.4% (4/9), and 42.8% (3/7) of patients of C. striatum-BSI were prescribed appropriate antibiotics within 24 h after blood culture turned to positivity in a different time to positivity of 0-24 h, 24-36 h, 36-48 h, respectively, which were all lower than MRSA group and MRSE group. The median time to therapy from BSI was two days in the C. striatum group, but 1.0 day in the MRSA and MRSE groups. The most frequently used antibiotics in all groups were vancomycin, accounting for more than half of the cases. No significant differences were observed between the groups using vancomycin, linezolid, or teicoplanin.

Table 3 Drug susceptibility results of C. striatum, MRSA, and MRSE group
Full size table
Fig. 2
figure 2

Initiation of appropriate treatment within 24h since positivle culture according to time to positivity

Full size image

We found the 28-day mortality and in-hospital mortality among the C. striatum group (52.0% and 56.0%, respectively) were higher than MRSA (25.8% and 27.4%, respectively) and MRSE (18.2% and 20.5%, respectively) groups, significant differences were observed in both comparisons.

Table 4 showed the factors associated with 28-day mortality in C. striatum-BSI, and septic shock was the univariable risk factor for mortality. The proportion of appropriate therapy within 24 h was 33.3% and 23.1% in survivors and non-survivors.

Table 4 Patient characteristics of survivors and non-survivors in C. striatum-BSI
Full size table

Discussion

We conducted a retrospective study among hospitalized patients with C. striatum-positive blood cultures, revealing a bacteremia rate of 60.4%(32/53) using a stringent diagnostic criteria. Among these confirmed bloodstream infections, C. striatum was mainly susceptible to vancomycin, linezolid, teicoplanin, and tigecycline. The proportion of C. striatum cases that received timely appropriate antibiotics was less than 30%, significantly lower compared to MRSA-BSI and MRSE-BSI, despite similar antibiotic susceptibility profiles. Furthermore, the observed 28-day mortality rate was 52%, notably higher than that of MRSA and MRSE.

C. striatum is commonly considered a contaminant in positive blood culture. Recent literature reported its contamination rates ranging from 29% to 42% [4, 6, 21]. Differences in these rates could be due to varying criteria used to ascertain contamination. Our observed contamination rate was 39.6% (21/53), relatively elevated, likely due to the adoption of more stringent criteria. This rate aligned with Yanai and colleagues’ study that applied the same criteria [10]. Patients identified as contaminants in our cohort had significantly longer time to positivity compared to the contaminated group (42.5h vs 27.0h) and displayed markedly lower 28-day mortality rates as well (52.0% vs 22.2%). These findings collectively support the precision in identifying this cohort of contaminated patients.

As for C. striatum BSIs, patients with immunocompromised status were 60%. This was accordant with Ishiwada and colleagues’ study, which showed 54% of C. striatum BSIs were under malignancy, and this rate was 46.4% in Yanai and colleagues’ research [10, 15]. Abe and colleagues’ research identified 147 cases of Corynebacterium bacteremia in patients with hematological disorders [5]. In our study, 64% of C. striatum-BSIs had no primary source of infection, which was slightly higher than the 40–53% reported in previous studies [9, 15]. This high proportion was reliable because we applied strict criteria for C. striatum-BSI with unknown origin, requiring two sets of positive blood cultures from different sites at the same time. Furthermore, since these patients presented with symptoms of infection, comprehensive screening for infection foci was conducted at the time of blood culture collection following the standard protocol. This result reflected the difficulty in identifying the primary infection sites for C. striatum-BSI and suggested that cases with C. striatum positive blood cultures but without definitive primary infection sites should be took into account to C. striatum-BSIs when patients had compatible clinical symptoms and had undergone comprehensive infection focus screening. The most common primary infection site of C. striatum-BSIs was catheter-related in our study, accounting for 16%, consistent with similar proportions of 19% found in previous studies [9, 15]. In contrast, implants and skin/soft tissues were the most common primary infection sites for MRSE-BSIs and MRSA-BSIs, which were rational to their clinical characteristics [22, 23].

In our study, the average time to blood culture positivity for C. striatum BSI was 27 h, which was longer than that observed in the control groups of MRSE-BSI (19 h) and MRSA-BSI (20 h). This difference could be attributed to the high proportion of immuncompromsied pateints in the C. striatum BSI group, who were more susceptible to infections even at lower bacterial loads. Although a longer time to positivity often implies contamination, the likelihood of mistaking contamination for bacteremia is low due to our study’s stringent criteria for the diagnosis of C. striatum BSI. Additionally, similar findings were reported in the studies by Ishiwada and Watanabe [15, 21]. The prolonged time to positivity in C. striatum BSI may lead to the suspicion of contamination, resulting in delayed antibiotic usage [24], as demonstrated in this study.

Patients with C. striatum BSI experienced worse clinical outcomes. In recent years, some outbreaks of nosocomial infections of C. striatum were reported, particularly among patients with chronic diseases, exposure to broad-spectrum antibiotics and longtime stay in hospital [2, 25,26,27]. The mortality of C. striatum-BSI in this study was two times higher than control groups. Meanwhile, C. striatum-BSI had a higher incidence of shock and was more likely to require invasive mechanical ventilation. The reported mortality of C. striatum-BSI was approximately 34% [9], which was lower than the 56% observed in this study. The high mortality is attributed to multiple factors. Firstly, there is a high proportion of immunocompromised patients in C. striatum-BSI patients, facing a higher risk of poor outcomes [28, 29]. Secondly, unlike most MRSA-BSI and MRSE-BSI with known primary infection foci, a high proportion of C. striatum BSI did not have identifiable infection sites, which are recognized to be related to a higher risk of severe organ dysfunction and mortality [30]. Thirdly, high mortality was associated with only a 28% rate of early appropriate antibiotic therapy and a long time interval from the onset of BSI to the initiation of appropriate treatment. These findings may be partially due to several reasons. The longer time to positivity could delay the early prescription. However, regardless of the time to positivity, only 43–57% of C. striatum BSI received appropriate therapies. This indicated that clinicians should be more aware of C. striatum-BSI. Furthermore, C. striatum was a multidrug-resistant pathogen [31]. Previous studies have demonstrated that C. striatum was resistant to many common antibiotics, such as cephalosporins, and only susceptible to a few antibiotics, such as linezolid, vancomycin, and teicoplanin [32, 33], which could lead to a lower rate of appropriate empiric antibiotic therapy.

Our study has some limitations. Due to the lack of a generally accepted definition, we could not precisely distinguish between true BSI with C. striatum and contamination cases. We applied a stringent definition for C. striatum-BSIs, which may carry the potential risk of misclassifying actual infections as contaminations. Nevertheless, the notable difference in mortality and disease severity between these two groups supports the appropriateness of the definition used in this study. Secondly, the study was conducted retrospectively at a single center, which may limit the generalizability of the findings to other settings. The limited number of cases hindered our exploration of risk factors associated with the prognosis of C. striatum-BSI.

In conclusion, we found the rate of C. striatum bacteremia was 60.4% among the positive blood cultures for C. striatum. C. striatum bacteremia is more common in immunocompromised patients, with a low proportion of appropriate antibiotics and a high mortality. Clinicians should pay full attention to C. striatum bacteremia and not easily regard positive blood cultures of Gram-positive bacilli as contamination.

Availability of data and materials

The datasets generated during and/or analyzed during the current study are available from the corresponding author on reasonable request.

Abbreviations

C. striatum :

Corynebacterium striatum

BSIs:

Bloodstream infections

MRSA:

Methicillin-resistant Staphylococcus aureus

MRSE:

Methicillin-resistant Staphylococcus epidermidis

ICU:

Intensive care unit

IMV:

Invasive mechanical ventilation

COPD:

Chronic obstructer pulmonary disease

CRRT:

Continuous renal replacement therapy

WBC:

White blood cell

IQR:

Interquartile range

SD:

Standard deviation

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Acknowledgements

We thank our team at Medical Intensive Care Unit, Peking Union Medical College Hospital.

Funding

We acknowledge the support from.

1. National Key R&D Program of China from Ministry of Science and Technology of the People's Republic of China (2022YFC2304601, 2021YFC2500801) by Bin Du.

2. CAMS Innovation Fund for Medical Sciences (CIFMS) 2021-I2M-1–062 from Chinese Academy of Medical Sciences by Bin Du.

3. National High Level Hospital Clinical Research Funding(2022-PUMCH-D-005, 2022-PUMCH-D-111, 2022-PUMCH-B-126) by Bin Du.

4. National key clinical specialty construction projects from National Health Commission by Bin Du.

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Authors and Affiliations

  1. Medical Intensive Care Unit, State Key Laboratory of Complex Severe and Rare Diseases, Peking Union Medical College Hospital, Peking Union Medical College and Chinese Academy of Medical Sciences, 1 Shuai Fu Yuan, Beijing, 100730, China

    Shu-Hua He, Yan Chen, Shan Li, Shi-Tong Diao, Yi-Fan Wang, Zhuo-Xin He, Li Weng, Jin-Min Peng & Bin Du

  2. Department of Clinical Laboratory, Peking Union Medical College Hospital, Peking Union Medical College, Chinese Academy of Medical Sciences, Beijing, China

    Hong-Li Sun

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  3. Hong-Li Sun
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  4. Shan Li
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  5. Shi-Tong Diao
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  6. Yi-Fan Wang
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  7. Zhuo-Xin He
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  8. Li Weng
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  9. Jin-Min Peng
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  10. Bin Du
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Contributions

All authors contributed to the study conception and design. Material preparation, data collection and analysis were performed by Shu-hua He, Jin-min Peng and Bin Du. The first draft of the manuscript was written by Shu-hua He and Jin-min Peng, and all authors commented on previous versions of the manuscript. All authors read and approved the final manuscript.

Corresponding authors

Correspondence to Jin-Min Peng or Bin Du.

Ethics declarations

Ethics approval and consent to participate

This study was approved by the Research Ethics Committee of Peking Union Medical College Hospital (PUMCH, K23C1014). The Research Ethics Committee of Peking Union Medical College Hospital waived the requirement for informed consent owing to the non‑interventional, retrospective study design.

Consent for publication

Not applicable.

Competing interests

The authors declare no competing interests.

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He, SH., Chen, Y., Sun, HL. et al. Comparison of bloodstream infections due to Corynebacterium striatum, MRSA, and MRSE. BMC Infect Dis 24, 988 (2024). https://doi.org/10.1186/s12879-024-09883-z

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  • DOI: https://doi.org/10.1186/s12879-024-09883-z

Keywords

BMC Infectious Diseases

ISSN: 1471-2334

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