Antifungal Efficacy during Candida krusei Infection in Non-Conventional Models Correlates with the Yeast In Vitro Susceptibility Profile

PLoS ONE

Volumn 8, Issue 3, 2013, Pages

  Scorzoni, Liliana ^a,b   de Lucas, Maria Pilar ^a   Mesa Arango, Ana Cecilia ^a,c   Fusco Almeida, Ana Marisa ^b   Lozano, Encarnación ^a   Cuenca Estrella, Manuel ^a   Mendes Giannini, Maria Jose ^b   Zaragoza, Oscar ^a  

^a INSTITUTO DE SALUD CARLOS III   (Spain)

^b SÃO PAULO STATE UNIVERSITY UNESP   (Brazil)

^c UNIVERSIDAD DE ANTIOQUIA   (Colombia)

Author keywords

[No Author keywords available]

Indexed keywords

AMPHOTERICIN B; CASPOFUNGIN; FLUCONAZOLE; VORICONAZOLE;

ANIMAL TISSUE; ANTIFUNGAL ACTIVITY; ANTIFUNGAL SUSCEPTIBILITY; ARTHROPOD LARVA; ARTICLE; CAENORHABDITIS ELEGANS; CANDIDA KRUSEI; CANDIDIASIS; CONCENTRATION RESPONSE; CONTROLLED STUDY; CYTOLYSIS; DRUG EFFICACY; FUNGAL VIRULENCE; GALLERIA MELLONELLA; HISTOPATHOLOGY; IN VITRO STUDY; MINIMUM INHIBITORY CONCENTRATION; NONHUMAN; PHAGOCYTOSIS; PROTECTION;

AMPHOTERICIN B; ANIMALS; ANTIFUNGAL AGENTS; CAENORHABDITIS ELEGANS; CANDIDA; CANDIDIASIS; FLUCONAZOLE; LEPIDOPTERA; PYRIMIDINES; TRIAZOLES;

CAENORHABDITIS ELEGANS; GALLERIA MELLONELLA; ISSATCHENKIA ORIENTALIS; MAMMALIA;

EID: 84875543551     PISSN: None     EISSN: 19326203     Source Type: Journal    
DOI: 10.1371/journal.pone.0060047     Document Type: Article

References (80)

1. Pfaller MA, Diekema DJ, (2007) Epidemiology of invasive candidiasis: a persistent public health problem. Clin Microbiol Rev 20: 133-163.
2. Almirante B, Rodriguez D, Park BJ, Cuenca-Estrella M, Planes AM, et al. (2005) Epidemiology and predictors of mortality in cases of Candida bloodstream infection: results from population-based surveillance, barcelona, Spain, from 2002 to 2003. J Clin Microbiol 43: 1829-1835.
3. Chen S, Slavin M, Nguyen Q, Marriott D, Playford EG, et al. (2006) Active surveillance for candidemia, Australia. Emerg Infect Dis 12: 1508-1516.
4. Labelle AJ, Micek ST, Roubinian N, Kollef MH, (2008) Treatment-related risk factors for hospital mortality in Candida bloodstream infections. Crit Care Med 36: 2967-2972.
5. Pfaller MA, Diekema DJ, (2010) Epidemiology of invasive mycoses in North America. Crit Rev Microbiol 36: 1-53.
6. Colombo AL, Tobón A, Restrepo A, Queiroz-Telles F, Nucci M, (2011) Epidemiology of endemic systemic fungal infections in Latin America. Med Mycol 49: 785-798.
7. Warnock DW, (2006) Fungal diseases: an evolving public health challenge. Med Mycol 44: 697-705.
8. Shorr AF, Gupta V, Sun X, Johannes RS, Spalding J, et al. (2009) Burden of early-onset candidemia: analysis of culture-positive bloodstream infections from a large U.S. database. Crit Care Med 37: 2519-2526; quiz 2535.
9. Eggimann P, Garbino J, Pittet D, (2003) Epidemiology of Candida species infections in critically ill non-immunosuppressed patients. Lancet Infect Dis 3: 685-702.
10. Colombo AL, Nucci M, Park BJ, Nouer SA, Arthington-Skaggs B, et al. (2006) Epidemiology of candidemia in Brazil: a nationwide sentinel surveillance of candidemia in eleven medical centers. J Clin Microbiol 44: 2816-2823.
11. Shao PL, Huang LM, Hsueh PR, (2007) Recent advances and challenges in the treatment of invasive fungal infections. Int J Antimicrob Agents 30: 487-495.
12. Pemán J, Salavert M, (2012) General epidemiology of invasive fungal disease. Enferm Infecc Microbiol Clin 30: 90-98.
13. Arendrup MC, (2010) Epidemiology of invasive candidiasis. Curr Opin Crit Care 16: 445-452.
14. Peman J, Canton E, Quindos G, Eraso E, Alcoba J, et al. (2012) Epidemiology, species distribution and in vitro antifungal susceptibility of fungaemia in a Spanish multicentre prospective survey. J Antimicrob Chemother 67: 1181-1187.
15. Trick WE, Fridkin SK, Edwards JR, Hajjeh RA, Gaynes RP, (2002) Secular trend of hospital-acquired candidemia among intensive care unit patients in the United States during 1989-1999. Clin Infect Dis 35: 627-630.
16. Pfaller MA, Diekema DJ, Gibbs DL, Newell VA, Nagy E, et al. (2008) Candida krusei, a multidrug-resistant opportunistic fungal pathogen: geographic and temporal trends from the ARTEMIS DISK Antifungal Surveillance Program, 2001 to 2005. J Clin Microbiol 46: 515-521.
17. Horn DL, Neofytos D, Anaissie EJ, Fishman JA, Steinbach WJ, et al. (2009) Epidemiology and outcomes of candidemia in 2019 patients: data from the prospective antifungal therapy alliance registry. Clin Infect Dis 48: 1695-1703.
18. Miceli MH, Díaz JA, Lee SA, (2011) Emerging opportunistic yeast infections. Lancet Infect Dis 11: 142-151.
19. Rodríguez-Tudela JL, Arendrup MC, Cuenca-Estrella M, Donnelly JP, Lass-Flörl C, (2010) EUCAST breakpoints for antifungals. Drug News Perspect 23: 93-97.
20. Abbas J, Bodey GP, Hanna HA, Mardani M, Girgawy E, et al. (2000) Candida krusei fungemia. An escalating serious infection in immunocompromised patients. Arch Intern Med 160: 2659-2664.
21. Fukuoka T, Johnston DA, Winslow CA, de Groot MJ, Burt C, et al. (2003) Genetic basis for differential activities of fluconazole and voriconazole against Candida krusei. Antimicrob Agents Chemother 47: 1213-1219.
22. Pappas PG, Rex JH, Sobel JD, Filler SG, Dismukes WE, et al. (2004) Guidelines for treatment of candidiasis. Clin Infect Dis 38: 161-189.
23. Spanakis EK, Aperis G, Mylonakis E, (2006) New agents for the treatment of fungal infections: clinical efficacy and gaps in coverage. Clin Infect Dis 43: 1060-1068.
24. Venkateswarlu K, Denning DW, Manning NJ, Kelly SL, (1996) Reduced accumulation of drug in Candida krusei accounts for itraconazole resistance. Antimicrob Agents Chemother 40: 2443-2446.
25. Orozco AS, Higginbotham LM, Hitchcock CA, Parkinson T, Falconer D, et al. (1998) Mechanism of fluconazole resistance in Candida krusei. Antimicrob Agents Chemother 42: 2645-2649.
26. Pemán J, Cantón E, Orero A, Viudes A, Frasquet J, et al. (2002) Epidemiology of candidemia in Spain- Multicenter study. Rev Iberoam Micol 19: 30-35.
27. Muñoz P, Sánchez-Somolinos M, Alcalá L, Rodríguez-Créixems M, Peláez T, et al. (2005) Candida krusei fungaemia: antifungal susceptibility and clinical presentation of an uncommon entity during 15 years in a single general hospital. J Antimicrob Chemother 55: 188-193.
28. Rogers TR, (2006) Antifungal drug resistance: limited data, dramatic impact? Int J Antimicrob Agents 27 Suppl 1: 7-11.
29. Rodriguez-Tudela JL, Alcazar-Fuoli L, Cuesta I, Alastruey-Izquierdo A, Monzon A, et al. (2008) Clinical relevance of resistance to antifungals. Int J Antimicrob Agents 32 Suppl 2: S111-113.
30. Colombo AL, Ngai AL, Bourque M, Bradshaw SK, Strohmaier KM, et al. (2010) Caspofungin use in patients with invasive candidiasis caused by common non-albicans Candida species: review of the caspofungin database. Antimicrob Agents Chemother 54: 1864-1871.
31. Steenbergen JN, Shuman HA, Casadevall A, (2001) Cryptococcus neoformans interactions with amoebae suggest an explanation for its virulence and intracellular pathogenic strategy in macrophages. Proc Natl Acad Sci U S A 98: 15245-15250.
32. Steenbergen JN, Nosanchuk JD, Malliaris SD, Casadevall A, (2003) Cryptococcus neoformans virulence is enhanced after growth in the genetically malleable host Dictyostelium discoideum. Infect Immun 71: 4862-4872.
33. Mylonakis E, Ausubel FM, Perfect JR, Heitman J, Calderwood SB, (2002) Killing of Caenorhabditis elegans by Cryptococcus neoformans as a model of yeast pathogenesis. Proc Natl Acad Sci U S A 99: 15675-15680.
34. Glavis-Bloom J, Muhammed M, Mylonakis E, (2012) Of model hosts and man: using Caenorhabditis elegans, Drosophila melanogaster and Galleria mellonella as model hosts for infectious disease research. Adv Exp Med Biol 710: 11-17.
35. Alarco AM, Marcil A, Chen J, Suter B, Thomas D, et al. (2004) Immune-deficient Drosophila melanogaster: a model for the innate immune response to human fungal pathogens. J Immunol 172: 5622-5628.
36. Fallon AM, Sun D, (2001) Exploration of mosquito immunity using cells in culture. Insect Biochem Mol Biol 31: 263-278.
37. Boman HG, Hultmark D, (1987) Cell-free immunity in insects. Annu Rev Microbiol 41: 103-126.
38. Kavanagh K, Reeves EP, (2004) Exploiting the potential of insects for in vivo pathogenicity testing of microbial pathogens. FEMS Microbiol Rev 28: 101-112.
39. Bergin D, Brennan M, Kavanagh K, (2003) Fluctuations in haemocyte density and microbial load may be used as indicators of fungal pathogenicity in larvae of Galleria mellonella. Microbes Infect 5: 1389-1395.
40. Fuchs BB, O'Brien E, Khoury JB, Mylonakis E, (2010) Methods for using Galleria mellonella as a model host to study fungal pathogenesis. Virulence 1: 475-482.
41. Desalermos A, Fuchs BB, Mylonakis E, (2012) Selecting an invertebrate model host for the study of fungal pathogenesis. PLoS Pathog 8: e1002451.
42. Fuchs BB, Mylonakis E, (2006) Using non-mammalian hosts to study fungal virulence and host defense. Curr Opin Microbiol 9: 346-351.
43. Mahajan-Miklos S, Tan MW, Rahme LG, Ausubel FM, (1999) Molecular mechanisms of bacterial virulence elucidated using a Pseudomonas aeruginosa-Caenorhabditis elegans pathogenesis model. Cell 96: 47-56.
44. Breger J, Fuchs BB, Aperis G, Moy TI, Ausubel FM, et al. (2007) Antifungal chemical compounds identified using a C. elegans pathogenicity assay. PLoS Pathog 3: e18.
45. Tampakakis E, Okoli I, Mylonakis E, (2008) A C. elegans-based, whole animal, in vivo screen for the identification of antifungal compounds. Nat Protoc 3: 1925-1931.
46. Okoli I, Coleman JJ, Tampakakis E, Tempakakis E, An WF, et al. (2009) Identification of antifungal compounds active against Candida albicans using an improved high-throughput Caenorhabditis elegans assay. PLoS One 4: e7025.
47. Gillum AM, Tsay EY, Kirsch DR, (1984) Isolation of the Candida albicans gene for orotidine-5′-phosphate decarboxylase by complementation of S. cerevisiae ura3 and E. coli pyrF mutations. Mol Gen Genet 198: 179-182.
48. Rodriguez-Tudela JL, Arendrup M, Barchiesi F, Bille J, Chryssanthou E, et al. (2008) EUCAST definitive document EDef 7.1: method for the determination of broth dilution MICs of antifungal agents for fermentative yeasts. Clin Microbiol Infect 14: 398-405.
49. Arendrup MC, Cuenca-Estrella M, Lass-Florl C, Hope W, (2012) EUCAST technical note on the EUCAST definitive document EDef 7.2: method for the determination of broth dilution minimum inhibitory concentrations of antifungal agents for yeasts EDef 7.2 (EUCAST-AFST). Clin Microbiol Infect 18: E246-247.
50. Alvarado-Ramirez E, Torres-Rodriguez JM, Sellart M, Vidotto V, (2008) Laccase activity in Cryptococcus gattii strains isolated from goats. Rev Iberoam Micol 25: 150-153.
51. Williamson PR, (1994) Biochemical and molecular characterization of the diphenol oxidase of Cryptococcus neoformans: identification as a laccase. J Bacteriol 176: 656-664.
52. Sulston J, Hodgkin J (1988) The Nematode Caenorhabditis elegans. Cold Spring Harbor, New York: Cold Spring Harbor Laboratory Press.
53. Fuchs BB, Eby J, Nobile CJ, El Khoury JB, Mitchell AP, et al. (2010) Role of filamentation in Galleria mellonella killing by Candida albicans. Microbes Infect 12: 488-496.
54. Ben-Ami R, Lewis RE, Kontoyiannis DP, (2008) Immunocompromised hosts: immunopharmacology of modern antifungals. Clin Infect Dis 47: 226-235.
55. Kelly J, Kavanagh K, (2011) Caspofungin primes the immune response of the larvae of Galleria mellonella and induces a non-specific antimicrobial response. J Med Microbiol 60: 189-196.
56. Mesa-Arango AC, Scorzoni L, Zaragoza O, (2012) It only takes one to do many jobs: Amphotericin B as antifungal and immunomodulatory drug. Frontiers in Microbiology 3: 286.
57. Mylonakis E, Casadevall A, Ausubel FM, (2007) Exploiting amoeboid and non-vertebrate animal model systems to study the virulence of human pathogenic fungi. PLoS Pathog 3: e101.
58. García-Rodas R, Casadevall A, Rodríguez-Tudela JL, Cuenca-Estrella M, Zaragoza O, (2011) Cryptococcus neoformans capsular enlargement and cellular gigantism during Galleria mellonella infection. PLoS One 6: e24485.
59. Pukkila-Worley R, Ausubel FM, Mylonakis E, (2011) Candida albicans infection of Caenorhabditis elegans induces antifungal immune defenses. PLoS Pathog 7: e1002074.
60. Jackson JC, Higgins LA, Lin X, (2009) Conidiation color mutants of Aspergillus fumigatus are highly pathogenic to the heterologous insect host Galleria mellonella. PLoS One 4: e4224.
61. Arendrup M, Horn T, Frimodt-Moller N, (2002) In vivo pathogenicity of eight medically relevant Candida species in an animal model. Infection 30: 286-291.
62. Cotter G, Doyle S, Kavanagh K, (2000) Development of an insect model for the in vivo pathogenicity testing of yeasts. FEMS Immunol Med Microbiol 27: 163-169.
63. Karyotakis NC, Anaissie EJ, Hachem R, Dignani MC, Samonis G, (1993) Comparison of the efficacy of polyenes and triazoles against hematogenous Candida krusei infection in neutropenic mice. J Infect Dis 168: 1311-1313.
64. Majithiya J, Sharp A, Parmar A, Denning DW, Warn PA, (2009) Efficacy of isavuconazole, voriconazole and fluconazole in temporarily neutropenic murine models of disseminated Candida tropicalis and Candida krusei. J Antimicrob Chemother 63: 161-166.
65. Fuchs BB, Bishop LR, Kovacs JA, Mylonakis E, (2011) Galleria mellonella are resistant to Pneumocystis murina infection. Mycopathologia 171: 273-277.
66. Mylonakis E, Moreno R, El Khoury JB, Idnurm A, Heitman J, et al. (2005) Galleria mellonella as a model system to study Cryptococcus neoformans pathogenesis. Infect Immun 73: 3842-3850.
67. Coleman JJ, Muhammed M, Kasperkovitz PV, Vyas JM, Mylonakis E, (2011) Fusarium pathogenesis investigated using Galleria mellonella as a heterologous host. Fungal Biol 115: 1279-1289.
68. Feldmesser M, Tucker S, Casadevall A, (2001) Intracellular parasitism of macrophages by Cryptococcus neoformans. Trends Microbiol 9: 273-278.
69. Garcia-Rodas R, Zaragoza O, (2012) Catch me if you can: phagocytosis and killing avoidance by Cryptococcus neoformans. FEMS Immunol Med Microbiol 64: 147-161.
70. Mesa-Arango AC, Forastiero A, Bernal-Martinez L, Cuenca-Estrella M, Mellado E, et al. (2012) The non-mammalian host Galleria mellonella can be used to study the virulence of the fungal pathogen Candida tropicalis and the efficacy of antifungal drugs during infection by this pathogenic yeast. Med Mycol.
71. Rowan R, Moran C, McCann M, Kavanagh K, (2009) Use of Galleria mellonella larvae to evaluate the in vivo anti-fungal activity of [Ag2(mal)(phen)3]. Biometals 22: 461-467.
72. Bidla G, Hauling T, Dushay MS, Theopold U, (2009) Activation of insect phenoloxidase after injury: endogenous versus foreign elicitors. J Innate Immun 1: 301-308.
73. Anaissie EJ, Karyotakis NC, Hachem R, Dignani MC, Rex JH, et al. (1994) Correlation between in vitro and in vivo activity of antifungal agents against Candida species. J Infect Dis 170: 384-389.
74. Coleman JJ, Ghosh S, Okoli I, Mylonakis E, (2011) Antifungal activity of microbial secondary metabolites. PLoS One 6: e25321.
75. Desalermos A, Muhammed M, Glavis-Bloom J, Mylonakis E, (2011) Using C. elegans for antimicrobial drug discovery. Expert Opin Drug Discov 6: 645-652.
76. Coleman JJ, Okoli I, Tegos GP, Holson EB, Wagner FF, et al. (2010) Characterization of plant-derived saponin natural products against Candida albicans. ACS Chem Biol 5: 321-332.
77. Drago M, Scaltrito MM, Morace G, (2004) In vitro activity of voriconazole and other antifungal agents against clinical isolates of Candida glabrata and Candida krusei. Eur J Clin Microbiol Infect Dis 23: 619-624.
78. Munoz P, Sanchez-Somolinos M, Alcala L, Rodriguez-Creixems M, Pelaez T, et al. (2005) Candida krusei fungaemia: antifungal susceptibility and clinical presentation of an uncommon entity during 15 years in a single general hospital. J Antimicrob Chemother 55: 188-193.
79. Ostrosky-Zeichner L, Paetznick VL, Rodriguez J, Chen E, Sheehan DJ, (2009) Activity of anidulafungin in a murine model of Candida krusei infection: evaluation of mortality and disease burden by quantitative tissue cultures and measurement of serum (1,3)-beta-D-glucan levels. Antimicrob Agents Chemother 53: 1639-1641.
80. Muhammed M, Fuchs BB, Wu MP, Breger J, Coleman JJ, et al. (2012) The role of mycelium production and a MAPK-mediated immune response in the C. elegans-Fusarium model system. Med Mycol 50: 488-496.