Assessment of efficacy of antifungals against Aspergillus fumigatus: Value of real-time bioluminescence imaging

Antimicrobial Agents and Chemotherapy

Volumn 57, Issue 7, 2013, Pages 3046-3059

  Galiger, Célimène ^a   Brock, Matthias ^b   Jouvion, Grégory ^a   Savers, Amélie ^a   Parlato, Marianna ^a   Ibrahim Granet, Oumaïma ^a  

^a INSTITUT PASTEUR   (France)

^b FRIEDRICH SCHILLER UNIVERSITY JENA   (Germany)

Author keywords

[No Author keywords available]

Indexed keywords

AMPHOTERICIN B LIPID COMPLEX; ANIDULAFUNGIN; ANTIFUNGAL AGENT; CASPOFUNGIN; MICAFUNGIN; PF 3910960; PF 579 955; UNCLASSIFIED DRUG; VORICONAZOLE;

ANIMAL EXPERIMENT; ANIMAL MODEL; ANIMAL TISSUE; ARTICLE; ASPERGILLOSIS; ASPERGILLUS FUMIGATUS; BIOLUMINESCENCE; CLINICAL TRIAL (TOPIC); CONIDIUM; CONTROLLED STUDY; DRUG EFFICACY; GERMINATION; IMAGING; LEUKOPENIA; LUNG INFECTION; MALE; MOUSE; NONHUMAN; PRIORITY JOURNAL; SURVIVAL; TREATMENT OUTCOME; VIRUS INFECTION; VIRUS STRAIN;

AMPHOTERICIN B; ANIMALS; ANTIFUNGAL AGENTS; ASPERGILLOSIS; ASPERGILLUS FUMIGATUS; ECHINOCANDINS; LUMINESCENT MEASUREMENTS; MALE; MICE; MICE, INBRED BALB C; MICROBIAL SENSITIVITY TESTS; PYRIMIDINES; TRIAZOLES;

EID: 84879014270     PISSN: 00664804     EISSN: 10986596     Source Type: Journal    
DOI: 10.1128/AAC.01660-12     Document Type: Article

References (50)

1. Patterson TF, Kirkpatrick WR, White M, Hiemenz JW, Wingard JR, Dupont B, Rinaldi MG, Stevens DA, Graybill JR. 2000. Invasive aspergillosis. Disease spectrum, treatment practices, and outcomes. Medicine (Baltimore, MD) 79:250-260. (Pubitemid 30616973)
2. Paterson PJ, Seaton S, Prentice HG, Kibbler CC. 2003. Treatment failure in invasive aspergillosis: susceptibility of deep tissue isolates following treatment with amphotericin B. J. Antimicrob. Chemother. 52:873-876. (Pubitemid 37407821)
3. Stevens DA, Schwartz HJ, Lee JY, Moskovitz BL, Jerome DC, Catanzaro A, Bamberger DM, Weinmann AJ, Tuazon CU, Judson MA, Platts-Mills TA, DeGraff AC, Jr. 2000. A randomized trial of itraconazole in allergic bronchopulmonary aspergillosis. N. Engl. J. Med. 342:756-762. (Pubitemid 30151919)
4. Metcalf SC, Dockrell DH. 2007. Improved outcomes associated with advances in therapy for invasive fungal infections in immunocompromised hosts. J. Infect. 55:287-299. (Pubitemid 47371900)
5. Goto N, Hara T, Tsurumi H, Ogawa K, Kitagawa J, Kanemura N, Kasahara S, Yamada T, Shimizu M, Nakamura M, Matsuura K, Moriwaki H. 2010. Efficacy and safety of micafungin for treating febrile neutropenia in hematological malignancies. Am. J. Hematol. 85:872-876.
6. Herbrecht R, Maertens J, Baila L, Aoun M, Heinz W, Martino R, Schwartz S, Ullmann AJ, Meert L, Paesmans M, Marchetti O, Akan H, Ameye L, Shivaprakash M, Viscoli C. 2010. Caspofungin first-line therapy for invasive aspergillosis in allogeneic hematopoietic stem cell transplant patients: an European Organisation for Research and Treatment of Cancer study. Bone Marrow Transplant. 45:1227-1233.
7. Sarfati J, Diaquin M, Debeaupuis JP, Schmidt A, Lecaque D, Beauvais A, Latge JP. 2002. A new experimental murine aspergillosis model to identify strains of Aspergillus fumigatus with reduced virulence. Nihon Ishinkin Gakkai Zasshi 43:203-213.
8. Kousha M, Tadi R, Soubani AO. 2011. Pulmonary aspergillosis: a clinical review. Eur. Respir. Rev. 20:156-174.
9. Balloy V, Huerre M, Latge JP, Chignard M. 2005. Differences in patterns of infection and inflammation for corticosteroid treatment and chemotherapy in experimental invasive pulmonary aspergillosis. Infect. Immun. 73:494-503. (Pubitemid 40041144)
10. Montagnoli C, Bozza S, Gaziano R, Zelante T, Bonifazi P, Moretti S, Bellocchio S, Pitzurra L, Romani L. 2006. Immunity and tolerance to Aspergillus fumigatus. Novartis Found. Symp. 279:66-77.
11. Sheppard DC, Graybill JR, Najvar LK, Chiang LY, Doedt T, Kirkpatrick WR, Bocanegra R, Vallor AC, Patterson TF, Filler SG. 2006. Standardization of an experimental murine model of invasive pulmonary aspergillosis. Antimicrob. Agents Chemother. 50:3501-3503. (Pubitemid 44527538)
12. Andreu N, Zelmer A, Wiles S. 2011. Noninvasive biophotonic imaging for studies of infectious disease. FEMS Microbiol. Rev. 35:360-394.
13. Brock M. 2012. Application of bioluminescence imaging for in vivo monitoring of fungal infections. Int. J. Microbiol. 2012:956794. doi:10.1155/2012/956794.
14. Hutchens M, Luker GD. 2007. Applications of bioluminescence imaging to the study of infectious diseases. Cell. Microbiol. 9:2315-2322. (Pubitemid 47365638)
15. Doyle TC, Nawotka KA, Purchio AF, Akin AR, Francis KP, Contag PR. 2006. Expression of firefly luciferase in Candida albicans and its use in the selection of stable transformants. Microb. Pathog. 40:69-81. (Pubitemid 43221900)
16. Doyle TC, Nawotka KA, Kawahara CB, Francis KP, Contag PR. 2006. Visualizing fungal infections in living mice using bioluminescent pathogenic Candida albicans strains transformed with the firefly luciferase gene. Microb. Pathog. 40:82-90. (Pubitemid 43221901)
17. Brock M, Jouvion G, Droin-Bergere S, Dussurget O, Nicola MA, Ibrahim-Granet O. 2008. Bioluminescent Aspergillus fumigatus, a new tool for drug efficiency testing and in vivo monitoring of invasive aspergillosis. Appl. Environ. Microbiol. 74:7023-7035.
18. Ibrahim-Granet O, Jouvion G, Hohl TM, Droin-Bergere S, Philippart F, Kim OY, Adib-Conquy M, Schwendener R, Cavaillon JM, Brock M. 2010. In vivo bioluminescence imaging and histopathopathologic analysis reveal distinct roles for resident and recruited immune effector cells in defense against invasive aspergillosis. BMC Microbiol. 10:105. doi:10.1186/1471-2180-10-105.
19. Jouvion G, Brock M, Droin-Bergere S, Ibrahim-Granet O. 2012. Duality of liver and kidney lesions after systemic infection of immunosuppressed and immunocompetent mice with Aspergillus fumigatus. Virulence 3:43-50.
20. Szekely A, Johnson EM, Warnock DW. 1999. Comparison of E-test and broth microdilution methods for antifungal drug susceptibility testing of molds. J. Clin. Microbiol. 37:1480-1483. (Pubitemid 29187822)
21. Cuenca-Estrella M, Arendrup MC, Chryssanthou E, Dannaoui E, Lass-Florl C, Sandven P, Velegraki A, Rodriguez-Tudela JL. 2007. Multicentre determination of quality control strains and quality control ranges for antifungal susceptibility testing of yeasts and filamentous fungi using the methods of the Antifungal Susceptibility Testing Subcommittee of the European Committee on Antimicrobial Susceptibility Testing (AFSTEUCAST). Clin. Microbiol. Infect. 13:1018-1022. (Pubitemid 47382259)
22. Sinha BK, Monga DP, Prasad S. 1988. A combination of Gomori-Grocott methenamine silver nitrate and hematoxylene and eosin staining technique for the demonstration of Candida albicans in tissue. Quad. Sclavo Diagn. 24:129-132.
23. Johnson EM. 2008. Issues in antifungal susceptibility testing. J. Antimicrob. Chemother. 61(Suppl 1):i13-i18.
24. Pfaller MA, Messer SA, Mills K, Bolmstrom A. 2000. In vitro susceptibility testing of filamentous fungi: comparison of Etest and reference microdilution methods for determining itraconazole MICs. J. Clin. Microbiol. 38:3359-3361.
25. Pfaller MA, Messer SA, Boyken L, Hollis RJ, Diekema DJ. 2003. In vitro susceptibility testing of filamentous fungi: comparison of Etest and reference M38-A microdilution methods for determining posaconazole MICs. Diagn. Microbiol. Infect. Dis. 45:241-244. (Pubitemid 36555673)
26. Martos AI, Romero A, Gonzalez MT, Gonzalez A, Serrano C, Castro C, Peman J, Canton E, Martin-Mazuelos E. 2010. Evaluation of the Etest method for susceptibility testing of Aspergillus spp. and Fusarium spp. to three echinocandins. Med. Mycol. 48:858-861.
27. Odds FC, Brown AJ, Gow NA. 2003. Antifungal agents: mechanisms of action. Trends Microbiol. 11:272-279. (Pubitemid 36725017)
28. Martinez LR, Ntiamoah P, Gacser A, Casadevall A, Nosanchuk JD. 2007. Voriconazole inhibits melanization in Cryptococcus neoformans. Antimicrob. Agents Chemother. 51:4396-4400. (Pubitemid 350209895)
29. Van Epps HL, Feldmesser M, Pamer EG. 2003. Voriconazole inhibits fungal growth without impairing antigen presentation or T-cell activation. Antimicrob. Agents Chemother. 47:1818-1823. (Pubitemid 36637800)
30. Martin MV, Yates J, Hitchcock CA. 1997. Comparison of voriconazole (UK-109,496) and itraconazole in prevention and treatment of Aspergillus fumigatus endocarditis in guinea pigs. Antimicrob. Agents Chemother. 41:13-16. (Pubitemid 26428125)
31. Gooch VD, Mehra A, Larrondo LF, Fox J, Touroutoutoudis M, Loros JJ, Dunlap JC. 2008. Fully codon-optimized luciferase uncovers novel temperature characteristics of the Neurospora clock. Eukaryot. Cell 7:28-37. (Pubitemid 351959591)
32. Adler-Moore J, Proffitt RT. 2002. AmBisome: liposomal formulation, structure, mechanism of action and pre-clinical experience. J. Antimicrob. Chemother. 49(Suppl 1):21-30. (Pubitemid 34162653)
33. Olson JA, George A, Constable D, Smith P, Proffitt RT, Adler-Moore JP. 2010. Liposomal amphotericin B and echinocandins as monotherapy or sequential or concomitant therapy in murine disseminated and pulmonary Aspergillus fumigatus infections. Antimicrob. Agents Chemother. 54: 3884-3894.
34. Gergis U, Markey K, Greene J, Kharfan-Dabaja M, Field T, Wetzstein G, Schell MJ, Huang Y, Anasetti C, Perkins J. 2010. Voriconazole provides effective prophylaxis for invasive fungal infection in patients receiving glucocorticoid therapy for GVHD. Bone Marrow Transplant. 45: 662-667.
35. Cordonnier C, Rovira M, Maertens J, Olavarria E, Faucher C, Bilger K, Pigneux A, Cornely OA, Ullmann AJ, Bofarull RM, de la Camara R, Weisser M, Liakopoulou E, Abecasis M, Heussel CP, Pineau M, Ljungman P, Einsele H. 2010. Voriconazole for secondary prophylaxis of invasive fungal infections in allogeneic stem cell transplant recipients: results of the VOSIFI study. Haematologicaae 95:1762-1768.
36. Cadena J, Levine DJ, Angel LF, Maxwell PR, Brady R, Sanchez JF, Michalek JE, Levine SM, Restrepo MI. 2009. Antifungal prophylaxis with voriconazole or itraconazole in lung transplant recipients: hepatotoxicity and effectiveness. Am. J. Transplant. 9:2085-2091.
37. White MH, Anaissie EJ, Kusne S, Wingard JR, Hiemenz JW, Cantor A, Gurwith M, Du Mond C, Mamelok RD, Bowden RA. 1997. Amphotericin B colloidal dispersion vs. amphotericin B as therapy for invasive aspergillosis. Clin. Infect. Dis. 24:635-642. (Pubitemid 27143557)
38. Denning DW, Ribaud P, Milpied N, Caillot D, Herbrecht R, Thiel E, Haas A, Ruhnke M, Lode H. 2002. Efficacy and safety of voriconazole in the treatment of acute invasive aspergillosis. Clin. Infect. Dis. 34:563-571. (Pubitemid 34165316)
39. Mikulska M, Viscoli C. 2011. Current role of echinocandins in the management of invasive aspergillosis. Curr. Infect. Dis. Rep. 13:517-527.
40. Petraitis V, Petraitiene R, Hope WW, Meletiadis J, Mickiene D, Hughes JE, Cotton MP, Stergiopoulou T, Kasai M, Francesconi A, Schaufele RL, Sein T, Avila NA, Bacher J, Walsh TJ. 2009. Combination therapy in treatment of experimental pulmonary aspergillosis: in vitro and in vivo correlations of the concentration- and dose-dependent interactions between anidulafungin and voriconazole by Bliss independence drug interaction analysis. Antimicrob. Agents Chemother. 53:2382-2391.
41. Seyedmousavi S, Bruggemann RJ, Melchers WJ, Verweij PE, Mouton JW. 2013. Pharmacodynamics of anidulafungin against clinical Aspergillus fumigatus isolates in a nonneutropenic murine model of disseminated aspergillosis. Antimicrob. Agents Chemother. 57:303-308.
42. Roffey SJ, Cole S, Comby P, Gibson D, Jezequel SG, Nedderman AN, Smith DA, Walker DK, Wood N. 2003. The disposition of voriconazole in mouse, rat, rabbit, guinea pig, dog, and human. Drug Metab. Dispos. 31:731-741. (Pubitemid 36617661)
43. Sugar AM, Liu XP. 2000. Effect of grapefruit juice on serum voriconazole concentrations in the mouse. Med. Mycol. 38:209-212. (Pubitemid 30391932)
44. Clemons KV, Espiritu M, Parmar R, Stevens DA. 2005. Comparative efficacies of conventional amphotericin B, liposomal amphotericin B (AmBisome), caspofungin, micafungin, and voriconazole alone and in combination against experimental murine central nervous system aspergillosis. Antimicrob. Agents Chemother. 49:4867-4875. (Pubitemid 41778896)
45. Johnson MD, MacDougall C, Ostrosky-Zeichner L, Perfect JR, Rex JH. 2004. Combination antifungal therapy. Antimicrob. Agents Chemother. 48:693-715. (Pubitemid 38280314)
46. Meletiadis J, Petraitis V, Petraitiene R, Lin P, Stergiopoulou T, Kelaher AM, Sein T, Schaufele RL, Bacher J, Walsh TJ. 2006. Triazole-polyene antagonism in experimental invasive pulmonary aspergillosis: in vitro and in vivo correlation. J. Infect. Dis. 194:1008-1018. (Pubitemid 44454087)
47. Sugar AM, Liu XP. 1998. Interactions of itraconazole with amphotericin B in the treatment of murine invasive candidiasis. J. Infect. Dis. 177:1660-1663. (Pubitemid 28243592)
48. Clemons KV, Parmar R, Martinez M, Stevens DA. 2006. Efficacy of Abelcet alone, or in combination therapy, against experimental central nervous system aspergillosis. J. Antimicrob. Chemother. 58:466-469. (Pubitemid 44294969)
49. Cornely OA, Maertens J, Bresnik M, Ullmann AJ, Ebrahimi R, Herbrecht R. 2010. Treatment outcome of invasive mould disease after sequential exposure to azoles and liposomal amphotericin B. J. Antimicrob. Chemother. 65:114-117.
50. Slesiona S, Ibrahim-Granet O, Olias P, Brock M, Jacobsen ID. 2012. Murine infection models for Aspergillus terreus pulmonary aspergillosis reveal long-term persistence of conidia and liver degeneration. J. Infect. Dis. 205:1268-1277.