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1 JCM Accepts, published online ahead of print on 26 May 2010 J. Clin. Microbiol. doi: /jcm Copyright 2010, American Society for Microbiology and/or the Listed Authors/Institutions. All Rights Reserved. 1 2 In Vitro Activity of Anidulafungin and Other Agents Against Esophageal Candidiasis Isolates from a Phase 3 Clinical Trial M. A. Pfaller 1, 2 *, R. Hollis 1, B. P. Goldstein 4, S. Messer 1, D. Diekema 1, 3, T. Henkel 5 ; Departments of Pathology 1, Epidemiology 2, and Medicine 3, University of Iowa College of Medicine and College of Public Health, Iowa City, Iowa 52242, Wayne, Pennsylvania , and Ception Therapeautics 5, Malvern, Pennsylvania Key Words: Anidulafungin, Candida, Fluconazole, Clinical trial, Esophageal candidiasis Short running title: Notes *Corresponding author: Michael A. Pfaller, M.D. Medical Microbiology Division, C606 GH Department of Pathology University of Iowa College of Medicine Iowa City, Iowa Phone: (319) Fax: (319) michael-pfaller@uiowa.edu 1

2 The efficacy of anidulafungin, an echinocandin antifungal agent with potent anti-candida activity, in treating esophageal candidiasis was tested in a double-blind study vs. oral fluconazole. Isolates were identified and tested for susceptibility. C. albicans represented >90% of baseline isolates. The MIC 90 of anidulafungin for all strains was 0.06 mg/l. 2

3 Anidulafungin is an echinocandin antifungal agent with broad-spectrum activity against Candida (2,12,13,17,19,20), including fluconazole-resistant strains (10,16), concentration dependent fungicidal activity and a long post-antifungal effect in vitro and in animal infection models (1,6,7,10,16,18). It is available in the US for intravenous treatment of esophageal candidiasis, a debilitating opportunistic infection among persons with HIV infection (9) for which cross resistance among azoles may limit treatment options (4,14). In patients treated with the anidulafungin dosage regimen for esophageal candidiasis (100 mg loading dose followed by 50 mg daily, half of the dosage used for invasive candidiasis) the steady-state mean maximum and minimum plasma concentrations were 4.2 and 1.6 µg/ml (Eraxis US Package Insert). Thus, anidulafungin may be a useful alternative to both amphotericin B and the azole antifungal agents in treating severe oral and esophageal candidiasis in persons with HIV infection and acquired immunodeficiency syndrome (AIDS). We determined the in vitro activity of anidulafungin against clinical isolates of Candida spp. from esophageal candidiasis patients, most of them HIV-infected, enrolled in a large (601 patients) Phase 3 randomized, comparative, double-blind, double-dummy clinical study. The comparator was oral fluconazole, 200 mg administered on day 1 followed by 100 mg daily for days. Candida isolates obtained from endoscopic biopsies or brushings (11) were sent to a reference laboratory for identification, using standard methods (8), and susceptibility testing. Standard antifungal powders included anidulafungin (Vicuron, Inc. King of Prussia, PA), fluconazole (Pfizer, New York, NY), voriconazole (Pfizer), caspofungin (Merck, Whitehouse Station, PA), flucytosine (Sigma, St. Louis, MO), amphotericin B (Sigma) and itraconazole (Janssen, Beerse, Belgium). Preparation of stock solutions and broth microdilution susceptibility testing were as detailed in CLSI document M27-A2 (5,15) for all agents except amphotericin B 3

4 (tested in Antibiotic Medium 3). Incubation at 35 C was for 24 h (echinocandins) and 48 h (azoles, amphotericin B, flucytosine). MICs, determined using a reading mirror, were defined as prominent decrease in turbidity (ca. 50%), except for amphotericin B (complete growth inhibition). Overall, 96% of patients in both treatment arms were infected with C. albicans at baseline, with or without additional Candida species. A majority of the non-albicans species isolated at baseline were present in mixed infection with C. albicans. The predominance of C. albicans is characteristic of esophageal candidiasis (3). A total of 441 unique baseline isolates were received by the reference laboratory, including 411 Candida albicans, 23 Candida glabrata, 3 Candida tropicalis, 2 Candida krusei, and one isolate each of Candida pelliculosa and Candida lusitaniae. Anidulafungin had potent activity against these isolates (Table 1). Its MIC 90 was 0.06 µg/ml and 99% of strains were inhibited by 0.12 µg/ml. The MIC distribution for caspofungin was similar. Micafungin was not available for testing at the time the study was conducted. For all of the azoles, susceptibility was greater than 90%. The MIC 50/90 of fluconazole for the 23 C. glabrata isolates were 8/16 µg/ml. Fluconazole-resistant strains included 3 C. albicans and 1 C. glabrata (MIC, 64 µg/ml) as well as the 2 C. krusei (considered resistant irrespective of MIC). The MIC range of anidulafungin for these 6 isolates was µg/ml. As noted previously, there is no cross resistance between azoles and echinocandins (10,13,20). As reported previously, the overall clinical and mycological efficacy of anidulafungin, evaluated at the end of therapy, was non-inferior to that of fluconazole (11). Eradication of Candida from the esophagus was either proven by a negative culture at the time of evaluation, or presumed on the basis of endoscopic improvement with no culture obtained (e.g., if there were 4

5 no lesions to be cultured). On a per patient basis, which requires eradication of all baseline pathogens from a patient, mycological success rates were, respectively, 87 and 91% for anidulafungin and fluconazole (11). Among the Candida isolates tested at the reference laboratory, there were too few in the fluconazole treatment arm that were fluconazole-resistant or, in the anidulafungin arm that had anidulafungin MICs >0.06 µg/ml to permit correlation between eradication of individual isolates and level of susceptibility. Currently, attempts are underway to rationalize susceptibility breakpoints for echinocandins (21,22). These analyses are based on the dosage utilized for the treatment of invasive candidiasis which, in the case of anidulafungin, is twice that used in the treatment of esophageal candidiasis. In conclusion, characterization of Candida esophageal isolates from a large clinical trial confirmed the potent in vitro activity of anidulafungin against both susceptible and fluconazoleresistant isolates seen in previous non-clinical studies. When determined at end of therapy, anidulafungin and fluconazole had similar efficacy in eradicating infecting organisms from esophageal lesions. 5

6 Beth Goldstein was an employee of Vicuron Pharmaceuticals Inc during the development of anidulafungin for treatment of esophageal candidiasis and is currently a consultant for Pfizer Inc. 89 6

7 90 REFERENCES Andes, D., D. J. Diekema., M. A. Pfaller, R. A. Prince, K. Marchillo, J. Ashbeck, and J. Hou In vivo pharmacodynamic characterization of anidulafungin in a neutropenic murine candidiasis model. Antimicrob. Agents Chemother. 52: Arevalo, M. P., A. J. Carrillo-Munoz, J. Salgado, D. Cardenes, S. Brio, G. Quindos, and A. Espinel-Ingroff Antifungal activity of the echinocandin anidulafungin (VER002, LY ) against yeast pathogens: a comparative study with M27-A microdilution method. J. Antimicrob. Chemother. 51: Bonacini, M., T. Young, and L. Laine The causes of esophageal symptoms in human immunodeficiency virus infection. A prospective study of 110 patients. Arch. Intern. Med. 151: Cartledge, J. D., J. Midgley, and B. G. Gazzard Clinically significant azole crossresistance in Candida isolates from HIV-positive patients with oral candidosis. AIDS. 11: CLSI Quality Control MIC Limits for Broth Microdilution; Informational Supplement M27-S2. CLSI, Wayne, PA. 6. Ernst, E. J., M. E. Klepser, and M. A. Pfaller Postantifungal effects of echinocandin, azole, and polyene antifungal agents against Candida albicans and Cryptococcus neoformans. Antimicrob. Agents Chemother. 44: Groll, A. H., D. Mickiene, R. Petraitiene, V. Petraitis, C. A. Lyman, J. S. Bacher, S. C. 7

8 Piscitelli, and T. J. Walsh Pharmacokinetic and pharmacodynamic modeling of anidulafungin (LY303366): reappraisal of its efficacy in neutropenic animal models of opportunistic mycoses using optimal plasma sampling. Antimicrob. Agents Chemother. 45: Hazen, K. C., and S. A. Howell Candida, Cryptococcus, and other yeasts of medical importance, p In P. R. Murray, E. J. Baron, J. H. Jorgensen, M. A. Pfaller, and R. H. Yolken (ed.), Manual of Clinical Microbiology 8th ed. ASM Press, Washington, D.C. 9. Horgan, M. M., and W. G. Powderly Oral fungal infections, p In E. J. Anaissie, M. R. McGinnis, and M. A. Pfaller (ed.), Clinical Mycology, Churchill Livingstone, New York. 10. Karlowsky J. A., G. A. Harding, S. A. Zelenitsky, D. J. Hoban, A. Kabani, T. V. Balko, M. A. Turik, and G. G. Zhanel In vitro kill curves of a new semisynthetic echinocandin, LY303366, against fluconazole-sensitive and -resistant Candida species. Antimicrob. Agents Chemother. 141: Krause D. S., A. E. Simjee, C. van Rensburg, J. Viljoen, T. J. Walsh, B. P. Goldstein, M. Wible, and T. Henkel A randomized, double-blind trial of anidulafungin versus fluconazole for the treatment of esophageal candidiasis. Clin. Infect. Dis. 39: Messer S. A., J. T. Kirby, H. S. Sader, T. R. Fritsche, and R. N. Jones Initial results from a longitudinal international surveillance programme for anidulafungin (2003). J. Antimicrob. Chemother. 54:

9 Messer S. A., G. J. Moet, J. T. Kirby, and R. N. Jones Activity of contemporary antifungal agents, including the novel echinocandin anidulafungin, tested against Candida spp., Cryptococcus spp., and Aspergillus spp.: report from the SENTRY Antimicrobial Surveillance Program (2006 to 2007). J. Clin. Microbiol. 47: Müller, F.-M. C., M. Weig, J. Peter, and T. J. Walsh Azole cross-resistance to ketoconazole, fluconazole, itraconazole, and voriconazole in clinical Candida albicans isolates from HIV-infected children with oropharyngeal candidosis. J. Antimicrob. Chemother. 46: NCCLS Reference Method for Broth Dilution Antifungal Susceptibility Testing of Yeasts; Approved Standard--Second Edition. NCCLS document M27-A2. NCCLS, Wayne, Pennsylvania, Nguyen K. T., P. Ta, B. T. Hoang, S. Cheng, B. Hao, M. H. Nguyen, and C. J. Clancy Anidulafungin is fungicidal and exerts a variety of postantifungal effects against Candida albicans, C. glabrata, C. parapsilosis, and C. krusei isolates. Antimicrob. Agents Chemother. 53: Ostrosky-Zeichner L., J. H. Rex, P. G. Pappas, R. J. Hamill, R. A. Larsen, H. W. Horowitz, W. G. Powderly, N. Hylsop, C. A. Kauffman, J. Cleary, J. E. Mangino, and J. Lee Antifungal susceptibility survey of 2000 bloodstream Candida isolates in the United States. Antimicrob. Agents Chemother. 47: Petraitiene, R., V. Petraitis, A. H. Groll, M. Candelario, T. Sein, A. Bell, C. A. Lyman, C. L. McMillian, J. Bacher, and T. J. Walsh Antifungal activity of LY303366, a 9

10 novel echinocandin B, in experimental disseminated candidiasis in rabbits. Antimicrob. Agents Chemother. 43: Pfaller, M. A., D. J. Diekema, S. A. Messer, R. J. Hollis, and R. N. Jones In vitro activities of caspofungin compared with those of fluconazole and itraconazole against 3, 959 clinical isolates of Candida spp., including 157 fluconazole-resistant isolates. Antimicrob. Agents Chemother. 47: Pfaller M. A., L. Boyken, R. J. Hollis, J. Kroeger, S. A. Messer, S. Tendolkar, and D. J. Diekema In vitro susceptibility of invasive isolates of Candida spp. to anidulafungin, caspofungin and micafungin: six years of global surveillance. J. Clin. Microbiol. 46: Pfaller, M.A., D. J. Diekema, L. Ostrosky-Zeichner, J. H. Rex, B. D. Alexander, D. Andes, S. D. Brown, V. Chaturvedi, M. A. Ghannoum, C. C. Knapp, D. J. Sheehan, and T. J. Walsh Correlation of MIC with outcome for Candida species tested against caspofungin, anidulafungin, and micafungin: analysis and proposal for interpretive MIC breakpoints. J. Clin. Microbiol. 46: Pfaller, M. A., L. Boyken R. J. Hollis, J. Kroeger, S. A. Messer, S. Tendolkar, R. N. Jones, J. Turnidge, and D. J. Diekema Wild-type MIC distributions and epidemiological cutoff values for the echinocandins and Candida spp. J. Clin. Microbiol. 48:

11 Table 1. In vitro susceptibility of 441 esophageal isolates of Candida spp. to anidulafungin and six other systemically active antifungal agents Antifungal Cumulative % inhibited at the following MIC (µg/ml) agent Anidulafungin Caspofungin a Fluconazole Voriconazole Itraconazole Flucytosine Amphotericin B a Caspofungin was tested against 404 isolates. 11

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