Molecular identification and antifungal susceptibility profile of Aspergillus flavus isolates recovered from clinical specimens in Kuwait

BMC Infectious Diseases

Volumn 13, Issue 1, 2013, Pages

  Al Wathiqi, Faten ^a   Ahmad, Suhail ^a   Khan, Ziauddin ^a  

^a KUWAIT UNIVERSITY   (Kuwait)

Author keywords

tubulin and calmodulin genes; Amphotericin B; Antifungal susceptibility; Aspergillus flavus; Echinocandins; Etest; Molecular characterization; Triazoles

Indexed keywords

AMPHOTERICIN B; ANIDULAFUNGIN; BETA TUBULIN; CALMODULIN; CASPOFUNGIN; ECHINOCANDIN; GENOMIC DNA; MICAFUNGIN; POSACONAZOLE; TRIAZOLE DERIVATIVE; VORICONAZOLE;

AGAR MEDIUM; ANALYTICAL EQUIPMENT; ANTIFUNGAL SUSCEPTIBILITY; ARTICLE; ASPERGILLUS FLAVUS; ASPERGILLUS PARASITICUS; BETA TUBULIN GENE; CALMODULIN GENE; CONTROLLED STUDY; DISK DIFFUSION; EPSILOMETER TEST; FUNGAL STRUCTURES; FUNGUS IDENTIFICATION; FUNGUS ISOLATION; GENETIC ANALYSIS; IN VITRO STUDY; KUWAIT; MINIMUM INHIBITORY CONCENTRATION; NONHUMAN; NUCLEOTIDE SEQUENCE; SEQUENCE ANALYSIS; TAXON;

AMPHOTERICIN B; ANTIFUNGAL AGENTS; ASPERGILLOSIS; ASPERGILLUS FLAVUS; GENES, FUNGAL; HUMANS; KUWAIT; MICROBIAL SENSITIVITY TESTS; PHYLOGENY; PYRIMIDINES; STATISTICS, NONPARAMETRIC; TRIAZOLES;

EID: 84874538574     PISSN: None     EISSN: 14712334     Source Type: Journal    
DOI: 10.1186/1471-2334-13-126     Document Type: Article

References (49)

1. Dasbach EJ, Davies GM, Teutsch SM. Burden of aspergillosis-related hospitalizations in the United States. Clin Infect Dis 2000, 31:1524-1528. 10.1086/317487, 11096031.
2. Krishnan S, Manavathu EK, Chandrasekar PH. Aspergillus flavus: an emerging non-fumigatus Aspergillus species of significance. Mycoses 2009, 52:206-222. 10.1111/j.1439-0507.2008.01642.x, 19207851.
3. Hageskal G, Kristensen R, Fristad RF, Skaar I. Emerging pathogen Aspergillus calidoustus colonizes water distribution systems. Med Mycol 2011, 49:588-593.
4. Coelho D, Silva S, Vale-Silva LS, Gomes H, Pinto EN, Sarmento AN, Pinheiro M. Aspergillus viridinutans: an agent of adult chronic invasive aspergillosis. Med Mycol 2011, 49:755-759.
5. Fadl FA, Hassan KM, Faizuddin M. Allergic fungal rhinosinusitis: report of 4 cases from Saudi Arabia. Saudi Med J 2000, 21:581-584.
6. Al-Dousary SH. Allergic fungal sinusitis: radiological and microbiological features of 59 cases. Am J Otolaryngol 2004, 25:213-218. 10.1016/j.amjoto.2003.12.003, 15124174.
7. Taj-Aldeen SJ, Hilal AA, Chong-Lopez A. Allergic Aspergillus flavus rhinosinusitis: a case report from Qatar. Eur Arch Otorhinolaryngol 2003, 260:331-335. 10.1007/s00405-002-0547-x, 12883959.
8. Taj-Aldeen SJ, Hilal AA, Schell WA. Allergic fungal rhinosinusitis: a report of 8 cases. Ann Saudi Med 2008, 28:17-21. 10.4103/0256-4947.51772, 18299641.
9. Hedayati MT, Bahoosh M, Kasiri A, Ghasemi M, Motahhari SJ, Poormosa R. Prevalence of fungal rhinosinusitis among patients with chronic rhinosinusitis from Iran. J Med Mycol 2010, 20:298-303.
10. Khan ZU, Ahmad S, Mokaddas E, Said T, Nair MP, Halim MA, Nampoory MR, McGinnis MR. Cerebral aspergillosis diagnosed by detection of Aspergillus flavus-specific DNA, galactomannan and (1@@3)-beta-D-glucan in clinical specimens. J Med Microbiol 2007, 56:129-132. 10.1099/jmm.0.46549-0, 17172527.
11. Hedayati MT, Pasqualotto AC, Warn PA, Bowyer P, Denning DW. Aspergillus flavus: human pathogen, allergen and mycotoxin producer. Microbiology 2007, 153:1677-692. 10.1099/mic.0.2007/007641-0, 17526826.
12. Khan ZU, Sanyal SC, Mokaddas E, Vislocky I, Anim JT, Salama AL, Shuhaiber H. Endocarditis due to Aspergillus flavus. Mycoses 1997, 40:213-217. 10.1111/j.1439-0507.1997.tb00217.x, 9476491.
13. Clinical and Laboratory Standards Institute Reference method for broth dilution antifungal susceptibility testing for filamentous fungi; approved standard. Document M38-A2 2008, Wayne, PA: Clinical and Laboratory Standards Institute, Clinical and Laboratory Standards Institute.
14. Espinel-Ingroff A, Cuenca-Estrella M, Fothergill A, Fuller J, Ghannoum M, Johnson E, Pelaez T, Pfaller MA, Turnidge J. Wild-type MIC distributions and epidemiological cutoff values for amphotericin B and Aspergillus spp. for the CLSI broth microdilution method (M38-A2 document). Antimicrob Agents Chemother 2011, 55:5150-5154. 10.1128/AAC.00686-11, 3195003, 21876047.
15. Espinel-Ingroff A, Fothergill A, Fuller J, Johnson E, Pelaez T, Turnidge J. Wild-type MIC distributions and epidemiological cutoff values for caspofungin and Aspergillus spp. for the CLSI broth microdilution method (M38-A2 document). Antimicrob Agents Chemother 2011, 55:2855-2859. 10.1128/AAC.01730-10, 3101428, 21422219.
16. Espinel-Ingroff A, Diekema DJ, Fothergill A, Johnson E, Pelaez T, Pfaller MA, Rinaldi MG, Canton E, Turnidge J. Wild-type MIC distributions and epidemiological cutoff values for the triazoles and six Aspergillus spp. for the CLSI broth microdilution method (M38-A2 document). J Clin Microbiol 2010, 48:3251-7. 10.1128/JCM.00536-10, 2937688, 20592159.
17. van der Linden JW, Snelders E, Kampinga GA, Rijnders BJ, Mattsson E, Debets-Ossenkopp YJ, Kuijper EJ, Van Tiel FH, Melchers WJ, Verweij PE. Clinical implications of azole resistance in Aspergillus fumigatus, The Netherlands, 2007-2009. Emerg Infect Dis 2011, 17:1846-1854. 10.3201/eid1710.110226, 3311118, 22000354.
18. Chowdhary A, Kathuria S, Randhawa HS, Gaur SN, Klaassen CH, Meis JF. Isolation of multiple-triazole-resistant Aspergillus fumigatus strains carrying the TR/L98H mutations in the cyp51A gene in India. J Antimicrob Chemother 2012, 67:362-366. 10.1093/jac/dkr443, 22028200.
19. Espinel-Ingroff A. Evaluation of broth microdilution testing parameters and agar diffusion Etest procedure for testing susceptibilities of Aspergillus spp. to caspofungin acetate (MK-0991). J Clin Microbiol 2003, 41:403-409. 10.1128/JCM.41.1.403-409.2003, 149640, 12517880.
20. Espinel-Ingroff A, Rezusta A. E-test method for testing susceptibilities of Aspergillus spp. to the new triazoles voriconazole and posaconazole and to established antifungal agents: comparison with NCCLS broth microdilution method. J Clin Microbiol 2002, 40:2101-2107. 10.1128/JCM.40.6.2101-2107.2002, 130678, 12037072.
21. Martos AI, Martín-Mazuelos E, Romero A, Serrano C, González T, Almeida C, Puche B, Cantón E, Pemán J, Espinel-Ingroff A. Evaluation of disk diffusion method compared to broth microdilution for antifungal susceptibility testing of 3 echinocandins against Aspergillus spp. Diagn Microbiol Infect Dis 2012, 73:53-56. 10.1016/j.diagmicrobio.2012.01.006, 22480568.
22. Martos AI, Romero A, González MT, González A, Serrano C, Castro C, Pemán J, Cantón E, Martín-Mazuelos E. Evaluation of the Etest method for susceptibility testing of Aspergillus spp. and Fusarium spp. to three echinocandins. Med Mycol 2010, 48:858-861. 10.3109/13693781003586943, 20144131.
23. Klich MA. Identification of common Aspergillus species 2002, Utrecht, The Netherlands: Centraalbureau voor Schimmelcultures Publication.
24. Ahmad S, Khan ZU, Theyyathel AM. Diagnostic value of DNA, (1-3)-beta-d-glucan, and galactomannan detection in serum and bronchoalveolar lavage of mice experimentally infected with Aspergillus terreus. Diagn Microbiol Infect Dis 2007, 59:165-171. 10.1016/j.diagmicrobio.2007.04.009, 17574786.
25. Khan Z, Ahmad S, Al-Ghimlas F, Al-Mutairi S, Joseph L, Chandy R, Sutton DA, Guarro J. Purpureocillium lilacinum as a cause of cavitary pulmonary disease: a new clinical presentation and observations on atypical morphologic characteristics of the isolate. J Clin Microbiol 2012, 50:1800-1804. 10.1128/JCM.00150-12, 3347118, 22322350.
26. European Committee on Antimicrobial Susceptibility Testing 2013, (http://www.eucast.org/antifungal_susceptibility_testing_afst/): Antifungal agents - Breakpoint tables for interpretation of MICs, Version 5.0, European Committee on Antimicrobial Susceptibility Testing.
27. Espinel-Ingroff A, Canton E, Fothergill A, Ghannoum M, Johnson E, Jones RN, Ostrosky-Zeichner L, Schell W, Gibbs DL, Wang A, Turnidge J. Quality control guidelines for amphotericin B, itraconazole, posaconazole, and voriconazole disk diffusion susceptibility tests with non-supplemented Mueller-Hinton Agar (CLSI M51-A document) for nondermatophyte filamentous fungi. J Clin Microbiol 2011, 49:2568-2571. 10.1128/JCM.00393-11, 3147863, 21543581.
28. Clinical Laboratory Standards Institute Development of in vitro susceptibility testing criteria and quality control parameters; approved guideline, 3rd ed 2008, Villanova, PA: CLSI document M23-A3: Clinical and Laboratory Standards Institute, Clinical Laboratory Standards Institute.
29. Varga J, Frisvad JC, Samson RA. Two new aflatoxin producing species, and an overview of Aspergillus section Flavi. Studies Mycol 2011, 69:57-80.
30. Colozza C, Posteraro B, Santilli S, De Carolis E, Sanguinetti M, Girmenia C. In vitro activities of amphotericin B and Am Bisome against Aspergillus isolates recovered from Italian patients treated for haematological malignancies. Int J Antimicrob Agents 2012, 39:440-443. 10.1016/j.ijantimicag.2012.01.013, 22429723.
31. Lass-Flörl C, Kofler G, Kropshofer G, Hermans J, Kreczy A, Dierich MP, Niederwieser D. In-vitro testing of susceptibility to amphotericin B is a reliable predictor of clinical outcome in invasive aspergillosis. J Antimicrob Chemother 1998, 42:497-502. 10.1093/jac/42.4.497, 9818749.
32. Badiee P, Alborzi A, Moeini M, Haddadi P, Farshad S, Japoni A, Ziyaeyan M. Antiungal susceptibility of the Aspergillus species by Etest and CLSI reference methods. Arch Iran Med 2012, 15:429-432.
33. Hadrich I, Makni F, Neji S, Cheikhrouhou F, Bellaaj H, Elloumi M, Ayadi A, Ranque S. Amphotericin B in vitro resistance is associated with fatal Aspergillus flavus infection. Med Mycol 2012, 50:829-834. 10.3109/13693786.2012.684154, 22587728.
34. Pfaller MA, Messer SA, Boyken L, Rice C, Tendolkar S, Hollis RJ, Diekema DJ. In vitro survey of triazole cross-resistance among more than 700 clinical isolates of Aspergillus species. J Clin Microbiol 2008, 46:2568-2572. 10.1128/JCM.00535-08, 2519461, 18562581.
35. Mittal V, Mittal R, Sharma PC. Voriconazole-refractory fungal infection of phacoemulsification tunnel. Indian J Ophthalmol 2010, 58:434-437. 10.4103/0301-4738.67072, 2992924, 20689204.
36. Liu W, Sun Y, Chen W, Liu W, Wan Z, Bu D, Li R. T778G mutation in cyp51C gene confers voriconazole-resistance in Aspergillus flavus causing aspergillosis. Antimicrob Agents Chemother 2012, 56:2598-2603. 10.1128/AAC.05477-11, 3346632, 22314539.
37. Krishnan-Natesan S, Chandrasekar PH, Alangaden GJ, Manavathu EK. Molecular characterisation of cyp51A and cyp51B genes coding for P450 14alpha-lanosterol demethylases A (CYP51Ap) and B (CYP51Bp) from voriconazole-resistant laboratory isolates of Aspergillus flavus. Int J Antimicrob Agents 2008, 32:519-524. 10.1016/j.ijantimicag.2008.06.018, 18775650.
38. Araujo R, Pina-Vaz C, Rodrigues AG. Susceptibility of environmental versus clinical strains of pathogenic Aspergillus. Int J Antimicrob Agents 2007, 29:108-111. 10.1016/j.ijantimicag.2006.09.019, 17189101.
39. Pfaller MA, Boyken L, Hollis RJ, Kroeger J, Messer SA, Tendolkar S, Diekema DJ. In vitro susceptibility of clinical isolates of Aspergillus spp. to anidulafungin, caspofungin, and micafungin: a head-to-head comparison using the CLSI M38-A2 broth microdilution method. J Clin Microbiol 2009, 47:3323-3325. 10.1128/JCM.01155-09, 2756949, 19710267.
40. Shivaprakash MR, Geertsen E, Chakrabarti A, Mouton JW, Meis JF. In vitro susceptibility of 188 clinical and environmental isolates of Aspergillus flavus for the new triazole isavuconazole and seven other antifungal drugs. Mycoses 2011, 54:e583-589. 10.1111/j.1439-0507.2010.01996.x, 21518026.
41. Pfaller MA, Messer SA, Boyken L, Hollis RJ, Diekema DJ. In vitro susceptibility testing of filamentous fungi: comparison of Etest and reference M38-A microdilution methods for determining posaconazole MICs. Diagn Microbiol Infect Dis 2003, 45:241-244. 10.1016/S0732-8893(02)00544-8, 12729993.
42. Messer SA, Diekema DJ, Hollis RJ, Boyken LB, Tendolkar S, Kroeger J, Pfaller MA. Evaluation of disk diffusion and Etest compared to broth microdilution for antifungal susceptibility testing of posaconazole against clinical isolates of filamentous fungi. J Clin Microbiol 2007, 45:1322-1324. 10.1128/JCM.02450-06, 1865846, 17267623.
43. Pfaller MA, Messer SA, Mills K, Bolmström A. In vitro susceptibility testing of filamentous fungi: comparison of Etest and reference microdilution methods for determining itraconazole MICs. J Clin Microbiol 2000, 38:3359-3361. 87386, 10970383.
44. Ozkutuk A, Ergon C, Metin DY, Yucesoy M, Polat SH. Comparison of disk diffusion, E-test and broth microdilution test in determination of susceptibility of Aspergillus species to amphotericin B, itraconazole and voriconazole. J Chemother 2008, 20:87-92.
45. Pfaller JB, Messer SA, Hollis RJ, Diekema DJ, Pfaller MA. In vitro susceptibility testing of Aspergillus spp.: comparison of Etest and reference microdilution methods for determining voriconazole and itraconazole MICs. J Clin Microbiol 2003, 41:1126-1129. 10.1128/JCM.41.3.1126-1129.2003, 150323, 12624040.
46. Guinea J, Peláez T, Alcalá L, Bouza E. Correlation between the Etest and the CLSI M-38 A microdilution method to determine the activity of amphotericin B, voriconazole, and itraconazole against clinical isolates of Aspergillus fumigatus. Diagn Microbiol Infect Dis 2007, 57:273-276. 10.1016/j.diagmicrobio.2006.09.003, 17141455.
47. Espinel-Ingroff A, Arthington-Skaggs B, Iqbal N, Ellis D, Pfaller MA, Messer S, Rinaldi M, Fothergill A, Gibbs DL, Wang A. Multicenter evaluation of a new disk agar diffusion method for susceptibility testing of filamentous fungi with voriconazole, posaconazole, itraconazole, amphotericin B, and caspofungin. J Clin Microbiol 2007, 45:1811-1820. 10.1128/JCM.00134-07, 1933077, 17428932.
48. Espinel-Ingroff A, Canton E. Comparison of Neo-Sensitabs tablet diffusion assay with CLSI broth microdilution M38-A and disk diffusion methods for testing susceptibility of filamentous fungi with amphotericin B, caspofungin, itraconazole, posaconazole, and voriconazole. J Clin Microbiol 2008, 46:1793-1803. 10.1128/JCM.01883-07, 2395104, 18337384.
49. Laboratory Standards Institute Performance standards for antifungal disk diffusion susceptibility testing of non-dermatophyte filamentous fungi; Informational supplement, 1st ed. CLSI document M51-A 2010, Wayne, PA: Clinical and Laboratory Standards Institute, Laboratory Standards Institute.