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Cited by 29Antifungal resistance and susceptibilityYeasts and Rust Fungi StudiesOcular Infections and Treatments

Distribution, trends, and antifungal susceptibility of Candida species causing candidemia in Japan, 2010–2019: A retrospective observational study based on national surveillance data

Open access
Kajihara, Toshiki, Yahara, Koji, Nagi, Minoru, Kitamura, Norikazu, Hirabayashi, Aki, Hosaka, Yumiko, Abe, Masahiro, Miyazaki, Yoshitsugu +1 more·2022·Medical Mycology
DOI 10.1093/mmy/myac071PMC PMC9521341
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Abstract

The increasing incidence of candidemia and the emergence of drug-resistant Candida species are major concerns worldwide. Therefore, long-term surveillance studies are required. Here, we provide one of the largest longitudinal overviews of the trends in the prevalence of Candida species using national data of 57 001 candidemia isolates obtained from > 2000 hospitals for the 2010–2019 period in the Japan Nosocomial Infections Surveillance database. The proportion of Candida species, except Candida krusei and Candida guilliermondii, was almost the same during the study period. The proportion of C. guilliermondii surpassed that of C. krusei in 2014. The incidence of candidemia due to C. albicans (P < 0.0001), C. parapsilosis (P = 0.0002), and C. tropicalis (P < 0.0001) have decreased significantly over this period. Azole susceptibility of C. tropicalis was low, with 17.8% of isolates resistant to fluconazole and 13.5% resistant to voriconazole. The micafungin susceptibility of C. glabrata was low, with 8.0% of isolates showing resistance. The resistance rate of C. krusei toward amphotericin B fluctuated considerably (between 3.2% and 35.7%) over this period. The incidence rate of candidemia caused by C. parapsilosis and C. guilliermondii in hospitals responsible for bone marrow transplantation was significantly higher than that in other hospitals. Overall, our study suggests that in Japan, the species distribution of Candida was almost the same in this period and similar to that reported in North America and Europe. A relatively high resistance to azoles and micafungin was observed in C. glabrata, C. tropicalis, and C. krusei isolates, which require continued surveillance.

AI snapshot

Written from the paper’s full text.

TL;DR

This retrospective national surveillance study of 57,001 candidemia isolates from >2000 Japanese hospitals found that Candida species distribution was largely stable from 2010–2019 and similar to North America/Europe. It also identified relatively high azole and micafungin resistance in C. tropicalis, C. glabrata, and C. krusei, supporting continued surveillance.

Key findings

  • Among 57,001 isolates, C. albicans was most common at 43.6% (n=24,864), followed by C. glabrata 19.5% (n=11,107), C. parapsilosis 18.8% (n=10,764), C. tropicalis 6.7% (n=3,827), C. guilliermondii 1.7% (n=949), C. krusei 1.4% (n=817), and C. dublinensis 0.15% (n=82).
  • Incidence of candidemia due to C. albicans, C. parapsilosis, and C. tropicalis decreased significantly over 2010–2019 (18.2%, P<0.0001; 7.45%, P=0.0002; and 30.1%, P<0.0001, respectively), while C. dublinensis increased (P<0.0001).
  • In 2019, C. tropicalis showed low azole susceptibility, with 17.8% of isolates resistant to fluconazole and 13.5% resistant to voriconazole; C. glabrata micafungin resistance ranged from 8.0–17.8%, and C. krusei amphotericin B resistance fluctuated between 3.2% and 35.7%.
  • Hospitals responsible for bone marrow transplantation had significantly higher proportions of C. parapsilosis and C. guilliermondii than other hospitals (P=0.0072 and P<0.001, respectively), and higher candidemia incidence (872.2 vs. 779.9/100,000 patients who underwent blood culture testing).

Methods

  • Retrospective observational analysis of inpatient data from the Japan Nosocomial Infections Surveillance (JANIS) database, January 2010–December 2019, covering 57,001 Candida isolates from blood samples and 55,580 candidemia patients; 2,075 hospitals submitted data in 2019.
  • Species distribution and antifungal susceptibility were tabulated for fluconazole, voriconazole, and micafungin using CLSI M60 2017 criteria, and amphotericin B using EUCAST guidelines; deduplication followed the WHO GLASS algorithm.
  • Statistical comparisons used Pearson’s χ² or Fisher’s exact test, and trends used the Cochran–Armitage trend test with P<0.05; analyses were performed in R 4.0.5 and JMP Pro 13. Hospitals responsible for bone marrow transplantation (186 certified hospitals) were compared with other hospitals using 2019 data.

Limitations

  • The paper states that JANIS is a voluntary surveillance system, so the number of participating hospitals varies each year; it does not collect information on how species identification is performed, does not collect strains, and susceptibility testing is performed for only about 30% of isolates using different methods across hospitals.
  • The text makes evident that incidence was calculated using patients who underwent blood culture testing rather than population or hospital admissions, because admissions are not mandatory in JANIS.
  • The text also makes evident that some species had small isolate numbers, particularly C. krusei, limiting interpretation of resistance trends.

Model-written summary. Check it against the paper before relying on it.

Integrity signals

Registry

Crossref · 10.1093/mmy/myac071

Cites

30 of 30 references verified0 citation errors · 0 not checkable

Statistics

Nothing to recompute.

Claims the paper makes

0 of 48 cited sources checked · 0 supported · 0 flagged

  • Findingown data

    The incidence of candidemia due to Candida dublinensis increased significantly from 2010 to 2019 (P < 0.0001).

    “On the other hand, that due to C. dublinensis has increased (P < 0.0001).”
    Quote in the paperNot a substantial claim
  • Findingown data

    In 2019, 13.5% of Candida tropicalis isolates were resistant to voriconazole.

    “Azole susceptibility of C. tropicalis was low, with 17.8% of isolates resistant to fluconazole and 13.5% resistant to voriconazole.”
    • Also stated in: § Notable susceptibility patterns towards antifungal agents · plain
      “Azole susceptibility of C. tropicalis (yellow line) was low, with 17.8% of isolates resistant to FLCZ and 13.5% resistant to VRCZ in 2019.”
    Quote in the paperNot a substantial claim
  • Findingown data

    The distribution of Candida species isolated from candidemia patients in Japan during 2010-2019 was 43.6% C. albicans, 19.5% C. glabrata, 18.8% C. parapsilosis, 6.7% C. tropicalis, 1.4% C. krusei, 1.7% C. guilliermondii, 0.15% C. dublinensis, and 8.1% other.

    “The distribution of Candida species isolated from the patients was as follows (Table 1): 43.6% (n = 24 864) C. albicans, 19.5% (n = 11 107) C. glabrata, 18.8% (n = 10 764) C. parapsilosis, 6.7% (n = 3827) C. tropicalis, 1.4% (n = 817) C. krusei, 1.7% (n = 949) C. guilliermondii, 0.15% (n = 82) C. dublinensis, and 8.1% (n = 4591) other.”
    Quote in the paperSubstantial claim
  • Findingown data

    The micafungin resistance of Candida glabrata ranged from 8.0% to 17.8% over 2010-2019.

    “The micafungin susceptibility of C. glabrata was low, with 8.0% of isolates showing resistance.”
    • Also stated in: § Notable susceptibility patterns towards antifungal agents · plain
      “The MCFG resistance of C. glabrata was high, ranging from 8.0–17.8%.”
    Quote in the paperSubstantial claim
  • Findingown data

    The incidence of candidemia due to Candida parapsilosis decreased significantly from 2010 to 2019 (P = 0.0002).

    “The incidence of candidemia due to C. albicans (P < 0.0001), C. parapsilosis (P = 0.0002), and C. tropicalis (P < 0.0001) have decreased significantly over this period.”
    • Also stated in: § Trends and incidence of candidemia · plain
      “The incidence of candidemia due to C. albicans, C. parapsilosis, and C. tropicalis has decreased from 2010–2019, with decreases of 18.2% (P < 0.0001), 7.45% (P = 0.0002), and 30.1% (P < 0.0001), respectively.”
    Quote in the paperSubstantial claim
  • May combine two claims. 20
  • The quote only partly states this claim. 2
  • Classified as probably not a substantial claim. 21

  • May combine two claims.

    Findingown data

    In 2019, 0.085% of C. albicans, 0.56% of C. glabrata, 0.17% of C. parapsilosis, and 1.12% of C. tropicalis isolates were cross-resistant to fluconazole and micafungin.

    “In 2019, 0.085% of C. albicans, 0.56% of C. glabrata, 0.17% of C. parapsilosis, and 1.12% of C. tropicalis isolates were cross-resistant to FLCZ and MCFG.”
    Quote in the paperNot a substantial claim

  • May combine two claims.

    Findingown data

    The species-specific incidence over the entire study period was 364/100,000 for C. albicans, 163/100,000 for C. glabrata, 158/100,000 for C. parapsilosis, 56/100,000 for C. tropicalis, 12/100,000 for C. krusei, 14/100,000 for C. guilliermondii, and 1.2/100,000 for C. dublinensis.

    “The species-specific incidence was calculated for the entire study period, and blood cultures of 364/100 000 patients tested positive for C. albicans, 163/100 000 for C. glabrata, 158/100 000 for C. parapsilosis, 56/100 000 for C. tropicalis, 12/100 000 for C. krusei, 14/100 000 for C. guilliermondii, and 1.2/100 000 for C. dublinensis.”
    Quote in the paperSubstantial claim

  • The quote only partly states this claim.

    Findingown data

    The incidence rate of candidemia caused by Candida parapsilosis in hospitals responsible for bone marrow transplantation was significantly higher than in other hospitals (P = 0.0072).

    “The incidence rate of candidemia caused by C. parapsilosis and C. guilliermondii in hospitals responsible for bone marrow transplantation was significantly higher than that in other hospitals.”
    • Also stated in: § Comparison between hospitals responsible for bone marrow transplantation and other hospitals · plain
      “The proportion of C. parapsilosis and C. guilliermondii in hospitals responsible for bone marrow transplantation was significantly higher than that in other hospitals (P = 0.0072 and P < 0.001, respectively).”
    Quote in the paperSubstantial claim

  • The quote only partly states this claim.

    Findingown data

    The incidence rate of candidemia caused by Candida guilliermondii in hospitals responsible for bone marrow transplantation was significantly higher than in other hospitals (P < 0.001).

    “The incidence rate of candidemia caused by C. parapsilosis and C. guilliermondii in hospitals responsible for bone marrow transplantation was significantly higher than that in other hospitals.”
    • Also stated in: § Comparison between hospitals responsible for bone marrow transplantation and other hospitals · plain
      “The proportion of C. parapsilosis and C. guilliermondii in hospitals responsible for bone marrow transplantation was significantly higher than that in other hospitals (P = 0.0072 and P < 0.001, respectively).”
    Quote in the paperSubstantial claim

  • May combine two claims.

    Findingown data

    The overall incidence of candidemia over the 10 years was 0.83%, which was higher than the 0.58 ± 0.09% reported by Kakeya et al.

    “The overall incidence of candidemia over the 10 years was 0.83%, which was higher than that (0.58 ± 0.09%) reported by Kakeya, et al.”
    Quote in the paperNot a substantial claim0 of 1 sources checked
    • cites [11] Kakeya, 2018, [National trends in the distribution of candida species causing Candidemia in Japan from 2003 to 2014], Med. Mycol. J. source

      Not checked in the free run.

  • May combine two claims.

    Interpretationown data

    In Japan, the species distribution of Candida during 2010-2019 was almost the same and similar to that reported in North America and Europe.

    “Overall, our study suggests that in Japan, the species distribution of Candida was almost the same in this period and similar to that reported in North America and Europe.”
    • Also stated in: § Discussion · hedged
      “Overall, our study shows that the proportion of each Candida species isolated from candidemia cases in Japan is more similar to that in the US and Europe, than to the proportion in the Asia-Pacific region, which may be due to the differences in the climate.”
    Quote in the paperSubstantial claim0 of 2 sources checked
    • cites [20] Koehler, 2019, Morbidity and mortality of candidaemia in Europe: an epidemiologic meta-analysis, Clin. Microbiol. Infect. source

      Not checked in the free run.

    • cites [21] Chapman, 2017, Changing epidemiology of candidaemia in Australia, J. Antimicrob. Chemother. source

      Not checked in the free run.

  • Probably not a substantial claim: may not pass S3 (load-bearing). May combine two claims.

    Premisecitation

    In the US, the most common Candida species was C. albicans (38%), followed by C. glabrata (30%), C. parapsilosis (14%), and C. tropicalis (7%).

    “The most common Candida species was C. albicans (38%), followed by C. glabrata (30%), C. parapsilosis (14%), and C. tropicalis (7%).6”
    Quote in the paperNot a substantial claim0 of 1 sources checked
    • cites [6] Tsay, 2020, Burden of Candidemia in the United States, 2017, Clin. Infect. Dis.

      Not checked in the free run.

  • Probably not a substantial claim: may not pass S3 (load-bearing). May combine two claims.

    Study design and conductnone given

    Drug susceptibility tests are conducted only for approximately 30% of the strains isolated in hospitals, and different methods of antifungal susceptibility testing are used by these hospitals.

    “Fourth, drug susceptibility tests are conducted only for approximately 30% of the strains isolated in the hospitals, and different methods of antifungal susceptibility testing are used by these hospitals.”
    Quote in the paperNot a substantial claim
    • Rests on an assumption: The tested subset of isolates is representative of all isolates for antifungal susceptibility.

  • May combine two claims.

    Interpretationcitation

    The resistance of Candida glabrata to micafungin might be higher in Japan than in other countries because micafungin is more frequently prescribed in Japan.

    “The resistance of C. glabrata to MCFG might be higher in Japan than in other countries because MCFG, which was developed in Japan,28 is more frequently prescribed in Japan.”
    Quote in the paperNot a substantial claim0 of 1 sources checked
    • cites [28] Higashiyama, 2004, Micafungin: a therapeutic review, Expert Rev. Anti Infect. Ther. source

      Not checked in the free run.

  • Probably not a substantial claim: may not pass S3 (load-bearing). May combine two claims.

    Study design and conductreasoning

    JANIS is a voluntary surveillance system, and the number of participating hospitals varies each year.

    “First, the JANIS is a voluntary surveillance. Therefore, the number of participating hospitals varies each year.”
    Quote in the paperNot a substantial claim

  • Probably not a substantial claim: may not pass S3 (load-bearing).

    Study design and conductnone given

    JANIS has not been collecting information about how species identification is conducted in each hospital.

    “Second, JANIS has not been collecting information about how species identification is conducted in each hospital.”
    Quote in the paperNot a substantial claim

  • Probably not a substantial claim: may not pass S3 (load-bearing). May combine two claims.

    Premisecitation

    In Latin America, the most common Candida species were C. albicans (37.6%), C. parapsilosis (26.5%), and C. tropicalis (17.6%), whereas C. glabrata was low.

    “The most common Candida species in this study were C. albicans (37.6%), C. parapsilosis (26.5%), and C. tropicalis (17.6%), whereas the distribution of C. glabrata was low.7”
    Quote in the paperNot a substantial claim0 of 1 sources checked
    • cites [7] Nucci, 2013, Epidemiology of candidemia in Latin America: a laboratory-based survey, PLoS One source

      Not checked in the free run.

  • Classified as probably not a substantial claim. May combine two claims.

    Study design and conductnone given

    JANIS has not been collecting strains, but has collected data on species, specimen, and antifungal susceptibility reported by participating hospitals.

    “Third, JANIS has not been collecting strains, but has collected data on species, specimen, and antifungal susceptibility reported by the participating hospitals.”
    Quote in the paperSubstantial claim

  • Probably not a substantial claim: may not pass S3 (load-bearing).

    Premisecitation

    In China, the most common Candida species were C. albicans (32.9%), C. parapsilosis (27.1%), C. tropicalis (18.7%), and C. glabrata (12.0%).

    “The most common Candida species among them was C. albicans (32.9%), followed by C. parapsilosis (27.1%), C. tropicalis (18.7%), and C. glabrata (12.0%).8”
    Quote in the paperNot a substantial claim0 of 1 sources checked
    • cites [8] Xiao, 2020, Distribution and antifungal susceptibility of candida species causing candidemia in China: an update from the CHIF-NET study, J. Infect. Dis. source

      Not checked in the free run.

  • Probably not a substantial claim: may not pass S3 (load-bearing). May combine two claims.

    Premisecitation

    In Japan, a national surveillance spanning 105 hospitals reported data for a single year, 2002.

    “In Japan, a national surveillance, which spanned 105 participating hospitals, reported data for a single year, 2002.10”
    Quote in the paperNot a substantial claim0 of 1 sources checked
    • cites [10] Takakura, 2004, National surveillance of species distribution in blood isolates of candida species in Japan and their susceptibility to six antifungal agents including voriconazole and micafungin, J. Antimicrob. Chemother. source

      Not checked in the free run.

  • May combine two claims.

    Interpretationcitation

    The Chinese results were considerably different from the present study: C. albicans was 10% lower, while C. parapsilosis and C. tropicalis were 10% higher.

    “These results were considerably different from our results as the proportion of isolated C. albicans was 10% lower, whereas that of isolated C. parapsilosis and C. tropicalis was 10% higher compared with that observed in our study.”
    Quote in the paperNot a substantial claim0 of 1 sources checked
    • cites [8] Xiao, 2020, Distribution and antifungal susceptibility of candida species causing candidemia in China: an update from the CHIF-NET study, J. Infect. Dis. source

      Not checked in the free run.

  • Probably not a substantial claim: may not pass S3 (load-bearing).

    Premisecitation

    Pfaller et al. reported that the proportion of C. albicans decreased to under 50% in 2009 in 39 countries, including Japan.

    “In a related study, Pfellar, et al. reported that the proportion of C. albicans decreased to under 50% in 2009 in 39 countries, including Japan.17”
    Quote in the paperNot a substantial claim0 of 1 sources checked
    • cites [17] Pfaller, 2019, Twenty years of the SENTRY antifungal surveillance program: results for Candida species from 1997-2016, Open Forum Infect Dis source

      Not checked in the free run.

  • Classified as probably not a substantial claim.

    Premisecitation

    In Japan, micafungin is generally prescribed for candidiasis.

    “In Japan, MCFG is generally prescribed for candidiasis.25”
    Quote in the paperSubstantial claim0 of 1 sources checked
    • cites [25] Kawabe, 2020, Trends of antifungal use based on sales data in Japan from 2006 to 2015, Biol. Pharm. Bull. source

      Not checked in the free run.

  • Probably not a substantial claim: may not pass S3 (load-bearing). May combine two claims.

    Premisecitation

    Kakeya et al. analyzed 1921 Candida isolates from 10 hospitals between 2003 and 2014 and reported an increase in non-albicans candidemia.

    “In Japan, Kakeya, et al. analyzed 1921 Candida isolates from 10 hospitals between 2003 and 2014 and reported an increase in the proportion of non-albicans candidemia.11”
    Quote in the paperNot a substantial claim0 of 1 sources checked
    • cites [11] Kakeya, 2018, [National trends in the distribution of candida species causing Candidemia in Japan from 2003 to 2014], Med. Mycol. J. source

      Not checked in the free run.

  • Probably not a substantial claim: may not pass S3 (load-bearing). May combine two claims.

    Premisecitation

    Lamoth et al. reported that the distribution of Candida species has been changing, with a decrease in C. albicans and an increase in C. glabrata and C. parapsilosis.

    “Lamoth, et al. reported that the distribution of Candida spp. has been changing; specifically, there has been a decrease in the proportion of C. albicans and an increase in that of C. glabrata and C. parapsilosis.5”
    Quote in the paperNot a substantial claim0 of 1 sources checked
    • cites [5] Lamoth, 2018, Changes in the epidemiological landscape of invasive candidiasis, J. Antimicrob. Chemother. source

      Not checked in the free run.

  • Probably not a substantial claim: may not pass S3 (load-bearing).

    Premisecitation

    In India and Latin America, Candida tropicalis is one of the most frequently encountered species.

    “In India and Latin America, it has been reported that C. tropicalis is one of the most frequently encountered species.7,23,24”
    Quote in the paperNot a substantial claim0 of 3 sources checked
    • cites [7] Nucci, 2013, Epidemiology of candidemia in Latin America: a laboratory-based survey, PLoS One source

      Not checked in the free run.

    • cites [23] Chakrabarti, 2015, Incidence, characteristics and outcome of ICU-acquired candidemia in India, Intensive Care Med source

      Not checked in the free run.

    • cites [24] Chander, 2013, Epidemiology of Candida blood stream infections: experience of a tertiary care centre in North India, J Infect Dev Ctries source

      Not checked in the free run.

  • May combine two claims.

    Premisecitation

    Another Japanese study reported chronological surveillance data from 10 hospitals between 2003 and 2014, but did not take antifungal susceptibility into consideration.

    “Another study reported chronological surveillance data from 10 participating hospitals between 2003 and 2014.11 However, this report did not take antifungal susceptibility into consideration.”
    Quote in the paperSubstantial claim0 of 1 sources checked
    • cites [11] Kakeya, 2018, [National trends in the distribution of candida species causing Candidemia in Japan from 2003 to 2014], Med. Mycol. J. source

      Not checked in the free run.

  • Probably not a substantial claim: may not pass S3 (load-bearing). May combine two claims.

    Premisecitation

    In a meta-analysis of European countries, Koehler et al. reported that 40-50% of candidemia cases were caused by C. albicans, 10-30% by C. glabrata, and 2-15% by C. parapsilosis.

    “In a meta-analysis of various reports from European countries, Koehler, et al. reported that 40–50% of candidemia cases were caused by C. albicans, 10–30% by C. glabrata, and 2–15% by C. parapsilosis, which is similar to the results of the present study.20”
    Quote in the paperNot a substantial claim0 of 1 sources checked
    • cites [20] Koehler, 2019, Morbidity and mortality of candidaemia in Europe: an epidemiologic meta-analysis, Clin. Microbiol. Infect. source

      Not checked in the free run.

  • Probably not a substantial claim: may not pass S3 (load-bearing).

    Premisecitation

    Tan et al. reported Candida tropicalis to be the second most abundant isolate (30.7%) in the Asia-Pacific region.

    “Tan, et al. obtained Candida spp. From seven countries in the Asia-Pacific region and reported C. tropicalis to be the second most abundant isolate (30.7%).22”
    Quote in the paperNot a substantial claim0 of 1 sources checked
    • cites [22] Tan, 2016, Antifungal susceptibility of invasive Candida bloodstream isolates from the Asia-Pacific region, Med. Mycol. source

      Not checked in the free run.

  • Probably not a substantial claim: may not pass S3 (load-bearing). May combine two claims.

    Premisecitation

    The fluconazole resistance rates around the world were 0.6-1.7% in C. albicans, 8.0-16.2% in C. glabrata, 1.3-15.0% in C. parapsilosis, and 1.1-5.1% in C. tropicalis.

    “the resistance rate of fluconazole (FLCZ) was found to be 0.6–1.7% in C. albicans, 8.0–16.2% in C. glabrata, 1.3–15.0% in C. parapsilosis, and 1.1–5.1% in C. tropicalis around the world.9”
    Quote in the paperNot a substantial claim0 of 1 sources checked
    • cites [9] Bassetti, 2020, Antifungal susceptibility testing in Candida, Aspergillus and Cryptococcus infections: are the MICs useful for clinicians?, Clin. Microbiol. Infect. source

      Not checked in the free run.

  • Probably not a substantial claim: may not pass S3 (load-bearing).

    Premisecitation

    Gamaletsou et al. reported that Candida parapsilosis accounted for 50% of hospitalized adult patients with hematologic malignancies.

    “In a prospective cohort multicenter study, Gamaletsou, et al. reported that C. parapsilosis accounted for 50% of hospitalized adult patients with hematologic malignancies.29”
    Quote in the paperNot a substantial claim0 of 1 sources checked
    • cites [29] Gamaletsou, 2014, A prospective, cohort, multicentre study of candidaemia in hospitalized adult patients with haematological malignancies, Clin. Microbiol. Infect. source

      Not checked in the free run.

  • Probably not a substantial claim: may not pass S3 (load-bearing).

    Premisecitation

    Kimura et al. reported that 14/30 cases of micafungin breakthrough candidemia in patients with hematological disorders were caused by Candida parapsilosis.

    “Kimura, et. al. reported that 14/30 cases of MCFG breakthrough candidemia in patients with hematological disorders were caused by C. parapsilosis.31”
    Quote in the paperNot a substantial claim0 of 1 sources checked
    • cites [31] Kimura, 2018, Micafungin breakthrough fungemia in patients with hematological disorders, Antimicrob. Agents Chemother. source

      Not checked in the free run.

  • May combine two claims.

    Premisecitation

    Patients subjected to bone marrow transplantation usually have a central venous catheter, and those with oral and gastrointestinal mucosal disorders and neutropenia are treated using total parenteral nutrition, which is a risk factor for candidemia caused by Candida parapsilosis.

    “Patients subjected to bone marrow transplantation usually have a central venous catheter, and those subjected to oral and gastrointestinal mucosal disorders and neutropenia are treated using total parenteral nutrition, which is one of the risk factors for candidemia caused by C. parapsilosis.30”
    Quote in the paperNot a substantial claim0 of 1 sources checked
    • cites [30] Toth, 2019, Candida parapsilosis: from genes to the bedside, Clin. Microbiol. Rev. source

      Not checked in the free run.

  • May combine two claims.

    Premisecitation

    No resistant Candida krusei strains have been reported in the Asia-Pacific, Switzerland, and Latin America; however, a Norwegian study reported 34.8% resistance of C. krusei to amphotericin B between 2004 and 2012.

    “No resistant C. krusei strains have been reported in the Asia-Pacific,8,21 Switzerland,18 and Latin America;7 however, a Norwegian study reported 34.8% resistance of C. krusei to AMPH between 2004 and 2012.27”
    Quote in the paperNot a substantial claim0 of 3 sources checked
    • cites [8] Xiao, 2020, Distribution and antifungal susceptibility of candida species causing candidemia in China: an update from the CHIF-NET study, J. Infect. Dis. source

      Not checked in the free run.

    • cites [21] Chapman, 2017, Changing epidemiology of candidaemia in Australia, J. Antimicrob. Chemother. source

      Not checked in the free run.

    • cites [18] Adam, 2021, Trends of the epidemiology of Candidemia in Switzerland: a 15-Year FUNGINOS survey, Open Forum Infect Dis source

      Not checked in the free run.

  • Probably not a substantial claim: may not pass S3 (load-bearing).

    Premisecitation

    Bassetti et al. reported the resistance rate of Candida tropicalis for fluconazole to be 1.1% and 5.1% in Latin America and North America, respectively.

    “Bassetti, et al. reported the resistance rate of C. tropicalis for FLCZ to be 1.1% and 5.1% in Latin America and North America, respectively.9”
    Quote in the paperNot a substantial claim0 of 1 sources checked
    • cites [9] Bassetti, 2020, Antifungal susceptibility testing in Candida, Aspergillus and Cryptococcus infections: are the MICs useful for clinicians?, Clin. Microbiol. Infect. source

      Not checked in the free run.

  • May combine two claims.

    Premisecitation

    The resistance rate of Candida tropicalis for voriconazole was reported to be 14%, 25.6%, and 16.7% in the Asia-Pacific region, China, and Australia, respectively.

    “The resistance rate of C. tropicalis for VRCZ was reported to be 14%, 25.6%, and 16.7% in the Asia-Pacific region,22 China26 and Australia,21 respectively.”
    Quote in the paperNot a substantial claim0 of 3 sources checked
    • cites [22] Tan, 2016, Antifungal susceptibility of invasive Candida bloodstream isolates from the Asia-Pacific region, Med. Mycol. source

      Not checked in the free run.

    • cites [26] Wang, 2021, Continual decline in azole susceptibility rates in candida tropicalis over a 9-year period in China, Front. Microbiol. source

      Not checked in the free run.

    • cites [21] Chapman, 2017, Changing epidemiology of candidaemia in Australia, J. Antimicrob. Chemother. source

      Not checked in the free run.

  • Probably not a substantial claim: may not pass S3 (load-bearing).

    Premisecitation

    Hematologic malignancy is a risk factor for candidemia.

    “Hematologic malignancy is a risk factor for candidemia.1”
    Quote in the paperNot a substantial claim0 of 1 sources checked
    • cites [1] Kullberg, 2015, Invasive candidiasis, N. Engl. J. Med. source

      Not checked in the free run.

  • Probably not a substantial claim: may not pass S3 (load-bearing).

    Premisecitation

    Pfaller et al. reported that the resistance rate of Candida glabrata for micafungin was 0.4%, 0.6%, 0%, and 2.8% in the Asia-Pacific region, Europe, Latin America, and North America between 2006 and 2016, respectively.

    “Pfaller et al. reported that the resistance rate of C. glabrata for MCFG was 0.4%, 0.6%, 0%, and 2.8% in the Asia-Pacific region, Europe, Latin America, and North America between 2006 and 2016, respectively.17”
    Quote in the paperNot a substantial claim0 of 1 sources checked
    • cites [17] Pfaller, 2019, Twenty years of the SENTRY antifungal surveillance program: results for Candida species from 1997-2016, Open Forum Infect Dis source

      Not checked in the free run.

33 of 33

  • The paper relies on this without support.

    The JANIS database is representative of candidemia in Japan.

    “we utilized comprehensive surveillance data collected in a national antimicrobial resistance surveillance program—the Japan Nosocomial Infections Surveillance (JANIS)”
    “based on the national surveillance data from JANIS (2010–2019)”

  • The paper relies on this without support.

    Species identification and antifungal susceptibility testing reported by participating hospitals are accurate and consistent across hospitals.

    “JANIS has not been collecting information about how species identification is conducted in each hospital.”
    “different methods of antifungal susceptibility testing are used by these hospitals.”

  • The paper relies on this without support.

    The number of patients who underwent blood culture testing is a valid denominator for estimating candidemia incidence.

    “Therefore, we used the number of patients who underwent blood culture tests to evaluate the incidence of candidemia.”

  • The paper relies on this without support.

    The tested subset of isolates is representative of all isolates for antifungal susceptibility.

    “Only some of the isolates submitted to the JANIS database (29.2% [7247/24 854 isolates] of C. albicans, 28.2% [3137/11 107 isolates] of C. glabrata, 32.5% [3499/10 764 isolates] of C. parapsilosis, 28.9% [1107/3827 isolates] of C. tropicalis, 29.7% [243/817 isolates] of C. krusei, and 40.7% [386/949 isolates] of C. guiliermondii) were subjected to antifungal susceptibility testing.”

  • The paper relies on this without support.

    The 186 hospitals certified by the Japanese Society for Transplantation and Cellular Therapy are representative of hospitals responsible for bone marrow transplantation.

    “The 186 hospitals were certified by Japanese Society for Transplantation and Cellular Therapy.”
5 of 5

Claims other papers make about this one

Each is checked against this paper’s own text: does it say what the citing paper says it does?

  • Recent population surveys have demonstrated emerging resistance rates to voriconazole in C. krusei, approximating 10% in some regions of the world.

    “In general, voriconazole has been considered the best oral option for C. krusei infections, however, recent population surveys have demonstrated emerging resistance rates to voriconazole, approximating 10% in some regions of the world.”

    From Epidemiology of Invasive Candidiasis (2024) · cites this paper as [107]

    Table 2 (Results, page unavailable) reports voriconazole resistance in C. krusei of 12.5% and 15.4% in two Japanese hospital groups in 2019, broadly consistent with an approximate 10% rate. The paper does not establish that rate across multiple world regions or show that C. krusei voriconazole resistance is increasing. (LLM, conf=0.82)

    Experimental — accuracy not yet measured

  • Echinocandin and amphotericin B resistance in C. krusei appears to be emerging, with rates of resistance in the 3% to 10% range among larger multicenter studies.

    “Echinocandin and amphotericin B resistance also appears to be emerging, with rates of resistance in the 3% to 10% range among larger multicenter studies.107,112”

    From Epidemiology of Invasive Candidiasis (2024) · cites this paper as [107]

    The Results (Notable susceptibility patterns; page unavailable) report C. krusei amphotericin B resistance, but its annual rate ranged from 3.2% to 35.7%, not consistently 3%–10%. Table 2 (page unavailable) reports 6.25% micafungin resistance in one hospital group, but 0% in the other and 14.3%–20.0% amphotericin B resistance. The paper describes fluctuation rather than an emerging upward trend and cautions that the number of C. krusei isolates was small. (LLM, conf=0.88)

    Experimental — accuracy not yet measured

Self-check

Percentages, sums and reported differences re-computed from the paper’s own numbers.

Each contradiction between two passages listed here was confirmed by an independent check.

  • Two different proportions are given for C. tropicalis

    Minor

    The discussion gives the study's C. tropicalis proportion as 5.8%, but the results give it as 6.7%.

  • Two different totals are given for C. albicans isolates

    Minor

    The susceptibility-testing section gives 24 854 C. albicans isolates, whereas the distribution section gives 24 864-a difference of 10.

2 of 2

Cites

Flagged first, then by citations

Research works printed but not linked: 1

  1. The European Committee on Antimicrobial Susceptibility Testing, 2020, Crinical breakpoints for fungi v. 10.0

Cited by

Sorted by citations

Related

Authors
Kajihara, T., Yahara, K., Nagi, M., Kitamura, N., Hirabayashi, A., Hosaka, Y., Abe, M., Miyazaki, Y., & Sugai, M.
Affiliations
National Institute of Infectious Diseases (JP)
Corresponding author
Kajihara, Toshiki
ORCID
Venue
Medical Mycology
Publisher
Oxford University Press (OUP)
Published
2022-09
Volume
60
Issue
9
ISSN
  • 0268-1218 (ISSN-L)
  • 1369-3786
  • 1460-2709
DOI
10.1093/mmy/myac071
PMC
PMC9521341
OpenAlex
W4295427929
Semantic Scholar
c40db3d9bada00303669cc730ff1f1b74d392c80
Cited by
29
References
30
Citations by year
2026: 7 · 2025: 9 · 2024: 6 · 2023: 7
FWCI
2.69
Type
journal article
Language
en
Open access
Licence
Locations
  • Medical Mycology (publishedVersion, cc-by)
  • PubMed Central (publishedVersion, cc-by)
  • PubMed (publishedVersion)
Funders
  • Emerging Technology Fund
  • Japan Agency for Medical Research and Development (21fk0108604j0001)
Topics
  • Health Sciences › Medicine › Infectious Diseases › Antifungal resistance and susceptibility
  • Life Sciences › Biochemistry, Genetics and Molecular Biology › Molecular Biology › Yeasts and Rust Fungi Studies
  • Health Sciences › Medicine › Ophthalmology › Ocular Infections and Treatments
Keywords
candidemia, Candida species distribution, antifungal susceptibility, Candida glabrata, Candida tropicalis, Candida krusei, Candida guilliermondii, Candida albicans, Candida parapsilosis, azole resistance, micafungin resistance, amphotericin B resistance, bone marrow transplantation, nosocomial fungal infections, Japan
MeSH terms
Candida parapsilosis, Micafungin, Amphotericin B, Antifungal Agents, Azoles, Candida, Candida albicans, Humans, Japan, Microbial Sensitivity Tests, Fluconazole, Drug Resistance, Fungal, Candida tropicalis, Candida glabrata, Candidemia, Voriconazole

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Claims read by deepseek-v4.1-flash under definition version 3 (extract-v3) on 2026-10-10.

Classified by jev-1.13-20260917 (gold-guideline-v0.2) on 2026-10-10.

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