The incidence of yeast infections has increased significantly over the past few years, constituting a leading cause of morbidity and mortality among hospitalised patients. The rapid identification of candidiasis is important for the clinical management of patients and to facilitate tracing the sources of infections in hospitalized patients. Here, we report a retrospective, single-centre study of Candida spp. distribution and antifungal susceptibility from January 2011 to May 2013 at a hospital in México City, regarding the importance of elucidating the identity of the infection-causing Candida species in order to improve prophylactic measures and treatment. Clinical data were collected from patient medical records and the laboratory database. Isolates were initially identified using standard mycology techniques, and then confirmed by PCR-based system using amplification of intergenic spacers (rDNA ITS) and restriction length polymorphism of PCR products after sequence-specific enzymatic cleavage (PCR-RFLP). We observed no shift from C. albicans to non-albicans Candida species: Candida albicans (73.7%) was the most prevalent species isolated, while C. dubliniensis was not identified in this study. Antifungal susceptibility was determined using FUNGITEST®; 17.4% of C. albicans isolates were resistant to fluconazole and 21.7% to itraconazole. Multiplex PCR microsatellite analysis of the clinical C. albicans isolates using primers for the CAI, CAIII and CAVI loci identified 29 different alleles for CAI, 8 alleles for CAIII and 31 for CAVI. The combined discriminatory power of these three microsatellites was 0.98, which was considered reliable for molecular typing. Genetic analysis of these isolates revealed a clonal population with a total of 62 genotypes from the examined isolates
References
[1]
Chang, A., Neofytos, D. and Horn, D. (2008) Candidemia in the 21st Century. Future Microbiology, 3, 463-472. http://dx.doi.org/10.2217/17460913.3.4.463
[2]
Vincent, J.L., Rello, J., Marshall, J., Silva, E., Anzueto, A., Martin, C.D., Moreno, R., Lipman, J., Gomersall, C., Sakr, Y. and Reinhart, K., E. I. G. O. Investigators (2009) International Study of the Prevalence and Outcomes of Infection In Intensive Care Units. Journal of the American Medical Association, 302, 2323-2329. http://dx.doi.org/10.1001/jama.2009.1754
[3]
Cornely, O.A., Bassetti, M., Calandra, T., Garbino, J., Kullberg, B.J., Lortholary, O., Meersseman, W., Akova, M., Arendrup, M.C., Arikan-Akdagli, S., Bille, J., Castagnola, E., Cuenca-Estrella, M., Donnelly, J.P., Groll, A.H., Herbrecht, R., Hope, W.W., Jensen, H.E., Lass-Florl, C., Petrikkos, G., Richardson, M.D., Roilides, E., Verweij, P.E., Viscoli, C. and Ullmann, A.J., E. F. I. S. Group (2012) ESCMID* Guideline for the Diagnosis and Management of Candida Diseases 2012: Non-Neutropenic Adult Patients. Clinical Microbiology and Infection, 18, 19-37. http://dx.doi.org/10.1111/1469-0691.12039
[4]
Chen, Y.L., Yu, S.J., Huang, H.Y., Chang, Y.L., Lehman, V.N., Silao, F.G., Bigol, U.G., Bungay, A.A., Averette, A. and Heitman, J. (2014) Calcineurin Controls Hyphal Growth, Virulence, and Drug Tolerance of Candida Tropicalis. Eukaryotic Cell, 13, 844-854. http://dx.doi.org/10.1128/EC.00302-13
[5]
Naglik, J.R., Moyes, D.L., Wachtler, B. and Hube, B. (2011) Candida Albicans Interactions with Epithelial Cells and Mucosal Immunity. Microbes and Infection, 13, 963-976. http://dx.doi.org/10.1016/j.micinf.2011.06.009
[6]
Czaika, V., Nenoff, P., Glockner, A., Fegeler, W., Becker, K. and Schmalreck, A.F. (2013) Epidemiology and Changes in Patient-Related Factors from 1997 to 2009 in Clinical Yeast Isolates Related to Dermatology, Gynaecology, and Paediatrics. International Journal of Microbiology, 2013, Article ID: 703905. http://dx.doi.org/10.1155/2013/703905
[7]
Mousavi, S.A.A., Khalesi, E., Bonjar, G.H.S., Aghighi, S., Sharifi, F. and Aram, F. (2007) Rapid Molecular Diagnosis For-Candida Species Using PCR-RFLP. Biotechnology, 6, 583-587. http://dx.doi.org/10.3923/biotech.2007.583.587
[8]
Abdulrahim, M.H., McManus, B.A., Flint, S.R. and Coleman, D.C. (2013) Genotyping Candida albicans from Candida Leukoplakia and Non-Candida Leukoplakia Shows No Enrichment of Multilocus Sequence Typing Clades but Enrichment of ABC Genotype C in Candida Leukoplakia. PLoS ONE, 8, e73738. http://dx.doi.org/10.1371/journal.pone.0073738
[9]
Lyon, J.P., Moraes, K.C., Moreira, L.M., Aimbire, F. and de Resende, M.A. (2010) Candida albicans: Genotyping Methods and Clade Related Phenotypic Characteristics. Brazilian Journal of Microbiology, 41, 841-849.
[10]
Sampaio, P., Gusmao, L., Correia, A., Alves, C., Rodrigues, A.G., Pina-Vaz, C., Amorim, A. and Pais, C. (2005) New Microsatellite Multiplex PCR for Candida albicans Strain Typing Reveals Microevolutionary Changes. Journal of Clinical Microbiology, 43, 3869-3876. http://dx.doi.org/10.1128/JCM.43.8.3869-3876.2005
[11]
Mikulska, M., Del Bono, V., Ratto, S. and Viscoli, C. (2012) Occurrence, Presentation and Treatment of Candidemia. Expert Review of Clinical Immunology, 8, 755-765. http://dx.doi.org/10.1586/eci.12.52
[12]
Chabasse, D. (2001) Intérêt de la numération des levures dans les urines. Revue de la littérature et résultats préliminaires d’une enquête multicentrique réalisée dans 15 centres hospitaliers universitaires. Annales Françaises d’Anesthésie et de Réanimation, 20, 400-406. http://dx.doi.org/10.1016/S0750-7658(01)00376-8
[13]
Mirhendi, H., Makimura, K., Khoramizadeh, M. and Yamaguchi, H. (2006) A One-Enzyme PCR-RFLP Assay for Identification of Six Medically Important Candida Species. Nihon Ishinkin Gakkai Zasshi, 47, 225-229. http://dx.doi.org/10.3314/jjmm.47.225
[14]
Donnelly, S. M., Sullivan, D. J., Shanley, D. B. and Coleman, D.C. (1999) Phylogenetic Analysis and Rapid Identification of Candida dubliniensis Based on Analysis of ACT1 Intron and Exon Sequences. Microbiology, 145, 1871-1882. http://dx.doi.org/10.1099/13500872-145-8-1871
[15]
Witthuhn, F., Toubas, D., Beguinot, I., Aubert, D., Rouger, C., Remy, G. and Pinon, J.M. (1999) Evaluation of the Fungitest Kit by Using Strains from Human Immunodeficiency Virus-Infected Patients: Study of azole Drug Susceptibility. Journal of Clinical Microbiology, 37, 864-866.
[16]
Hunter, P.R. and Gaston, M.A. (1988) Numerical Index of the Discriminatory Ability of Typing Systems: An Application of Simpson’s Index of Diversity. Journal of Clinical Microbiology, 26, 2465-2466.
[17]
Cavalli-Sforza, L.L. and Edwards, A.W. (1967) Phylogenetic Analysis. Models and Estimation Procedures. The American Journal of Human Genetics, 19, 233-257.
[18]
Kumamoto, C.A. and Vinces, M.D. (2005) Contributions of Hyphae and Hypha-co-Regulated Genes to Candida albicans Virulence. Cellular Microbiology, 7, 1546-1554. http://dx.doi.org/10.1111/j.1462-5822.2005.00616.x
[19]
Nucci, M., Queiroz-Telles, F., Tobon, A.M., Restrepo, A. and Colombo, A.L. (2010) Epidemiology of Opportunistic Fungal Infections in Latin America. Clinical Infectious Diseases, 51, 561-570. http://dx.doi.org/10.1086/655683
[20]
Corzo-Leon, D.E., Alvarado-Matute, T., Colombo, A.L., Cornejo-Juarez, P., Cortes, J., Echevarria, J.I., Guzman-Blanco, M., Macias, A.E., Nucci, M., Ostrosky-Zeichner, L., Ponce-de-Leon, A., Queiroz-Telles, F., Santolaya, M.E., Thompson-Moya, L., Tiraboschi, I.N., Zurita, J. and Sifuentes-Osornio, J. (2014) Surveillance of Candida spp Bloodstream Infections: Epidemiological Trends and Risk Factors of Death in Two Mexican Tertiary Care Hospitals. PLoS ONE, 9, e97325. http://dx.doi.org/10.1371/journal.pone.0097325
[21]
Gonzalez, G.M., Elizondo, M. and Ayala, J. (2008) Trends in Species Distribution and Susceptibility of Bloodstream Isolates of Candida Collected in Monterrey, Mexico, to Seven Antifungal Agents: Results of a 3-Year (2004 to 2007) Surveillance Study. Journal of Clinical Microbiology, 46, 2902-2905. http://dx.doi.org/10.1128/JCM.00937-08
[22]
Chen, C.Y., Huang, S.Y., Tsay, W., Yao, M., Tang, J.L., Ko, B.S., Chou, W.C., Tien, H.F. and Hsueh, P.R. (2012) Clinical Characteristics of Candidaemia in Adults with Haematological Malignancy, and Antimicrobial Susceptibilities of the Isolates at a Medical Centre in Taiwan, 2001-2010. International Journal of Antimicrobial Agents, 40, 533-538. http://dx.doi.org/10.1016/j.ijantimicag.2012.07.022
[23]
Yamamoto, A.C.A., de Paula, C.R., Dias, L.B., Tadano, T., Martins, E.R., Amadio, J.V. and Hahn, R.C. (2012) Epidemiological and Clinical Characteristics of Nosocomial Candidiasis in University Hospitals in Cuiaba—Mato Grosso, Brazil. Revista Iberoamericana de Micologíal, 29, 164-168. http://dx.doi.org/10.1016/j.riam.2012.01.001
[24]
Quindos, G. (2014) Epidemiology of Candidaemia and Invasive Candidiasis. A Changing Face. Revista Iberoamericana de Micología, 31, 42-48. http://dx.doi.org/10.1016/j.riam.2013.10.001
[25]
Chai, Y.A., Wang, Y., Khoo, A.L., Chan, F.Y., Chow, C., Kumarasinghe, G., Singh, K. and Tambyah, P.A. (2007) Predominance of Candida tropicalis Bloodstream Infections in a Singapore Teaching Hospital. Medical Mycology, 45, 435-439. http://dx.doi.org/10.1080/13693780701385868
[26]
Yap, H.Y., Kwok, K.M., Gomersall, C.D., Fung, S.C., Lam, T.C., Leung, P.N., Hui, M. and Joynt, G.M. (2009) Epidemiology and Outcome of Candida Bloodstream Infection in an Intensive Care Unit in Hong Kong. Hong Kong Medical Journal, 15, 255-261.
[27]
Farooqi, J.Q., Jabeen, K., Saeed, N., Iqbal, N., Malik, B., Lockhart, S.R., Zafar, A., Brandt, M.E. and Hasan, R. (2013) Invasive Candidiasis in Pakistan: Clinical Characteristics, Species Distribution and Antifungal Susceptibility. Journal of Medical Microbiology, 62, 259-268.
[28]
Costa, A.R., Silva, F., Henriques, M., Azeredo, J., Oliveira, R. and Faustino, A. (2010) Candida Clinical Species Identification: Molecular and Biochemical Methods. Annals of Microbiology, 60, 105-112. http://dx.doi.org/10.1007/s13213-009-0007-6
[29]
Khan, Z., Ahmad, S., Joseph, L. and Chandy, R. (2012) Candida dubliniensis: An Appraisal of Its Clinical Significance as a Bloodstream Pathogen. PLoS ONE, 7, e32952. http://dx.doi.org/10.1371/journal.pone.0032952
[30]
Garcia-Agudo, L., Garcia-Martos, P., Marin-Casanova, P. and Rodriguez-Iglesias, M. (2012) [Susceptibility to Fluconazole of Clinical Interest Yeasts: New Breakpoints]. Revista Española de Quimioterapia, 25, 266-268.
[31]
Pfaller, M.A. and Diekema, D.J. (2012) Progress in Antifungal Susceptibility Testing of Candida spp. by Use of Clinical and Laboratory Standards Institute Broth Microdilution Methods, 2010 to 2012. Journal of Clinical Microbiology, 50, 2846-2856. http://dx.doi.org/10.1128/JCM.00937-12
[32]
Peyron, F., Favel, A., Michel-Nguyen, A., Gilly, M., Regli, P. and Bolmstrom, A. (2001) Improved Detection of Amphotericin B-Resistant Isolates of Candida lusitaniae by Etest. Journal of Clinical Microbiology, 39, 339-342. http://dx.doi.org/10.1128/JCM.39.1.339-342.2001
[33]
Spampinato, C. and Leonardi, D. (2013) Molecular Fingerprints to Identify Candida Species. BioMed Research International, 2013, Article ID: 923742. http://dx.doi.org/10.1155/2013/923742
[34]
Amouri, I., Sellami, H., Abbes, S., Hadrich, I., Mahfoudh, N., Makni, H. and Ayadi, A. (2012) Microsatellite Analysis of Candida Isolates from Recurrent Vulvovaginal Candidiasis. Journal of Medical Microbiology, 61, 1091-1096.
[35]
Rustchenko, E. (2007) Chromosome Insta-bility in Candida albicans. FEMS Yeast Research, 7, 2-11. http://dx.doi.org/10.1111/j.1567-1364.2006.00150.x
[36]
Pfaller, M.A., Messer, S.A., Houston, A., Rangel-Frausto, M.S., Wiblin, T., Blumberg, H.M., Edwards, J.E., Jarvis, W., Martin, M.A., Neu, H.C., Saiman, L., Patterson, J.E., Dibb, J.C., Roldan, C.M., Rinaldi, M.G. and Wenzel, R.P. (1998) National Epidemiology of Mycoses Survey: A Multicenter Study of Strain Variation and Antifungal Susceptibility among Isolates of Candida Species. Diagnostic Microbiology and Infectious Disease, 31, 289-296. http://dx.doi.org/10.1016/S0732-8893(97)00245-9
[37]
Voss, A., Hollis, R.J., Pfaller, M.A., Wenzel, R.P. and Doebbeling, B.N. (1994) Investigation of the Sequence of Colonization and Candidemia in Nonneutropenic Patients. Journal of Clinical Microbiology, 32, 975-980.
