Lack of detection of Candida nivariensis and Candida bracarensis among 440 clinical Candida glabrata sensu lato isolates in Kuwait


Autoři: Mohammad Asadzadeh aff001;  Ahlam F. Alanazi aff001;  Suhail Ahmad aff001;  Noura Al-Sweih aff001;  Ziauddin Khan aff001
Působiště autorů: Department of Microbiology, Faculty of Medicine, Kuwait University, Jabriya, Kuwait aff001
Vyšlo v časopise: PLoS ONE 14(10)
Kategorie: Research Article
doi: 10.1371/journal.pone.0223920

Souhrn

Occurrence of Candida nivariensis and Candida bracarensis, two species phenotypically similar to Candida glabrata sensu stricto, in human clinical samples from different geographical settings remains unknown. This study developed a low-cost multiplex PCR (mPCR) and three species-specific singleplex PCR assays. Reference strains of common Candida species were used during development and the performance of mPCR and singleplex PCR assays was evaluated with 440 clinical C. glabrata sensu lato isolates. The internal transcribed spacer (ITS) region of rDNA was also sequenced from 85 selected isolates and rDNA sequence variations were used for determining genetic relatedness among the isolates by using MEGA X software. Species-specific amplicons for C. glabrata (~360 bp), C. nivariensis (~250 bp) and C. bracarensis (~180 bp) were obtained in mPCR while no amplicon was obtained from other Candida species. The three singleplex PCR assays also yielded expected results with reference strains of Candida species. The mPCR amplified ~360 bp amplicon from all 440 C. glabrata sensu lato isolates thus identifying all clinical isolates in Kuwait as C. glabrata sensu stricto. The results of mPCR were confirmed for all 440 isolates as they yielded an amplicon only in C. glabrata sensu stricto-specific singleplex PCR assay. The rDNA sequence data identified 28 ITS haplotypes among 85 isolates with 18 isolates belonging to unique haplotypes and 67 isolates belonging to 10 cluster haplotypes. In conclusion, we have developed a simple, low-cost mPCR assay for rapid differentiation of C. glabrata sensu stricto from C. nivariensis and C. bracarensis. Our data obtained from a large collection of clinical C. glabrata sensu lato isolates show that C. nivariensis and C. bracarensis are rare pathogens in Kuwait. Considerable genetic diversity among C. glabrata sensu stricto isolates was also indicated by rDNA sequence analyses.

Klíčová slova:

Candida – Candida albicans – DNA isolation – DNA sequencing – Haplotypes – Multiple alignment calculation – Polymerase chain reaction – Kuwait


Zdroje

1. Pfaller MA, Diekema DJ. Epidemiology of invasive candidiasis: a persistent public health problem. Clin Microbiol Rev 2007; 20:133–163. doi: 10.1128/CMR.00029-06 17223626

2. Diekema D, Arbefeville S, Boyken L, Kroeger J, Pfaller M. The changing epidemiology of healthcare-associated candidemia over three decades. Diagn Microbiol Infect Dis 2012; 73:45–48. doi: 10.1016/j.diagmicrobio.2012.02.001 22578938

3. Guinea J. Global trends in the distribution of Candida species causing candidemia. Clin Microbiol Infect 2014; 20(Supp. 6):5–10.

4. Pfaller MA, Moet GJ, Messer SA, Jones RN, Castanheira M. Candida bloodstream infections: comparison of species distributions and antifungal resistance patterns in community-onset and nosocomial isolates in the SENTRY Antimicrobial Surveillance Program, 2008–2009. Antimicrob Agents Chemother 2011; 55:561–566. doi: 10.1128/AAC.01079-10 21115790

5. Khan Z, Ahmad S, Joseph L and Chandy R. Candida dubliniensis: an appraisal of its clinical significance as a bloodstream pathogen. PLoS One 2012; 7:e32952. doi: 10.1371/journal.pone.0032952 22396802

6. Lockhart SR, Iqbal N, Cleveland AA, Farley MM, Harrison LH, Bolden CB, et al. Species identification and antifungal susceptibility testing of Candida bloodstream isolates from population-based surveillance studies in two U.S. cities from 2008 to 2011. J Clin Microbiol 2012; 50:3435–3442. doi: 10.1128/JCM.01283-12 22875889

7. Cleveland AA, Farley MM, Harrison LH, Stein B, Hollick R, Lockhart SR, et al. Changes in incidence and antifungal drug resistance in candidemia: results from population-based laboratory surveillance in Atlanta and Baltimore, 2008–2011. Clin Infect Dis 2012; 55:1352–1361. doi: 10.1093/cid/cis697 22893576

8. Colombo AL, Guimarães T, Sukienik T, Pasqualotto AC, Andreotti R, Queiroz-Telles F, et al. Prognostic factors and historical trends in the epidemiology of candidemia in critically ill patients: an analysis of five multicenter studies sequentially conducted over a 9-year period. Intensive Care Med 2014; 40:1489–1498. doi: 10.1007/s00134-014-3400-y 25082359

9. Angoulvant A, Guitard J, Hennequin C. Old and new pathogenic Nakaseomyces species: epidemiology, biology, identification, pathogenicity and antifungal resistance. FEMS Yeast Res 2016; 16:fov114. doi: 10.1093/femsyr/fov114 26691882

10. Pfaller MA. Antifungal drug resistance: mechanisms, epidemiology, and consequences for treatment. Am J Med 2012; 125:S3–S13. doi: 10.1016/j.amjmed.2011.11.001 22196207

11. Sanguinetti M, Posteraro B, Lass-Flörl C. Antifungal drug resistance among Candida species: mechanisms and clinical impact. Mycoses 2015; 58 Suppl 2:2–13.

12. Kołaczkowska A, Kołaczkowski M. Drug resistance mechanisms and their regulation in non-albicans Candida species. J Antimicrob Chemother 2016; 71:1438–1450. doi: 10.1093/jac/dkv445 26801081

13. Pappas PG, Kauffman CA, Andes DR, Clancy CJ, Marr KA, Ostrosky-Zeichner L, et al. Clinical Practice Guideline for the Management of Candidiasis: 2016 Update by the Infectious Diseases Society of America. Clin Infect Dis 2016; 62:e1–e50. doi: 10.1093/cid/civ933 26679628

14. Katiyar S, Pfaller M, Edlind T. Candida albicans and Candida glabrata clinical isolates exhibiting reduced echinocandin susceptibility. Antimicrob Agents Chemother 2006; 50:2892–2894. doi: 10.1128/AAC.00349-06 16870797

15. Desnos-Olivier M, Dromer F, Dannaoui E. Detection of capofungin resistance in Candida spp. by Etest. J Clin Microbiol 2008; 46:2389–2392. doi: 10.1128/JCM.00053-08 18448691

16. Dannaoui E, Desnos-Ollivier M, Garcia-Hermoso D, Grenouillet F, Cassaing S, Baixench MT, et al. Candida spp. with acquired echinocandin resistance, France, 2004–2010. Emerg Infect Dis 2012; 8:86–90.

17. Alexander BD, Johnson MD, Pfeiffer CD, Jiménez-Ortigosa C, Catania J, Booker R, et al. Increasing echinocandin resistance in Candida glabrata: clinical failure correlates with presence of FKS mutations and elevated minimum inhibitory concentrations. Clin Infect Dis 2013; 56:1724–1732. doi: 10.1093/cid/cit136 23487382

18. Saraya T, Tanabe K, Araki K, Yonetani S, Makino H, Watanabe T, et al. Breakthrough invasive Candida glabrata in patients on micafungin: a novel FKS gene conversion correlated with sequential elevation of MIC. J Clin Microbiol 2014; 52:2709–2712. doi: 10.1128/JCM.03593-13 24789192

19. Khan Z, Ahmad S, Mokaddas E, Meis JF, Joseph L, Abdullah A, et al. Development of echinocandin resistance in Candida tropicalis following short-term exposure to caspofungin for empiric therapy. Antimicrobial Agents and Chemotherapy 2018; 62:e01926–17. doi: 10.1128/AAC.01926-17 29437623

20. Khan ZU, Ahmad S, Al-Obaid I, Al-Sweih NA, Joseph L, Farhat D. Emergence of resistance to amphotericin B and triazoles in Candida glabrata vaginal isolates in a case of recurrent vaginitis. J Chemother 2008; 20:488–491. doi: 10.1179/joc.2008.20.4.488 18676230

21. Vandeputte P, Tronchin G, Larcher G, Ernoult E, Bergès T, Chabasse D, et al. A nonsense mutation in the ERG6 gene leads to reduced susceptibility to polyenes in a clinical isolate of Candida glabrata. Antimicrob Agents Chemother 2008; 52:3701–3709. doi: 10.1128/AAC.00423-08 18694952

22. Hull CM, Bader O, Parker JE, Weig M, Gross U, Warrilow AG, et al. Two clinical isolates of Candida glabrata exhibiting reduced sensitivity to amphotericin B both harbor mutations in ERG2. Antimicrob Agents and Chemother 2012; 56:6417–6421.

23. Khan Z, Ahmad S, Joseph L, Al-Obaid K. Isolation of cholesterol-dependent, multidrug-resistant Candida glabrata strains from blood cultures of a candidemia patient in Kuwait. BMC Infect Dis 2014;14:188. doi: 10.1186/1471-2334-14-188 24712485

24. Ahmad S, Joseph L, Parker JE, Asadzadeh M, Kelly SL, Meis JF, Khan Z. ERG6 and ERG2 are major targets conferring reduced susceptibility to amphotericin B in clinical Candida glabrata isolates in Kuwait. Antimicrob Agents Chemother 2019; 63:e01900–18. doi: 10.1128/AAC.01900-18 30455247

25. Healey KR, Zhao Y, Perez WB, Lockhart SR, Sobel JD, Farmakiotis D, et al. Prevalent mutator genotype identified in fungal pathogen Candida glabrata promotes multi-drug resistance. Nat Commun 2016; 7:1–10.

26. Healey KR, Perlin DS. Fungal Resistance to Echinocandins and the MDR Phenomenon in Candida glabrata. J fungi 2018; 4:1–14.

27. Alcoba-Flórez J, Méndez-Alvarez S, Cano J, Guarro J, Pérez-Roth E, del Pilar Arévalo M. Phenotypic and molecular characterization of Candida nivariensis sp. nov., a possible new opportunistic fungus. J Clin Microbiol 2005; 43:4107–4111. doi: 10.1128/JCM.43.8.4107-4111.2005 16081957

28. Correia A, Sampaio P, James S, Pais C. Candida bracarensis sp. nov., a novel anamorphic yeast species phenotypically similar to Candida glabrata. Int J Syst Evol Microbiol 2006; 56:313–317. doi: 10.1099/ijs.0.64076-0 16403904

29. Borman AM, Petch R, Linton CJ, Palmer MD, Bridge PD, Johnson EM. Candida nivariensis, an emerging pathogenic fungus with multidrug resistance to antifungal agents. J Clin Microbiol 2008; 46:933–938. doi: 10.1128/JCM.02116-07 18199788

30. Lockhart SR, Messer SA, Gherna M, Bishop JA, Merz WG, Pfaller MA, et al. Identification of Candida nivariensis and Candida bracarensis in a large global collection of Candida glabrata isolates: comparison to the literature. J Clin Microbiol 2009; 47:1216–1217. doi: 10.1128/JCM.02315-08 19193845

31. Jamal WY, Ahmad S, Khan ZU, Rotimi VO. Comparative evaluation of two matrix-assisted laser desorption/ionization time-of-flight mass spectrometry (MALDI-TOF MS) systems for the identification of clinically significant yeasts. Int J Infect Dis 2014; 26:167–170. doi: 10.1016/j.ijid.2014.05.031 25080355

32. Asadzadeh M, Ahmad S, Hagen F, Meis JF, Al-Sweih N, Khan Z. Simple, low-cost detection of Candida parapsilosis complex isolates and molecular fingerprinting of Candida orthopsilosis strains in Kuwait by ITS region sequencing and amplified fragment length polymorphism analysis. PLoS One 2015; 10:e0142880. doi: 10.1371/journal.pone.0142880 26580965

33. Ahmad S, Mustafa AS, Khan Z, Al-Rifaiy AI, Khan ZU. PCR-enzyme immunoassay of rDNA in the diagnosis of candidemia and comparison with amplicon detection by agarose gel electrophoresis. Int J Med Microbiol 2004; 294:45–51. doi: 10.1016/j.ijmm.2004.01.002 15293453

34. Khan ZU, Ahmad S, Mokaddas E, Chandy R, Cano J, Guarro J. Actinomucor elegans var. kuwaitiensis isolated from the wound of a diabetic patient. Antonie van Leeuwoenhoek 2008; 94:343–352.

35. Khan ZU, Ahmad S, Hagen F, Fell JW, Kowshik T, Chandy R, et al. Cryptococcus randhawai sp. nov., a novel anamorphic basidiomycetous yeast isolated from tree trunk hollow of Ficus religiosa (peepal tree) from New Delhi, India. Antonie Van Leeuwenhoek 2010; 97:253–259. doi: 10.1007/s10482-009-9406-8 20091225

36. Asadzadeh M, Ahmad S, Al-Sweih N, Khan Z. Population structure and molecular genetic characterization of 5-flucytosine-susceptible and -resistant clinical Candida dubliniensis isolates from Kuwait. PLoS One 2017; 12:e0175269. doi: 10.1371/journal.pone.0175269 28380072

37. Li J, Shan Y, Fan S, Liu X. Prevalence of Candida nivariensis and Candida bracarensis in vulvovaginal candidiasis. Mycopathologia 2014; 178:279–283. doi: 10.1007/s11046-014-9800-2 25118875

38. Bishop JA, Chase N, Lee R, Kurtzman CP, Merz WG. Production of white colonies on CHROMagar Candida medium by members of the Candida glabrata clade and other species with overlapping phenotypic traits. J Clin Microbiol 2008; 46:3498–3500. doi: 10.1128/JCM.00982-08 18685009

39. Luo G & Mitchell TG. Rapid identification of pathogenic fungi directly from cultures by using multiplex PCR. J Clin Microbiol 2002; 40:2860–2865. doi: 10.1128/JCM.40.8.2860-2865.2002 12149343

40. Alcoba-Flórez J, Arévalo Mdel P, González-Paredes FJ, Cano J, Guarro J, Pérez-Roth E, et al. PCR protocol for specific identification of Candida nivariensis, a recently described pathogenic yeast. J Clin Microbiol 2005; 43:6194–6196. doi: 10.1128/JCM.43.12.6194-6196.2005 16333128

41. Romeo O, Scordino F, Pernice I, Lo Passo C, Criseo G. A multiplex PCR protocol for rapid identification of Candida glabrata and its phylogenetically related species Candida nivariensis and Candida bracarensis. J Microbiol Methods 2009; 79:117–120. doi: 10.1016/j.mimet.2009.07.016 19635503

42. Enache-Angoulvant A, Guitard J, Grenouillet F, Martin T, Durrens P, Fairhead C, et al. Rapid discrimination between Candida glabrata, Candida nivariensis, and Candida bracarensis by use of a singleplex PCR. J Clin Microbiol 2011; 49:3375–3379. doi: 10.1128/JCM.00688-11 21752976

43. Arastehfar A, Fang W, Pan W, Liao W, Yan L, Boekhout T. Identification of nine cryptic species of Candida albicans, C. glabrata, and C. parapsilosis complexes using one-step multiplex PCR. BMC Infect Dis. 2018; 18:480. doi: 10.1186/s12879-018-3381-5 30253748

44. Bishop JA, Chase N, Magill SS, Kurtzman CP, Fiandaca MJ, Merz WG. Candida bracarensis detected among isolates of Candida glabrata by peptide nucleic acid fluorescence in situ hybridization: susceptibility data and documentation of presumed infection. J Clin Microbiol 2008; 46:443–446. doi: 10.1128/JCM.01986-07 18077641

45. Huber JA, Morrison HG, Huse SM, Neal PR, Sogin ML, Mark Welch DB. Effect of PCR amplicon size on assessments of clone library microbial diversity and community structure. Environ Microbiol 2009; 11:1292–1302. doi: 10.1111/j.1462-2920.2008.01857.x 19220394

46. Debode F, Marien A, Janssen E, Bragard C, Berben G. The influence of amplicon length on real-time PCR results. Biotechnol Agron Soc Environ 2017; 21:3–11.

47. Lehmann LE, Hunfeld KP, Emrich T, Haberhausen G, Wissing H, Hoeft A, et al. A multiplex real-time PCR assay for rapid detection and differentiation of 25 bacterial and fungal pathogens from whole blood samples. Med Microbiol Immunol 2008; 197:313–324. doi: 10.1007/s00430-007-0063-0 18008085

48. Lucignano B, Ranno S, Liesenfeld O, Pizzorno B, Putignani L, Bernaschi P, et al. Multiplex PCR allows rapid and accurate diagnosis of bloodstream infections in newborns and children with suspected sepsis. J Clin Microbiol 2011; 49:2252–2258. doi: 10.1128/JCM.02460-10 21471340

49. Grif K, Fille M, Würzner R, Weiss G, Lorenz I, Gruber G, et al. Rapid detection of bloodstream pathogens by real-time PCR in patients with sepsis. Wien Klin Wochenschr 2012; 124:266–270. doi: 10.1007/s00508-012-0159-4 22527822

50. Galán F, García-Agudo L, Guerrero I, Marín P, García-Tapia A, García-Martos P, et al. Evaluation of mass spectrometry for the identification of clinically interesting yeasts. Enferm Infecc Microbiol Clin 2015; 33:372–378. doi: 10.1016/j.eimc.2014.10.003 25444360

51. Hou X, Xiao M, Chen SC, Wang H, Yu SY, Fan X, et al. Identification and Antifungal Susceptibility Profiles of Candida nivariensis and Candida bracarensis in a Multi-Center Chinese Collection of Yeasts. Front Microbiol 2017; 8:5. doi: 10.3389/fmicb.2017.00005 28154553

52. Dodgson AR, Pujol C, Denning DW, Soll DR, Fox AJ. Multilocus sequence typing of Candida glabrata reveals geographically enriched clades. J Clin Microbiol 2003; 41:5709–5717. doi: 10.1128/JCM.41.12.5709-5717.2003 14662965

53. Asadzadeh M, Ahmad S, Al-Sweih N, Khan ZU. Rapid molecular differentiation and genotypic heterogeneity among Candida parapsilosis and Candida orthopsilosis strains isolated from clinical specimens in Kuwait. J Med Microbiol 2009; 58:745–752. doi: 10.1099/jmm.0.008235-0 19429750

54. Gee SF, Joly S, Soll DR, Meis JF, Verweij PE, Polacheck I, et al. Identification of four distinct genotypes of Candida dubliniensis and detection of microevolution in vitro and in vivo. J Clin Microbiol 2002; 40:556–574. doi: 10.1128/JCM.40.2.556-574.2002 11825972

55. Ahmad S, Khan ZU, Joseph L, Asadzadeh M, Theyyathel A. Genotypic heterogeneity and molecular basis of 5-flucytosine resistance among Candida dubliniensis isolates recovered from clinical specimens in Kuwait. Med Mycol 2012; 50:244–251. doi: 10.3109/13693786.2011.597446 21895416

56. Borman AM, Szekely A, Linton CJ, Palmer MD, Brown P, Johnson EM. Epidemiology, antifungal susceptibility, and pathogenicity of Candida africana isolates from the United Kingdom. J Clin Microbiol 2013; 51:967–972. doi: 10.1128/JCM.02816-12 23303503

57. Khan Z, Ahmad S, Al-Sweih N, Khan S, Joseph L. Candida lusitaniae in Kuwait: prevalence, antifungal susceptibility and role in neonatal fungemia. PLoS One 2019; 14: e0213532. doi: 10.1371/journal.pone.0213532 30845213

58. Fujita S, Senda Y, Okusi T, Ota Y, Takada H, Yamada K, Kawano M. Catheter-related fungemia due to fluconazole-resistant Candida nivariensis. J Clin Microbiol 2007; 45:3459–3461. doi: 10.1128/JCM.00727-07 17652473

59. Wahyuningsih R, SahBandar IN, Theelen B, Hagen F, Poot G, Meis JF, et al. Candida nivariensis isolated from an Indonesian human immunodeficiency virus-infected patient suffering from oropharyngeal candidiasis. J Clin Microbiol 2008; 46:388–391. doi: 10.1128/JCM.01660-07 18003796

60. Warren TA, McTaggart L, Richardson SE, Zhang SX. Candida bracarensis bloodstream infection in an immunocompromised patient. J Clin Microbiol 2010; 48:4677–4679. doi: 10.1128/JCM.01447-10 20881164

61. López-Soria LM, Bereciartua E, Santamaría M, Soria LM, Hernández-Almaraz JL, Mularoni A, et al. First case report of catheter-related fungemia by Candida nivariensis in the Iberian Peninsula. Rev Iberoam Micol 2013; 30:69–71. doi: 10.1016/j.riam.2012.09.001 22982698

62. Gorton RL, Jones GL, Kibbler CC, Collier S. Candida nivariensis isolated from a renal transplant patient with persistent candiduria-Molecular identification using ITS PCR and MALDI-TOF. Med Mycol Case Rep 2013; 2:156–158. doi: 10.1016/j.mmcr.2013.10.001 24432244

63. Aznar-Marin P, Galan-Sanchez F, Marin-Casanova P, García-Martos P, Rodríguez-Iglesias M. Candida nivariensis as a new emergent agent of vulvovaginal candidiasis: description of cases and review of published studies. Mycopathologia 2016; 181:445–449. doi: 10.1007/s11046-015-9978-y 26708316

64. Figueiredo-Carvalho MH, Ramos Lde S, Barbedo LS, Chaves AL, Muramoto IA, Santos AL, et al. First description of Candida nivariensis in Brazil: antifungal susceptibility profile and potential virulence attributes. Mem Inst Oswaldo Cruz 2016; 111:51–58. doi: 10.1590/0074-02760150376 26814644

65. Treviño-Rangel RJ, Espinosa-Pérez JF, Villanueva-Lozano H, Montoya AM, Andrade A, Bonifaz A, et al. First report of Candida bracarensis in Mexico: hydrolytic enzymes and antifungal susceptibility pattern. Folia Microbiol (Praha) 2018; 63:517–523.

66. Chowdhary A, Randhawa HS, Khan ZU, Ahmad S, Juneja S, Sharma B, et al. First isolations in India of Candida nivariensis, a globally emerging opportunistic pathogen. Med Mycol 2010; 48:416–420. doi: 10.1080/13693780903114231 19626545

67. Cuenca-Estrella M, Gomez-Lopez A, Isla G, Rodriguez D, Almirante B, Pahissa A, et al. Prevalence of Candida bracarensis and Candida nivariensis in a Spanish collection of yeasts: comparison of results from a reference centre and from a population-based surveillance study of candidemia. Med Mycol 2011; 49:525–529. doi: 10.3109/13693786.2010.546373 21198347

68. Mirhendi H, Bruun B, Schønheyder HC, Christensen JJ, Fuursted K, Gahrn-Hansen B, et al. Differentiation of Candida glabrata, C. nivariensis and C. bracarensis based on fragment length polymorphism of ITS1 and ITS2 and restriction fragment length polymorphism of ITS and D1/D2 regions in rDNA. Eur J Clin Microbiol Infect Dis 2011; 30:1409–1416. doi: 10.1007/s10096-011-1235-9 21607825

69. Pemán J, Cantón E, Quindós G, Eraso E, Alcoba J, Guinea J, et al. Epidemiology, species distribution and in vitro antifungal susceptibility of fungaemia in a Spanish multicentre prospective survey. J Antimicrob Chemother 2012; 67:1181–1187. doi: 10.1093/jac/dks019 22351683

70. Sharma C, Wankhede S, Muralidhar S, Prakash A, Singh PK, Kathuria S, et al. Candida nivariensis as an etiologic agent of vulvovaginal candidiasis in a tertiary care hospital of New Delhi, India. Diagn Microbiol Infect Dis 2013; 76:46–50. doi: 10.1016/j.diagmicrobio.2013.02.023 23537782

71. Esposto MC, Prigitano A, Romeo O, Criseo G, Trovato L, Tullio V, et al. Looking for Candida nivariensis and C. bracarensis among a large Italian collection of C. glabrata isolates: results of the FIMUA working group. Mycoses 2013; 56:394–396. doi: 10.1111/myc.12026 23170902

72. Swoboda-Kopeć E, Sikora M, Golas M, Piskorska K, Gozdowski D, Netsvyetayeva I. Candida nivariensis in comparison to different phenotypes of Candida glabrata. Mycoses 2014; 57:747–753. doi: 10.1111/myc.12264 25267284

73. Tay ST, Lotfalikhani A, Sabet NS, Ponnampalavanar S, Sulaiman S, Na SL, et al. Occurrence and characterization of Candida nivariensis from a culture collection of Candida glabrata clinical isolates in Malaysia. Mycopathologia 2014; 178:307–314. doi: 10.1007/s11046-014-9778-9 25022264

74. Feng X, Ling B, Yang X, Liao W, Pan W, Yao Z. Molecular Identification of Candida Species Isolated from Onychomycosis in Shanghai, China. Mycopathologia 2015; 180:365–371. doi: 10.1007/s11046-015-9927-9 26227864

75. Morales-López SE, Taverna CG, Bosco-Borgeat ME, Maldonado I, Vivot W, Szusz W, et al. Candida glabrata species complex prevalence and antifungal susceptibility testing in a culture collection: First description of Candida nivariensis in Argentina. Mycopathologia 2016; 181:871–878. doi: 10.1007/s11046-016-0052-1 27681573

76. Morales-López S, Dudiuk C, Vivot W, Szusz W, Córdoba SB, Garcia-Effron G. Phenotypic and Molecular Evaluation of Echinocandin Susceptibility of Candida glabrata, Candida bracarensis, and Candida nivariensis Strains Isolated during 30 Years in Argentina. Antimicrob Agents Chemother 2017; 61:e00170–17. doi: 10.1128/AAC.00170-17 28461313

77. Miranda-Cadena K, Marcos-Arias C, Mateo E, Aguirre JM, Quindós G, Eraso E. Prevalence and antifungal susceptibility profiles of Candida glabrata, Candida parapsilosis and their close-related species in oral candidiasis. Arch Oral Biol 2018; 95:100–107. doi: 10.1016/j.archoralbio.2018.07.017 30096698

78. Malek M, Mrowiec P, Klesiewicz K, Skiba-Kurek I, Szczepański A, Białecka J, et al. Prevalence of human pathogens of the clade Nakaseomyces in a culture collection-the first report on Candida bracarensis in Poland. Folia Microbiol (Praha) 2018 Oct 25.

79. Arastehfar A, Daneshnia F, Salehi MR, Zarrinfar H, Khodavaisy S, Haas PJ, et al. Molecular characterization and antifungal susceptibility testing of Candida nivariensis from blood samples—an Iranian multicentre study and a review of the literature. J Med Microbiol 2019; 68:770–777. doi: 10.1099/jmm.0.000963 30924763


Článek vyšel v časopise

PLOS One


2019 Číslo 10