Tracking Candidemia Trends and Antifungal Resistance Patterns across Europe: An In-Depth Analysis of Surveillance Systems and Surveillance Studies
Abstract
:1. Introduction
2. Materials and Methods
2.1. Data and Search Strategy
2.2. Inclusion Criteria for National Surveillance Systems and Multicentre Surveillance Studies
2.3. Data Analysis and Statistics
2.4. Ethics
3. Results
3.1. Candidemia Surveillance in Europe
3.1.1. Representation of Candida Species and Resistance Patterns in Surveillance Studies
3.1.2. Representation of Candida Species and Resistance Patterns in National Surveillance Systems
3.2. Trends in Isolates Included in Surveillances and Antifungal Resistance Rates across Europe
4. Discussion
5. Conclusions
Supplementary Materials
Author Contributions
Funding
Institutional Review Board Statement
Informed Consent Statement
Data Availability Statement
Conflicts of Interest
References
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Pathogen | Antifungal | N° of Countries Reporting Data | N° of Surveillance Studies | N° of Isolates |
---|---|---|---|---|
C. albicans | Azole | 13 (BE; CH; CZ; DK; ES; FR; GR; IS; IT; RO; SI; SE; UK) | 25 | 8595 |
Echinocandin | 12 (BE; CH; CZ; DK; ES; FR; GR; IS; IT; SI; SE; UK) | 24 | 6066 | |
Polyene | 12 (BE; CH; CZ; DK; ES; FR; GR; IS; IT; SI; SE; UK) | 23 | 8454 | |
C. glabrata | Azole | 13 (BE; CH; CZ; DK; ES; FR; GR; IS; IT; RO; SI; SE; UK) | 25 | 3572 |
Echinocandin | 12 (BE; CH; CZ; DK; ES; FR; GR; IS; IT; SI; SE; UK) | 23 | 3001 | |
Polyene | 11 (BE; CH; CZ; DK; ES; FR; IS; IT; SI; SE; UK) | 21 | 2986 | |
C. parapsilosis | Azole | 13 (BE; CH; CZ; DK; ES; FR; GR; IS; IT; RO; SI; SE; UK) | 27 | 3593 |
Echinocandin | 12 (BE; CH; CZ; DK; ES; FR; GR; IS; IT; SI; SE; UK) | 21 | 1381 | |
Polyene | 11 (BE; CH; CZ; DK; ES; FR; IS; IT; SI; SE; UK) | 20 | 1113 | |
C. tropicalis | Azole | 11 (BE; CH; CZ; DK; ES; GR; IS; IT; SI; SE; UK) | 22 | 1143 |
Echinocandin | 11 (BE; CH; CZ; DK; ES; GR; IS; IT; SI; SE; UK) | 23 | 670 | |
Polyene | 10 (BE; CH; CZ; DK; ES; IS; IT; SI; SE; UK) | 20 | 679 | |
C. krusei | Azole | 6 (CH; DK; ES; IT; SI; SE) | 12 | 383 |
Echinocandin | 7 (CH; DK; ES; GR; IT; SI; SE) | 14 | 342 | |
Polyene | 6 (CH; DK; ES; IT; SI; SE) | 12 | 391 |
Country | Surveillance Period | C. albicans | C. glabrata | C. parapsilosis | C. tropicalis | C. krusei |
---|---|---|---|---|---|---|
(a) Azole Resistance N° resistant isolates/N° total isolates (% resistance) | ||||||
Belgium | 2013–2014; * 2018–2022 | 7/179 (3.9) | 11/97 (11.3) | 3/5 (60) * | 4/20 (20.0) | - |
Czech Republic | 2012–2015; * 2018–2022 | 0/28 (0.0) | 0/0 (0.0) * | 1/6 (16.7) * | 1/8 (12.5) | - |
Denmark | 2016–2018 | 3/602 (0.5) | 49/460 (10.7) | 1/60 (1.6) | 3/70 (4.0) | 46/52 (88.5) |
France | 2014–2018 | 0/135 (0.0) | 8/66 (12.1) | 0/41 (0.0) | - | - |
Greece | 2009–2018; * 2018–2022 | 49/1883 (3.0) | 1/2 (50%) * | 441/2216 (20.0) | 23/373 (6.0) | - |
Iceland | 2000–2011 | 0/124 (0.0) | 1/36 (2.8) | 0/11 (0.0) | 1/28 (3.6) | - |
Italy | 2020–2021; * 2018–2022; ** 2016–2017 | 4/104 (3.8) | 1/8 (12.5) * | 106/146 (72.6) | 1/9 (11.1) | 0/10 (0.0) ** |
Romania | 2010–2011 | 1/57 (1.8) | 4/25 (16.0) | 0/59 (0.0) | - | - |
Slovenia | 2001–2012 | 1/272 (0.4) | 82/96 (85.7) | 1/35 (2.7) | 0/19 (0.0) | 0/11 (0.0) |
Spain | 2005–2006 | 0/97 (0.0) | 1/27 (3.7) | 0/34 (0.0) | 0/30 (0.0) | 0/7 (0.0) |
Sweden | 2015–2016; * 2018–2022 | 5/200 (2.5) | 0/3 (0.0) * | 1/14 (7.1) * | 0/15 (0.0) | 5/7 (71.4) |
Switzerland | 2014–2018 | 0/330 (0.0) | 16/176 (9.0) | 2/50 (4.0) | 5/45 (11.0) | 0/11 (0.0) |
United Kingdom | 2006–2017; * 2018–2022 | 1/46 (2.2) | 0/11 (0.0) * | 2/6 (33.3) * | 0/4 (0.0) | - |
Median resistance rate (%) | 0.45 | 11.00 | 4.00 | 6.00 | 0.00 | |
(b) Echinocandin Resistance N° resistant isolates/N° total isolates (% resistance) | ||||||
Belgium | 2013–2014 | 0/179 (0.0) | 1/97 (1.0) | 0/35(0.0) | 0/20 (0.0) | - |
Czech Republic | 2012–2015 | 1/28 (3.6) | 0/10 (0.0) | 0/5 (0.0) | 1/8 (12.5) | - |
Denmark | 2016–2018 | 0/608 (0.0) | 6/454 (1.3) | 0/61 (0.0) | 0/75 (0.0) | 3/69 (4.2) |
France | 2014–2018 | 0/135 (0.0) ‡ | 0/67 (0.0) ‡ | 0/41 (0.0) ‡ | - | - |
Greece | 2009–2018 | 0/724 (0.0) | 7/203 (3.0) | 0/396 (0.0) | 0/75 (0.0) | 0/33 (0.0) |
Iceland | 2000–2011 | 0/41 (0.0) ‡ | 0/14 (0.0) ‡ | 0/5 (0.0) ‡ | 0/7 (0.0)‡ | - |
Italy | 2020–2021; ** 2016–2017 | 3/86 (3.5) | 0/28 (0.0) | 0/127 (0.0) | 0/8 (0.0) | 0/10 (0.0) ** |
Slovenia | 2001–2012 | 1/177 (0.6) ‡ | 2/65 (2.9) ‡ | 0/20 (0.0) ‡ | 0/14 (0.0) ‡ | 0/7 (0.0) ‡ |
Spain | 2005–2006 | 0/97 (0.0) ‡ | 0/27 (0.0) ‡ | 0/34 (0.0) ‡ | 0/30 (0.0) ‡ | 0/7 (0.0) ‡ |
Sweden | 2015–2016 | 1/199 (0.5) | 3/81 (3.7) | 7/36 (19.4) | 1/12 (8.3) | 3/9 (33.3) |
Switzerland | 2014–2018 | 2/212 (1.0) | 1/124 (1.0) | 0/39 (0.0) | 0/32 (0.0) | 0/15 (0.0) |
United Kingdom | 2006–2017; * 2012–2013 | 0/46 (0.0) † | 0/17 (0.0) † | 0/29 (0.0) * | 0/4 (0.0) ‡ | - |
Median resistance rate (%) | 0.00 | 0.50 | 0.00 | 0.00 | 0.00 | |
(c) Polyene Resistance N° resistant isolates/N° total isolates (% resistance) | ||||||
Belgium | 2013–2014 | 0/179 (0.0) | 0/97 (0.0) | 0/35 (0.0) | 0/20 (0.0) | - |
Czech Republic | 2012–2015 | 0/28 (0.0) | 0/10 (0.0) | 0/5 (0.0) | 0/8 (0.0) | - |
Denmark | 2016–2018 | 0/608 (0.0) | 0/460 (0.0) | 0/61 (0.0) | 0/75 (0.0) | 0/72 (0.0) |
France | 2014–2018 | 0/135 (0.0) | 6/65 (9.2) | 0/41 (0.0) | - | - |
Greece | 2009–2018 | 49/1883 (3.0) | - | - | - | - |
Iceland | 2000–2011 | 0/124 (0.0) | 0/36 (0.0) | 0/11 (0.0) | 0/28 (0.0) | - |
Italy | 2020–2021; * 2011–2015 | 0/44 (0.0) * | 0/16 (0.0) * | 1/35 (2.9) * | 0/13 (0.0) * | 0/14 (0.0) * |
Slovenia | 2001–2012 | 0/272 (0.0) | 11/96 (11.2) | 1/35 (2.7) | 0/19 (0.0) | 6/11 (54.5) |
Spain | 2005–2006 | 0/97 (0.0) | 0/27 (0.0) | 0/34 (0.0) | 0/30 (0.0) | 0/7 (0.0) |
Sweden | 2015–2016 | 0/235 (0.0) | 0/81 (0.0) | 0/37 (0.0) | 0/13 (0.0) | 0/13 (0.0) |
Switzerland | 2014–2018 | 0/214 (0.0) | 0/147 (0.0) | 1/40 (2.5) | 0/35 (0.0) | 0/16 (0.0) |
United Kingdom | 2006–2017 | 0/46 (0.0) | 0/17 (0.0) | 0/23 (0.0) | 0/4 (0.0) | - |
Median resistance rate (%) | 0.0 | 0.0 | 0.0 | 0.0 | 0.0 |
Candida Species | Antifungal | N° of Countries with Surveillance Systems |
---|---|---|
C. albicans | Azole | 6 (AT; HR; IT; NO; ES; UK) |
Echinocandin | 5 (AT; HR; NO; ES; UK) | |
Polyene | 5 (AT; HR; NO; ES; UK) | |
C. glabrata | Azole | 4 (AT; HR; NO; UK) |
Echinocandin | 4 (AT; HR; NO; UK) | |
Polyene | 4 (AT; HR; NO; UK) | |
C. parapsilosis | Azole | 5 (AT; HR; NO; ES; UK) |
Echinocandin | 5 (AT; HR; NO; ES; UK) | |
Polyene | 5 (AT; UK; NO; ES; HR) | |
C. tropicalis | Azole | 3 (AT; NO; HR) |
Echinocandin | 3 (AT; NO; HR) | |
Polyene | 3 (AT; NO; HR) | |
C. krusei | Azole | - |
Echinocandin | 1 (HR) | |
Polyene | 1 (HR) |
Antifungal | Candida Species | Austria 2022 | Croatia 2022 | Italy 2019 | Norway 2022 | Spain 2022 | United Kingdom 2022 | N° Total Isolates |
---|---|---|---|---|---|---|---|---|
Azole | C. albicans | 191 | 67 | 17 | 139 | 17 | 796 | 1227 |
C. glabrata | 87 | 28 | - | 41 | - | 372 | 528 | |
C. parapsilosis | 28 | 67 | - | 17 | 23 | 218 | 353 | |
C. tropicalis | 17 | 10 | - | 12 | - | - | 39 | |
C. krusei | - | - * | - | - | - | - | - | |
Echinocandin | C. albicans | 191 | 67 | - | 139 | 10 | 518 | 925 |
C. glabrata | 87 | 28 | - | 41 | - | 325 | 481 | |
C. parapsilosis | 28 | 67 | - | 17 | 13 | 155 | 280 | |
C. tropicalis | 17 | 10 | - | 12 | - | - | 39 | |
C. krusei | - | 6 | - | - | - | - | 6 | |
Polyene | C. albicans | 191 | 67 | - | 15 | 139 | 697 | 1109 |
C. glabrata | 87 | 28 | - | 41 | - | 452 | 608 | |
C. parapsilosis | 28 | 67 | - | 17 | 22 | 205 | 339 | |
C. tropicalis | 17 | 10 | - | 12 | - | - | 39 | |
C. krusei | - | 6 | - | - | - | - | 6 |
Antifungal | Candida Species | Austria 2022 | Croatia 2022 | Italy 2019 ‡ | Norway 2022 | Spain 2022 ‡ | United Kingdom 2022 † | Median Resistance Rate (%) |
---|---|---|---|---|---|---|---|---|
Azole | C. albicans | 0/191 (0.0) | 2/67 (3.0) | 2/17 (11.8) | 0/139 (0.0) | 0/17 (0.0) | 10/796 (1.3) | 0.7 |
C. glabrata | 12/87 (13.8) | 28/28 (100.0) | - | 7/41 (17.1) | - | 54/372 (14.5) | 15.8 | |
C. parapsilosis | 0/28 (0.0) | 54/67 (80.6) | - | 0/17 (0.0) | 10/23 (43.5) | 4/218 (1.8) | 1.8 | |
C. tropicalis | 1/17 (5.9) | 2/10 (20.0) | - | 0/12 (0.0) | - | - | 5.9 | |
Echinocandin | C. albicans | 11/191 (5.8) | 0/67 (0.0) | - | 0/139 (0.0) | 0/10 (0.0) | 0/518 (0.0) | 0.0 |
C. glabrata | 0/87 (0.0) | 0/28 (0.0) | - | 2/41 (4.9) | - | 13/325 (4.0) | 2.0 | |
C. parapsilosis | 1/28 (3.7) | 1/67 (1.6) | - | 0/17 (0.0) | 2/13 (15.4) | 1/155 (0.6) | 1.6 | |
C. tropicalis | 1/17 (5.9) | 0/10 (0.0) | - | 0/12 (0.0) | - | - | 0.0 | |
C. krusei | - | 0/6 (0.0) | - | - | - | - | 0.0 | |
Polyene | C. albicans | 0/191 (0.0) | 0/67 (0.0) | - | 0/15 (0.0) | 0/139 (0.0) | 5/697 (0.7) | 0.0 |
C. glabrata | 0/87 (0.0) | 0/28 (0.0) | - | 0/41 (0.0) | - | 8/452 (1.8) | 0.0 | |
C. parapsilosis | 0/28 (0.0) | 1/67 (1.5) | - | 0/17 (0.0) | 0/22 (0.0) | 1/205 (0.5) | 0.0 | |
C. tropicalis | 0/17 (0.0) | 2/10 (20.0) | - | 0/12 (0.0) | - | - | 0.0 | |
C. krusei | - | 3/6 (50.0) | - | - | - | - | 50.0 * |
Antifungal | Candida Species | Isolate Number Growth per Year (β) | p-Value |
---|---|---|---|
Azole | C. albicans | 58.0 | 0.004 |
C. glabrata | 16.7 | 0.059 | |
C. parapsilosis | 29.7 | 0.004 | |
C. tropicalis | 2.0 | 0.015 | |
Echinocandin | C. albicans | 39.6 | 0.007 |
C. glabrata | 15.5 | 0.030 | |
C. parapsilosis | 23.3 | 0.006 | |
C. tropicalis | 2.0 | 0.018 | |
C. krusei | 1.1 | 0.062 | |
Polyene | C. albicans | 56.8 | 0.004 |
C. glabrata | 31.8 | 0.008 | |
C. parapsilosis | 27.3 | 0.005 | |
C. tropicalis | 2.1 | 0.011 | |
C. krusei | 1.1 | 0.062 |
(Generalised Linear Model (Not Accounting for Heterogeneity) | Bayesian Multilevel Mixed-Effects Model (Accounting for Heterogeneity) | ||||||
---|---|---|---|---|---|---|---|
(Without Accounting for Heterogeneity) | (Accounting for Heterogeneity) | ||||||
Antifungal | Candida Species | Slope (Trend) | p-Value | Trend | Slope (Trend) | p-Value | Trend |
Azole | C. albicans | −0.151 | 0.001 | ↘ | −0.046 | 0.735 | ↔ |
C. glabrata | −0.128 | <0.001 | ↘ | −0.122 | 0.765 | ↔ | |
C. parapsilosis | 0.329 | <0.001 | ↗ | 0.035 | 0.812 | ↔ | |
C. tropicalis | 0.219 | 0.213 | ↔ | 0.227 | 0.530 | ↔ | |
Echinocandin | C. albicans | 0.085 | 0.053 | ↔ | −0.050 | 0.708 | ↔ |
C. glabrata | 0.121 | 0.006 | ↔ | 0.003 | 0.982 | ↔ | |
C. parapsilosis | 0.017 | 0.768 | ↔ | −0.477 | 0.134 | ↔ | |
C. tropicalis | −0.043 | 0.811 | ↔ | −0.525 | 0.554 | ↔ | |
Polyene | C. albicans | −0.030 | 0.652 | ↔ | −0.041 | <0.001 | ↘ |
C. glabrata | −0.143 | 0.077 | ↔ | 0.022 | 0.982 | ↔ | |
C. parapsilosis | −0.248 | 0.082 | ↔ | - | - | - |
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Odoj, K.; Garlasco, J.; Pezzani, M.D.; Magnabosco, C.; Ortiz, D.; Manco, F.; Galia, L.; Foster, S.K.; Arieti, F.; Tacconelli, E. Tracking Candidemia Trends and Antifungal Resistance Patterns across Europe: An In-Depth Analysis of Surveillance Systems and Surveillance Studies. J. Fungi 2024, 10, 685. https://doi.org/10.3390/jof10100685
Odoj K, Garlasco J, Pezzani MD, Magnabosco C, Ortiz D, Manco F, Galia L, Foster SK, Arieti F, Tacconelli E. Tracking Candidemia Trends and Antifungal Resistance Patterns across Europe: An In-Depth Analysis of Surveillance Systems and Surveillance Studies. Journal of Fungi. 2024; 10(10):685. https://doi.org/10.3390/jof10100685
Chicago/Turabian StyleOdoj, Karin, Jacopo Garlasco, Maria Diletta Pezzani, Cristina Magnabosco, Diego Ortiz, Federica Manco, Liliana Galia, Sarah K. Foster, Fabiana Arieti, and Evelina Tacconelli. 2024. "Tracking Candidemia Trends and Antifungal Resistance Patterns across Europe: An In-Depth Analysis of Surveillance Systems and Surveillance Studies" Journal of Fungi 10, no. 10: 685. https://doi.org/10.3390/jof10100685
APA StyleOdoj, K., Garlasco, J., Pezzani, M. D., Magnabosco, C., Ortiz, D., Manco, F., Galia, L., Foster, S. K., Arieti, F., & Tacconelli, E. (2024). Tracking Candidemia Trends and Antifungal Resistance Patterns across Europe: An In-Depth Analysis of Surveillance Systems and Surveillance Studies. Journal of Fungi, 10(10), 685. https://doi.org/10.3390/jof10100685