Antifungal drug susceptibility and phylogenetic diversity among Cryptococcus isolates from dogs and cats in North America

Journal of Clinical Microbiology

Volumn 52, Issue 6, 2014, Pages 2061-2070

  Singer, Lisa M ^a   Meyer, Wieland ^b   Firacative, Carolina ^b,c   Thompson III, George R ^d   Samitz, Eileen ^e   Sykes, Jane E ^e  

^a MICHIGAN STATE UNIVERSITY   (United States)

^b UNIVERSITY OF SYDNEY   (Australia)

^c INSTITUTO NACIONAL DE SALUD   (Colombia)

^d UNIVERSITY OF CALIFORNIA   (United States)

^e UNIVERSITY OF CALIFORNIA   (United States)

Author keywords

[No Author keywords available]

Indexed keywords

AMPHOTERICIN B; ANIDULAFUNGIN; CASPOFUNGIN; FLUCONAZOLE; FLUCYTOSINE; ITRACONAZOLE; MICAFUNGIN; POSACONAZOLE; VORICONAZOLE; ANTIFUNGAL AGENT;

ANTIFUNGAL SUSCEPTIBILITY; ARTICLE; BROTH DILUTION; CAT; CONTROLLED STUDY; CRYPTOCOCCUS GATTII; CRYPTOCOCCUS NEOFORMANS; DOG; FUNGUS ISOLATION; GENETIC VARIABILITY; HUMAN VERSUS ANIMAL COMPARISON; LABORATORY DEVICE; MULTILOCUS SEQUENCE TYPING; NONHUMAN; NORTH AMERICA; NUCLEOTIDE SEQUENCE; PHYLOGENY; POLYMERASE CHAIN REACTION; PRIORITY JOURNAL; RESTRICTION FRAGMENT LENGTH POLYMORPHISM; SEQUENCE HOMOLOGY; ANIMAL; CAT DISEASE; CLASSIFICATION; CLUSTER ANALYSIS; CRYPTOCOCCOSIS; DNA FINGERPRINTING; DNA SEQUENCE; DOG DISEASE; DRUG EFFECTS; FEMALE; FILOBASIDIELLA; GENETICS; GENOTYPE; HUMAN; ISOLATION AND PURIFICATION; MALE; MICROBIAL SENSITIVITY TEST; MICROBIOLOGICAL EXAMINATION; MICROBIOLOGY; MOLECULAR GENETICS; VETERINARY;

ANIMALS; ANTIFUNGAL AGENTS; CAT DISEASES; CATS; CLUSTER ANALYSIS; CRYPTOCOCCOSIS; CRYPTOCOCCUS; DNA FINGERPRINTING; DOG DISEASES; DOGS; FEMALE; GENETIC VARIATION; GENOTYPE; HUMANS; MALE; MICROBIAL SENSITIVITY TESTS; MOLECULAR SEQUENCE DATA; MULTILOCUS SEQUENCE TYPING; MYCOLOGICAL TYPING TECHNIQUES; NORTH AMERICA; PHYLOGENY; POLYMORPHISM, RESTRICTION FRAGMENT LENGTH; SEQUENCE ANALYSIS, DNA;

EID: 84901659786     PISSN: 00951137     EISSN: 1098660X     Source Type: Journal    
DOI: 10.1128/JCM.03392-13     Document Type: Article

References (49)

1. Sykes JE, Malik R. 2014. Cryptococcosis, p 599-612. In Sykes JE (ed), Canine and feline infectious diseases. Elsevier, St. Louis, MO.
2. Fries BC, Cox GM. 2011. Cryptococcosis in AIDS, p 515-525. In Heitman J, Kozel TR, Kwon-Chung KJ, Perfect J, Casadevall A (ed), Cryptococcus-from human pathogen to model yeast. ASM Press, Washington, DC.
3. Bartlett KH, Kidd SE, Kronstad JW. 2008. The emergence of Cryptococcus gattii in British Columbia and the Pacific Northwest. Curr. Infect. Dis. Rep. 10:58-65. http://dx.doi.org/10.1007/s11908-008-0011-1 (Pubitemid 351419363)
4. O'Brien CR, Krockenberger MB, Wigney DI, Martin P, Malik R. 2004. Retrospective study of feline and canine cryptococcosis in Australia from 1981 to 2001: 195 cases. Med. Mycol. 42:449-460. http://dx.doi.org/10.1080/ 13693780310001624547 (Pubitemid 39445477)
5. Trivedi SR, Malik R, Meyer W, Sykes JE. 2011. Feline cryptococcosis: impact of current research on clinical management. J. Feline Med. Surg. 13:163-172. http://dx.doi.org/10.1016/j.jfms.2011.01.009
6. Trivedi SR, Sykes JE, Cannon MS, Wisner ER, Meyer W, Sturges BK, Dickinson PJ, Johnson LR. 2011. Clinical features and epidemiology of cryptococcosis in cats and dogs in California: 93 cases (1988-2010). J. Am. Vet. Med. Assoc. 239:357-369. http://dx.doi.org/10.2460/javma.239.3 .357
7. Sudan A, Livermore J, Howard SJ, Al-Nakeeb Z, Sharp A, Goodwin J, Gregson L, Warn PA, Felton TW, Perfect JR, Harrison TS, Hope WW. 2013. Pharmacokinetics and pharmacodynamics of fluconazole for cryptococcal meningoencephalitis: implications for antifungal therapy and in vitro susceptibility breakpoints. Antimicrob. Agents Chemother. 57: 2793-2800. http://dx.doi.org/10.1128/AAC. 00216-13
8. O'Brien CR, Krockenberger MB, Martin P, Wigney DI, Malik R. 2006. Long-term outcome of therapy for 59 cats and 11 dogs with cryptococcosis. Aust. Vet. J. 84:384-392. http://dx.doi.org/10.1111/j.1751-0813.2006.00040.x. (Pubitemid 46639248)
9. Sykes JE, Sturges BK, Cannon MS, Gericota B, Higgins RJ, Trivedi SR, Dickinson PJ, Vernau KM, Meyer W, Wisner ER. 2010. Clinical signs, imaging features, neuropathology, and outcome in cats and dogs with central nervous system cryptococcosis from California. J. Vet. Intern. Med. 24:1427-1438. http://dx.doi.org/10.1111/j.1939-1676.2010.0633.x.
10. McGill S, Malik R, Saul N, Beetson S, Secombe C, Robertson I, Irwin P. 2009. Cryptococcosis in domestic animals in Western Australia: a retrospective study from 1995-2006. Med. Mycol. 47:625-639. http://dx.doi.org/10.1080/ 13693780802512519
11. Lester SJ, Kowalewich NJ, Bartlett KH, Krockenberger MB, Fairfax TM, Malik R. 2004. Clinicopathologic features of an unusual outbreak of cryptococcosis in dogs, cats, ferrets, and a bird: 38 cases (January to July 2003). J. Am. Vet. Med. Assoc. 225:1716-1722. http://dx.doi.org/10.2460/javma .2004.225.1716 (Pubitemid 39602462)
12. Meyer W, Aanensen DM, Boekhout T, Cogliati M, Diaz MR, Esposto MC, Fisher M, Gilgado F, Hagen F, Kaocharoen S, Litvintseva AP, Mitchell TG, Simwami SP, Trilles L, Viviani MA, Kwon-Chung J. 2009. Consensus multi-locus sequence typing scheme for Cryptococcus neofor-mans and Cryptococcus gattii. Med. Mycol. 47:561-570. http://dx.doi.org/10.1080/13693780902953886
13. Gillece JD, Schupp JM, Balajee SA, Harris J, Pearson T, Yan Y, Keim P, DeBess E, Marsden-Haug N, Wohrle R, Engelthaler DM, Lockhart SR. 2011. Whole genome sequence analysis of Cryptococcus gattii from the Pacific Northwest reveals unexpected diversity. PLoS One 6:e28550. http://dx.doi.org/10.1371/ journal.pone.0028550
14. Byrnes EJ, III, Li W, Lewit Y, Ma H, Voelz K, Ren P, Carter DA, Chaturvedi V, Bildfell RJ, May RC, Heitman J. 2010. Emergence and pathogenicity of highly virulent Cryptococcus gattii genotypes in the northwest United States. PLoS Pathog. 6:e1000850. http://dx.doi.org/10.1371/journal.ppat.1000850
15. Lockhart SR, Iqbal N, Harris JR, Grossman NT, DeBess E, Wohrle R, Marsden-Haug N, Vugia DJ. 2013. Cryptococcus gattii in the United States: genotypic diversity of human and veterinary isolates. PLoS One 8:e74737. http://dx.doi.org/10.1371/journal.pone.0074737
16. Byrnes EJ, III, Li W, Ren P, Lewit Y, Voelz K, Fraser JA, Dietrich FS, May RC, Chaturvedi S, Chaturvedi V, Heitman J. 2011. A diverse population of Cryptococcus gattii molecular type VGIII in southern Californian HIV/AIDS patients. PLoS Pathog. 7:e1002205. http://dx.doi.org/10.1371/journal.ppat. 1002205
17. Campbell LT, Currie BJ, Krockenberger M, Malik R, Meyer W, Heitman J, Carter D. 2005. Clonality and recombination in genetically differentiated subgroups of Cryptococcus gattii. Eukaryot. Cell 4:1403-1409. http://dx.doi.org/10.1128/EC.4.8.1403-1409.2005 (Pubitemid 41176694)
18. Litvintseva AP, Thakur R, Reller LB, Mitchell TG. 2005. Prevalence of clinical isolates of Cryptococcus gattii serotype C among patients with AIDS in sub-Saharan Africa. J. Infect. Dis. 192:888-892. http://dx.doi.org/10.1086/ 432486 (Pubitemid 41193087)
19. Lockhart SR, Iqbal N, Bolden CB, DeBess EE, Marsden-Haug N, Worhle R, Thakur R, Harris JR. 2012. Epidemiologic cutoff values for triazole drugs in Cryptococcus gattii: correlation of molecular type and in vitro susceptibility. Diagn. Microbiol. Infect. Dis. 73:144-148. http://dx.doi.org/10.1016/j. diagmicrobio.2012.02.018
20. Iqbal N, DeBess EE, Wohrle R, Sun B, Nett RJ, Ahlquist AM, Chiller T, Lockhart SR. 2010. Correlation of genotype and in vitro susceptibilities of Cryptococcus gattii strains from the Pacific Northwest of the United States. J. Clin. Microbiol. 48:539-544. http://dx.doi.org/10.1128/JCM.01505-09
21. Chong HS, Dagg R, Malik R, Chen S, Carter D. 2010. In vitro susceptibility of the yeast pathogen cryptococcus to fluconazole and other azoles varies with molecular genotype. J. Clin. Microbiol. 48:4115-4120. http://dx.doi.org/10.1128/JCM.01271-10
22. Trilles L, Meyer W, Wanke B, Guarro J, Lazéra M. 2012. Correlation of antifungal susceptibility and molecular type within the Cryptococcus neoformans/ C. gattii species complex. Med. Mycol. 50:328-332. http://dx.doi.org/10.3109/13693786.2011.602126
23. Hagen F, Illnait-Zaragozi MT, Bartlett KH, Swinne D, Geertsen E, Klaassen CH, Boekhout T, Meis JF. 2010. In vitro antifungal susceptibilities and amplified fragment length polymorphism genotyping of a worldwide collection of 350 clinical, veterinary, and environmental Cryptococcus gattii isolates. Antimicrob. Agents Chemother. 54:5139-5145. http://dx.doi.org/10.1128/AAC.00746- 10
24. Chowdhary A, Randhawa HS, Sundar G, Kathuria S, Prakash A, Khan Z, Sun S, Xu J. 2011. In vitro antifungal susceptibility profiles and genotypes of 308 clinical and environmental isolates of Cryptococcus neoformans var. grubii and Cryptococcus gattii serotype B from north-western India. J. Med. Microbiol. 60:961-967. http://dx.doi.org/10.1099/jmm.0.029025-0
25. Duncan C, Schwantje H, Stephen C, Campbell J, Bartlett K. 2006. Cryptococcus gattii in wildlife of Vancouver Island, British Columbia, Canada. J. Wildl. Dis. 42:175-178. http://dx.doi.org/10.7589/0090-3558-42.1.175 (Pubitemid 43827161)
26. Cantón E, Pemán J, Iñiguez C, Hervás D, Lopez-Hontangas JL, Pina-Vaz C, Camarena JJ, Campos-Herrero I, García-García I, García-Tapia AM, Guna R, Merino P, Pérez del Molino L, Rubio C, Suárez A, FUNGEMYCA Study Group. 2013. Epidemiological cutoff values for fluconazole, itraconazole, posaconazole, and voriconazole for six Candida species as determined by the colorimetric Sensititre YeastOne method. J. Clin. Microbiol. 51:2691-2695. http://dx.doi.org/10.1128/JCM.01230-13
27. Kwon-Chung KJ, Polacheck I, Bennett JE. 1982. Improved diagnostic medium for separation of Cryptococcus neoformans var. neoformans (serotypes A and D) and Cryptococcus neoformans var. gattii (serotypes B and C). J. Clin. Microbiol. 15:535-537 (Pubitemid 12178899)
28. Meyer W, Castaneda A, Jackson S, Huynh M, Castañeda E. 2003. Molecular typing of IberoAmerican Cryptococcus neoformans isolates. Emerg. Infect. Dis. 9:189-195. http://dx.doi.org/10.3201/eid0902.020246 (Pubitemid 36231789)
29. Halliday CL, Bui T, Krockenberger M, Malik R, Ellis DH, Carter DA. 1999. Presence of alpha and a mating types in environmental and clinical collections of Cryptococcus neoformans var. gattii strains from Australia. J. Clin. Microbiol. 37:2920-2926 (Pubitemid 29391911)
30. MacDougall L, Kidd SE, Galanis E, Mak S, Leslie MJ, Cieslak PR, Kronstad JW, Morshed MG, Bartlett KH. 2007. Spread of Cryptococcus gattii in British Columbia, Canada, and detection in the Pacific Northwest, U. S. A. Emerg. Infect. Dis. 13:42-50. http://dx.doi.org/10.3201/eid1301.060827 (Pubitemid 46057836)
31. Meyer W, Mitchell TG. 1995. Polymerase chain reaction fingerprinting in fungi using single primers specific to minisatellites and simple repetitive DNA sequences: strain variation in Cryptococcus neoformans. Electrophoresis 16:1648-1656. http://dx.doi.org/10.1002/elps.11501601273
32. Pfeiffer T, Ellis D. 1991. Environmental isolation of Cryptococcus neoformans gattii from California. J. Infect. Dis. 163:929-930. http://dx.doi.org/10.1093/infdis/163.4.929
33. Carriconde F, Gilgado F, Arthur I, Ellis D, Malik R, van de Wiele N, Robert V, Currie BJ, Meyer W. 2011. Clonality and alpha-a recombination in the Australian Cryptococcus gattii VGII population-an emerging outbreak in Australia. PLoS One 6:e16936. http://dx.doi.org/10.1371/journal.pone.0016936
34. Kidd SE, Hagen F, Tscharke RL, Huynh M, Bartlett KH, Fyfe M, Macdougall L, Boekhout T, Kwon-Chung KJ, Meyer W. 2004. A rare genotype of Cryptococcus gattii caused the cryptococcosis outbreak on Vancouver Island (British Columbia, Canada). Proc. Natl. Acad. Sci. U. S. A. 101:17258-17263. http://dx.doi.org/10. 1073/pnas.0402981101 (Pubitemid 39627807)
35. Meyer W, Mitchell TG, Freedman EZ, Vilgalys R. 1993. Hybridization probes for conventional DNA fingerprinting used as single primers in the polymerase chain reaction to distinguish strains of Cryptococcus neoformans. J. Clin. Microbiol. 31:2274-2280 (Pubitemid 23254186)
36. Kwon-Chung KJ, Bennett JE, Theodore TS. 1978. Cryptococcus bacillisporus sp. nov.: serotype B-C of Cryptococcus neoformans. Int. J. Syst. Bacteriol. 28:616-620. http://dx.doi.org/10.1099/00207713-28-4-616 (Pubitemid 9054796)
37. Litvintseva AP, Thakur R, Vilgalys R, Mitchell TG. 2006. Multilocus sequence typing reveals three genetic subpopulations of Cryptococcus neoformans var. grubii (serotype A), including a unique population in Botswana. Genetics 172:2223-2238. http://dx.doi.org/10.1534/genetics.105.046672
38. Vaden SL, Heit MC, Hawkins EC, Manaugh C, Riviere JE. 1997. Fluconazole in cats: pharmacokinetics following intravenous and oral administration and penetration into cerebrospinal fluid, aqueous humour and pulmonary epithelial lining fluid. J. Vet. Pharmacol. Ther. 20:181-186. http://dx.doi.org/10.1111/j. 1365-2885.1997.tb00093.x. (Pubitemid 27244740)
39. Humphrey MJ, Jevons S, Tarbit MH. 1985. Pharmacokinetic evaluation of UK-49,858, a metabolically stable triazole antifungal drug, in animals and humans. Antimicrob. Agents Chemother. 28:648-653. http://dx.doi.org/10.1128/AAC. 28.5.648 (Pubitemid 16215530)
40. Cogliati M, Zamfirova RR, Tortorano AM, Viviani MA, Fimua Cryptococcosis Network. 2013. Molecular epidemiology of Italian clinical Cryptococcus neoformans var. grubii isolates. Med. Mycol. 51:499-506. http://dx.doi.org/10. 3109/13693786.2012.751642
41. Khayhan K, Hagen F, Pan W, Simwami S, Fisher MC, Wahyuningsih R, Chakrabarti A, Chowdhary A, Ikeda R, Taj-Aldeen SJ, Khan Z, Ip M, Imran D, Sjam R, Sriburee P, Liao W, Chaicumpar K, Vuddhakul V, Meyer W, Trilles L, van Iersel LJ, Meis JF, Klaassen CH, Boekhout T. 2013. Geographically structured populations of Cryptococcus neoformans variety grubii in Asia correlate with HIV status and show a clonal population structure. PLoS One 8:e72222. http://dx.doi.org/10.1371/journal.pone.0072222
42. Choi YH, Ngamskulrungroj P, Varma A, Sionov E, Hwang SM, Carriconde F, Meyer W, Litvintseva AP, Lee WG, Shin JH, Kim EC, Lee KW, Choi TY, Lee YS, Kwon-Chung KJ. 2010. Prevalence of the VNIc genotype of Cryptococcus neoformans in non-HIV-associated cryptococcosis in the Republic of Korea. FEMS Yeast Res. 10:769-778. http://dx.doi.org/10.1111/j.1567-1364.2010.00648.x.
43. Wiesner DL, Moskalenko O, Corcoran JM, McDonald T, Rolfes MA, Meya DB, Kajumbula H, Kambugu A, Bohjanen PR, Knight JF, Boulware DR, Nielsen K. 2012. Cryptococcal genotype influences immunologic response and human clinical outcome after meningitis. mBio 3:e00196-12. hp://dx.doi.org/10.1128/mBio.00196-12.
44. Mihara T, Izumikawa K, Kakeya H, Ngamskulrungroj P, Umeyama T, Takazono T, Tashiro M, Nakamura S, Imamura Y, Miyazaki T, Ohno H, Yamamoto Y, Yanagihara K, Miyzaki Y, Kohno S. 2013. Multilocus sequence typing of Cryptococcus neoformans in non-HIV associated cryptococcosis in Nagasaki, Japan. Med. Mycol. 51:252-260. http://dx.doi.org/10.3109/13693786.2012.708883.
45. Simwami SP, Khayhan K, Henk DA, Aanensen DM, Boekhout T, Hagen F, Brouwer AE, Harrison TS, Donnelly CA, Fisher MC. 2011. Low diversity Cryptococcus neoformans variety grubii multilocus sequence types from Thailand are consistent with an ancestral African origin. PLoS Pathog. 7:e1001343. http://dx.doi.org/ 10.1371/journal.ppat.1001343.
46. Bertout S, Dunyach C, Drakulovski P, Reynes J, Mallié M. 2011. Comparison of the SensititreYeastOnedilutionmethodwith the ClinicalandLaboratory Standards Institute (CLSI) M27-A3 microbroth dilution reference method for determining MIC of eight antifungal agents on 102 yeast strains. Pathol. Biol. (Paris) 59:48-51. http://dx.doi.org/10.1016/j.patbio.2010.07.020
47. Espinel-Ingroff A, Aller AI, Canton E, Castañón-Olivares LR, Chowdhary A, Cordoba S, Cuenca-Estrella M, Fothergill A, Fuller J, Govender N, Hagen F, Illnait-Zaragozi MT, Johnson E, Kidd S, Lass-Flörl C, Lockhart SR, Martins MA, Meis JF, Melhem MS, Ostrosky-Zeichner L, Pelaez T, Pfaller MA, Schell WA, St-Germain G, Trilles L, Turnidge J. 2012. Cryptococcus neoformans-Cryptococcus gattii species complex: an international study of wild-type susceptibility endpoint distributions and epidemiological cutoff values for fluconazole, itraconazole, posaconazole, and voriconazole. Antimicrob. Agents Chemother. 56:5898-5906. http://dx.doi.org/10.1128/AAC.01115- 12
48. Varma A, Kwon-Chung KJ. 2010. Heteroresistance of Cryptococcus gattii to fluconazole. Antimicrob. Agents Chemother. 54:2303-2311. http://dx.doi.org/10. 1128/AAC.00153-10.
49. Malik R, Medeiros C, Wigney DI, Love DN. 1996. Suspected drug eruption in seven dogs during administration of flucytosine. Aust. Vet. J. 74:285-288. http://dx.doi.org/10.1111/j.1751-0813.1996.tb13776.x. (Pubitemid 126646749)