Abstract
In this study, we aimed to analyze the annual, age- and sex-specific frequencies and antifungal resistance rates of Candida albicans infections over an 11-year period (2013 − 2023) at a university hospital in South Chungcheong Province, South Korea. A total of 476 cases identified as C. albicans from 260,769 blood cultures were analyzed retrospectively. The annual number of C. albicans isolates increased by 161.1% in 2019 and 136.7% in 2022 compared with that in the previous year. The mean age of patients from whom C. albicans was isolated was 65.8 years, with 51.8% patients being aged 60–79 years. The number of isolates was higher in male patients than in female patients (male-to-female ratio: 1.4:1). Of the isolates, 6.6% were resistant to flucytosine and 4.5% were resistant to voriconazole, whereas all isolates were susceptible to caspofungin and micafungin. Overall, this study provides vital foundational data for tertiary general hospitals in the Chungcheong region and for developing national infection management strategies, thereby providing a valuable basis for future in-depth studies.
Keywords: Antifungal susceptibility, bloodstream infection, Candida albicans, candidemia
1. Introduction
Bloodstream infections (BSIs) are serious infections with a mortality rate of 20–30% [1]. The increase in the number of older patients and those with weakened immune systems owing to organ transplants, chemotherapy, and radiation therapy has led to an increased incidence of opportunistic infections and severe sepsis caused by bacterial species previously considered nonpathogenic [2]. In South Korea, the number of patients with sepsis increased by 14.9% in 2022 compared with that in 2018 [3]. Additionally, national mortality statistics show that the death rate from sepsis increased by 218.0% in 2022 compared with that in 2012 [4].
Candidemia, a fungal BSI, is a major contributor to increased morbidity and mortality [5]. A survey conducted by the Korea Disease Control and Prevention Agency from 2020 to 2022 revealed a steady annual increase in the isolation of Candida spp. from blood cultures [6].
Fluconazole has few side effects, is easy to administer, and is widely used to treat candidemia [7]. However, its extensive use has led to increased resistance among Candida spp., raising concerns regarding changes in susceptibility to azole antifungal agents [8,9]. The inappropriate use of antibiotics during BSI treatment or delayed treatment worsens patient outcomes, making it essential to select appropriate antifungal agents and initiate treatment early based on the specific Candida species [10,11].
Despite significant advances in antifungal therapy, candidemia continues to have an overall mortality rate of approximately 60% [12]. The increase in BSIs has led to an increase in the number of blood cultures performed. In bacterial BSIs, the distribution of species isolated from blood cultures and patterns of antibiotic susceptibility exhibit temporal and regional differences [13]. Therefore, regular epidemiological surveys on BSIs caused by fungi, monitoring of species distribution and antifungal susceptibility patterns, and control of emergence of new resistant strains are crucial for the appropriate selection of antimicrobials in clinical settings and development of appropriate diagnostic and treatment strategies. Accordingly, data on Candida species isolated from blood and antifungal susceptibility testing provide crucial information for developing empirical treatment guidelines for candidemia and antifungal therapy [9,14].
In this study, we aimed to analyze the annual, age- and sex-specific isolation frequencies and antifungal resistance rates of Candida albicans isolated from blood cultures over an 11-year period (2013–2023) in patients treated at a tertiary university hospital in the Chungcheong region of South Korea. The findings provide essential data to guide fungal infection control and antifungal stewardship policies, potentially contributing to the development of hospital and public health policies, thereby enhancing patient treatment and strengthening public health.
2. Materials and methods
2.1. Study participants
In this study, we analyzed cases of C. albicans fungemia isolated from 260,769 blood culture samples submitted to the Department of Laboratory Medicine at Dankook University Hospital between 2013 and 2023. If the same C. albicans strain was isolated multiple times in blood cultures from the same patient within a month, only the first isolate was included in the analysis. However, if the same strain was isolated from a patient more than a month apart, it was classified as a new case of C. albicans candidemia. After identifying the clinical isolates and conducting antifungal susceptibility testing, a retrospective study was performed using electronic health record data. This retrospective study was conducted in accordance with the principles of the Declaration of Helsinki with approval from the Institutional Review Board of Dankook University (IRB No. 2024-06-010-002). The requirement for informed consent was waived owing to the retrospective study design.
2.2. Blood culture, fungal identification, and antifungal susceptibility testing
Each blood culture test was counted as one set comprising both aerobic and anaerobic media. Blood culture bottles inoculated with aerobic (bioMérieux Plus Aerobic/F medium) or anaerobic (bioMérieux Plus Anaerobic/F medium) media were incubated at 35–37 °C for 5 d using the Bact/Alert 3D system (bioMérieux, Marcy L’Etoile, France).
For blood culture bottles testing positive, Gram staining was performed to identify yeast-like microorganisms. Specimens showing budding yeast cells were subcultured onto Sabouraud dextrose agar (SDA) and blood agar plates and then incubated at 36 °C for 16–48 h. Candida spp. were identified based on colony morphology, growth rate, and colony surface texture.
Identification of C. albicans was performed using the Vitek II system (bioMérieux) with YST ID cards according to the manufacturer’s instructions. If automatic identification results were inconclusive, high-precision species identification was performed using the VITEK-MS system (bioMérieux).
2.3. Antifungal susceptibility testing
Antifungal susceptibility testing was performed using YST ID cards on the VITEK-2 system (bioMérieux) according to the manufacturer’s instructions. Susceptibility interpretations followed the Clinical and Laboratory Standards Institute (CLSI) M60 guidelines [15].
Minimum inhibitory concentration (MIC) breakpoints for caspofungin, fluconazole, micafungin, and voriconazole were interpreted according to the CLSI M60 guidelines [15]. For flucytosine, breakpoints were interpreted based on the CLSI M27-A2 recommendations [16]. Since the CLSI guidelines do not provide breakpoints for amphotericin B, the European Committee on Antimicrobial Susceptibility Testing (EUCAST) guidelines were used [17]. Breakpoints for individual isolates are presented in Table 1.
Table 1.
Interpretation guidelines for antifungal susceptibility tests of Candida albicans.
| Organisms | Antifungal agent | MIC range (μg/mL) |
Source | |||
|---|---|---|---|---|---|---|
| S | I | SDD | R | |||
| Candida albicans | Amphotericin B | ≤1 | – | – | >1 | EUCAST |
| Caspofungin | ≤0.25 | 0.5 | – | ≥1 | CLSI | |
| Flucytosine | ≤4 | 8–16 | – | ≥32 | CLSI | |
| Fluconazole | ≤2 | – | 4 | ≥8 | CLSI | |
| Micafungin | ≤0.25 | 0.5 | – | ≥1 | CLSI | |
| Voriconazole | ≤0.12 | 0.25–0.5 | ≥1 | CLSI | ||
I: intermediate; MIC: minimal inhibitory concentration; R: resistant; S: susceptible; SDD: susceptible dose dependent; CLSI: Clinical and Laboratory Standards Institute; EUCAST: European committee on antimicrobial susceptibility
2.4. Statistical analysis
The culture results (percentages) and antifungal resistance rates were calculated using Excel (Microsoft, Redmond, WA). Statistical analyses were performed using SPSS version 28.0 (IBM Corp., Armonk, NY).
3. Results
3.1. Analysis of blood culture cases and positivity rates
The number of blood cultures requested increased annually over the 11-year study period from 2013 to 2023, except in 2020, in which the number of cultures decreased followed by a subsequent rise. In total, 260,769 blood cultures were conducted, with 18,216 testing positive, a 7.0% positivity rate. Among the positive blood cultures, fungi were isolated in 1282 samples, an isolation rate of 8.2%. Of these fungal-positive cultures, Candida spp. were isolated in 1257 samples from 412 patients, of which 476 samples from 139 patients were identified as C. albicans (Table 2).
Table 2.
Data on the number of positive cases in blood cultures and positivity rates for fungi and Candida albicans from 2013 to 2023.
| Year | No. of blood cultures | No. of positive cultures (%) | No. (%) of cultures positive for fungi |
No. of cultures positive for C. albicans |
No. of patients positive for C. albicans |
|---|---|---|---|---|---|
| 2013 | 17,896 | 1442 (8.1) | 97 (6.7) | 67 | 14 |
| 2014 | 20,235 | 1366 (6.8) | 124 (9.1) | 30 | 8 |
| 2015 | 21,030 | 1388 (6.6) | 120 (8.6) | 44 | 14 |
| 2016 | 23,934 | 1632 (6.8) | 142 (8.7) | 59 | 18 |
| 2017 | 24,296 | 1600 (6.6) | 102 (6.4) | 30 | 8 |
| 2018 | 25,640 | 1461 (5.7) | 75 (5.1) | 18 | 10 |
| 2019 | 27,937 | 1878 (6.7) | 105 (5.6) | 47 | 14 |
| 2020 | 22,962 | 1592 (6.9) | 68 (4.3) | 26 | 7 |
| 2021 | 23,113 | 1786 (7.7) | 153 (8.6) | 30 | 7 |
| 2022 | 26,005 | 1864 (7.2) | 133 (7.1) | 71 | 21 |
| 2023 | 27,721 | 2207 (8.0) | 163 (7.4) | 54 | 18 |
| Total | 260,769 | 18,216 (7.0) | 1,282 (7.0) | 476 | 139 |
The years 2019 and 2022 exhibited the most significant increases in C. albicans cases compared with the previous year, with substantial growth rates of 161.1% and 136.7%, respectively. During the study period (2013–2023), the average annual growth rate of C. albicans cases was 18.1%. The highest year-to-year increase in the number of C. albicans isolates was from 2021 to 2022 (200.0% increase) and from 2014 to 2015 (75.0% increase), whereas the largest year-to-year decrease was from 2016 to 2017 (55.6% decrease). The mean annual increase in the number of C. albicans-positive patients during the study period was 20.6%.
3.2. Frequency of C. albicans isolation by age and sex
The mean age of patients from whom C. albicans was isolated over the 11-year study period was 65.8 years. Patients aged 60 − 79 years accounted for the highest number of positive cases, with 36 cases each in the 60 − 69 and 70 − 79 years age groups, collectively comprising 51.8% of the total. This was followed by patients aged ≥80 years, those aged 50 − 59 years, and those aged 40 − 49 years. Male patients accounted for a higher proportion of C. albicans BSI cases (58.3%) than female patients (41.7%), with a male-to-female ratio of 1.4:1. Furthermore, male patients outnumbered female patients in all age groups except for the 70 − 79 and ≥80 years age groups. In the 70 − 79 years age group, the number of male and female patients was equal (18 isolates each), whereas in the ≥80 years age group, the number of isolates was higher in female (n = 15) than in male patients (n = 14; Figure 1).
Figure 1.
Number of patients with positive Candida albicans blood cultures by sex and age group from 2013 to 2023. p < 0.001 for the difference in the number of patients with C. albicans bloodstream infection by sex.
3.3. Antifungal resistance rates of C. albicans
Analysis of antifungal resistance rates for C. albicans over the 11-year period revealed that the resistance rate was the highest for flucytosine (6.6%), followed by voriconazole (4.5%), fluconazole (2.9%), and amphotericin B (2.4%). No caspofungin- or micafungin-resistant strains were detected (Figure 2).
Figure 2.
Antifungal resistance rates of Candida albicans from 2013 to 2023. AB: amphotericin B, CAS: caspofungin, FCT: flucytosine, FLU: fluconazole, MCF: micafungin, VRC: voriconazole.
3.4. Number of blood culture specimens received and C. albicans-positive cases by age group
The number of blood culture specimens and C. albicans-positive specimens collected from January 2013 to August 2023 were analyzed by age group. The age group with the highest number of blood culture specimens was 70–79 years (52,465 cases), followed by the 60–69 and ≥80 years age groups. A total of 250,949 blood culture specimens were received, with patients aged ≥60 years accounting for 54.5% of the total. Among patients aged under 60 years, infants aged <1 year constituted the highest number of specimens (22,821 cases), accounting for 20.0% of the specimens in the under-60 age group (Table 3).
Table 3.
Number of blood culture samples received and positive Candida albicans cases by age group.
| Age (years) |
Number of blood culture specimens received from Jan 2013 to Aug 2023 | Number (%) of C. albicans isolates from Jan 2013 to Aug 2023 |
|---|---|---|
| <1 | 22,821 | 8 (0.04) |
| 1–9 | 9128 | 0 (0) |
| 10–19 | 6579 | 2 (0.03) |
| 20–29 | 8612 | 0 (0) |
| 30–39 | 12,283 | 6 (0.05) |
| 40–49 | 20,706 | 34 (0.16) |
| 50–59 | 34,062 | 71 (0.21) |
| 60–69 | 42,341 | 133 (0.31) |
| 70–79 | 52,465 | 100 (0.19) |
| >80 | 41,952 | 97 (0.23) |
| Total | 250,949 | 451 (0.18) |
p < 0.001 for the difference in the C. albicans positivity rate by age.
The age group with the highest number of C. albicans-positive cases was 60–69 years, followed by the 70–79 and ≥80 years age groups. In total, 330 C. albicans-positive cultures were isolated from patients aged 60 years and older, representing 73.2% of the 451 total isolates. Additionally, the 451 C. albicans isolates accounted for 0.18% of the total number of culture samples received.
4. Discussion
Performing blood cultures to diagnose infectious diseases is a primary function of clinical microbiology laboratories, and the demand for blood cultures continues to increase. Therefore, to effectively treat patients with BSIs, it is important to understand the distribution of pathogens commonly isolated in blood cultures of hospitalized patients, along with their antibiotic susceptibility profiles. Determining the incidence of fungal diseases is challenging because they present with nonspecific symptoms and are not commonly suspected in general clinical practice. Given that the causative agents of BSIs and antimicrobial susceptibility results can vary by region, it is essential to regularly analyze the types of microorganisms isolated in blood cultures and the trends in antimicrobial susceptibility at each hospital so that clinicians can make appropriate choices of antimicrobial agents when developing treatment plans [18].
During the study period from 2013 to 2023, blood culture results from a tertiary medical institution in central South Korea exhibited a steady increase, except for 2020. In a study by Hwang et al. [19], the number of blood culture samples submitted to the diagnostic laboratory increased annually from 2009 to 2018. Although the blood culture positivity rate in the study by Hwang et al. was 0.6% higher, and the fungal positivity rate was 6.4%, which was lower than that observed in this study. In 2020, when COVID-19 was prevalent in South Korea, the number of blood cultures requested decreased. A study by Lee [20], analyzing the distribution patterns of bacteria in blood cultures before and after the COVID-19 pandemic, revealed that the total number of blood cultures requested decreased by 36.28% after COVID-19 compared with that before [20], which the authors attributed to factors such as a fear of COVID-19, regional movement restrictions, and restrictions on hospital visits leading to a decrease in both inpatient and outpatient numbers. Although the number of C. albicans specimens and patients fluctuated annually, there was a notable increase in 2022. This significant increase in the number of patients with positive blood cultures, as evidenced by data from the Health Insurance Review and Assessment Service (HIRA) [3] and the findings of this study, indicates a nationwide increase in patient numbers. In this study, C. albicans accounted for 37.1% of all positive fungal blood cultures, which is 7.3% higher than the proportion reported by Hwang et al. [19]. Given the high proportion of C. albicans in fungal blood cultures, regular surveillance is necessary.
The detection rate of C. albicans was the highest in male patients aged 60 years and older. These results are consistent with the findings reported by Hwang et al. [19], Kim et al. [21], and Shin et al. [22].
According to a report by the US Centers for Disease Control and Prevention (CDC), the annual incidence of fungal BSIs caused by Candida spp. is the highest among individuals aged 65 years and older and more common in male patients than in female patients [23]. In this study, the number of cases among patients aged 80 years and older was lower than that among patients aged 60–69 and 70–79 years. Based on data from the Korean Statistical Information Service (KOSIS), the life expectancy in South Korea was 82.7 years in 2022. Given the relatively smaller population of individuals aged 80 years and older, it is likely that the lower number of patients in this age group can be attributed to the limited number of individuals in the age group in the general population [24].
In antifungal susceptibility testing of C. albicans, flucytosine exhibited the highest resistance rate (6.6%). Khan et al. [25] reported a fluconazole resistance rate of 0.8% among C. albicans isolates from 371 patients between 2006 and 2011; however, in this study, the fluconazole resistance rate was 2.9%, indicating a gradual increase in fluconazole resistance over time. Additionally, Kim et al. [21] did not observe fluconazole resistance in clinical C. albicans isolates before 2013; however, since 2013, fluconazole- and azole-resistant strains have been continuously isolated. This is attributable to the low toxicity and easy administration of fluconazole; therefore, it is widely used globally for treating Candida BSIs [7]. The emergence of fluconazole resistance among Candida spp. should be monitored.
Voriconazole, the antifungal agent with the second-highest resistance rate, is effective in treating infections caused by C. albicans strains that are resistant to fluconazole and itraconazole. However, it has been suggested that the increased use of voriconazole may lead to a rise in voriconazole-resistant C. albicans [26]. In this study, the voriconazole resistance rate was 4.5%, which is lower than the 6.0% reported in other studies; however, given the potential for voriconazole resistance to increase, careful monitoring is warranted [26].
According to the Global Antimicrobial Resistance Surveillance System in Korea (Kor-GLASS), which conducts national surveys on antimicrobial resistance in South Korea, the number of BSIs caused by Candida spp. has been increasing annually, and the proportion of strains that are resistant to antifungal drugs, such as fluconazole, voriconazole, and caspofungin, increased from 2020 to 2022 [6]. Additionally, a study conducted in the United States from 2008 to 2013 by Cleveland et al. [27] revealed a significant increase in the population-based incidence of Candida BSIs in two major cities during the study period, along with an increased incidence of multidrug-resistant infections. To address the overuse of antifungal agents and the emergence of resistant strains, it is necessary to not rely solely on Kor-GLASS, which conducts antimicrobial resistance surveys domestically but to introduce an antimicrobial stewardship program, such as those successfully implemented in the United States and the United Kingdom, to strengthen the management of antimicrobial use.
Referring to age-specific data on sepsis claims from 2019 to 2023 provided by HIRA, the highest number of claims was from patients aged 80 years and older, followed by those aged 70–70 and 60–69 years [28]. Furthermore, HIRA reports that individuals aged 60 years and older account for 72.8% of sepsis claims. Although this differs slightly from the distribution of age-specific specimen rates found in this study, our data demonstrate that 73.2% of C. albicans-positive BSI cases were in patients aged ≥60 years, indicating a similar trend of higher prevalence in older age groups. This can be attributed to the higher incidence of chronic conditions such as obesity, diabetes, and HIV in older individuals, which increase their susceptibility to sepsis, particularly owing to chronic diseases related to the kidneys and respiratory system [29]. In addition, older adults are more frequently exposed to factors that favor candidemia, such as prolonged hospitalization, antibiotic therapy, use of intravenous catheters, diabetes, and malignant tumors [30], than younger individuals.
In patients younger than 60 years of age, the highest number of blood culture requests was among infants aged under 1 year. Although the causes of sepsis can vary depending on the timing, a high proportion of these cases are likely to have been due to neonatal sepsis, caused by exposure to medical equipment or new environments immediately after birth. The conditions in the neonatal unit and the health status of both the mother and the fetus contribute to the higher number of cases during the neonatal period.
Owing to the retrospective nature of this study, we were unable to consider the clinical details of patients, including antifungal treatment, or their demographic characteristics. Therefore, future research should focus on investigating the history of antimicrobial and antifungal use and analyzing molecular, genetic, and epidemiological characteristics in patients with antifungal resistance. This would aid in understanding the patterns of antifungal resistance and identifying infection pathways. Additionally, it is desirable to expand the scope of our research to include non-C. albicans species and conduct further studies to investigate the epidemiological changes in Candida spp. in BSIs over the 11-year period.
In summary, we analyzed the results of 260,769 blood cultures performed in our hospital from 2013 to 2023, providing a comprehensive understanding of C. albicans BSIs and antifungal resistance. The findings from our analysis of the distribution patterns of positivity rates according to sex, age, and year provide a sound basis for reevaluating diagnostic and treatment strategies. Additionally, we aim to continuously monitor the use of antimicrobial and antifungal agents through systematic and ongoing hospital infection management and operational surveillance systems, utilizing these data as a foundation for managing resistance and establishing appropriate antimicrobial prescription guidelines. The findings of this study can serve as a crucial foundation not only for tertiary general hospitals in the Chungcheong region but also for developing national infection control strategies, offering a valuable basis for future in-depth research.
Institutional review board statement
This study was conducted in accordance with the Declaration of Helsinki and approved by the Institutional Review Board at Dankook University (IRB No. 2024-06-010-002).
Informed consent statement
Since this study involved analysis of retrospective data, the requirement for informed consent was waived. Additionally, because all personal identifiers were removed during data collection, there was no risk for or harm to the sample donors.
Author contributions
Conceptualization, J.K.K.; funding acquisition, J.K.K.; formal analysis and investigation, K.Y.K.; writing – original draft preparation, K.Y.K. and G.Y.K.; writing – review and editing, J.K.K., K.K.L., and G.Y.K.; resources, J.K.K.; material preparation and data collection, K.Y.K. All authors commented on previous versions of the manuscript. K.Y.K and G.Y.K contributed equally to this work as co-first authors. All authors have read and agreed to the published version of the manuscript.
Disclosure statement
The authors declare no conflicts of interest.
Data availability statement
The original contributions presented in the study are included in the article; further inquiries can be directed to the corresponding author.
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Associated Data
This section collects any data citations, data availability statements, or supplementary materials included in this article.
Data Availability Statement
The original contributions presented in the study are included in the article; further inquiries can be directed to the corresponding author.