Distribution of Candida species in oral candidiasis patients: Association between sites of isolation, ability to form biofilm, and susceptibility to antifungal drugs
Main Article Content
Abstract
Background: The oral cavity is a complex structure. Differences in oral mucosa surfaces are keratinized epithelium (KE) lined on the gingival, palate, and tongue surface, while non-keratinized epithelium (NKE) lined on the buccal surface and lips. In denture wearer, denture surface is also exposed in the oral cavity. Clinical manifestations of oral candidiasis vary depending on the type of infection. The ability to form biofilm which is the virulent factor of Candida spp. may affects by these mucosa and abiotic surfaces and leading to drug resistant strains.
Objectives: To compare the distribution of Candida spp. by site of infection, its ability to form biofilm, and susceptibility to antifungal agents.
Materials and methods: The samples were collected from lesions in the oral cavity by using the imprint culture technique, and yeast species were identified by conventional and PCR methods. Biofilm formation was measured by crystal violet (CV) assay. Susceptibility to amphotericin B and azoles was performed in according to CLSI guideline (M27 A3).
Results: One hundred and fifty-two isolates were identified from 99 patients. A majority of isolates were 50% isolated from KE surface (gingiva, palate, and tongue), followed by 34.9% from NKE surface (buccal mucosa and lip), and 15.1% from surface of denture. Candida albicans was the most common species (80.9%) frequently isolated from the tongue and buccal surface, followed by C. tropicalis (7.2%) frequently isolated from the tongue and palate, and C. glabrata (5.3%) was frequently isolated from dentures. In consideration to site of infections, yeast isolated from denture surface showed a significant lower biofilm production compared to the NKE surface (p=0.029). The percentage of drug resistant strains in Candida spp. isolated from denture was 17.4%, NKE surface 14.6% and KE surface 8.1%.
Conclusion: This data indicate that site of infection; KE and NKE surfaces in the oral cavity had not affected to biofilm formation of Candida spp., except in denture wearer. Drug resistant in clinical isolates involved in high biofilm former strains and the species C. glabrata.
Article Details
This work is licensed under a Creative Commons Attribution-NonCommercial-NoDerivatives 4.0 International License.
Personal views expressed by the contributors in their articles are not necessarily those of the Journal of Associated Medical Sciences, Faculty of Associated Medical Sciences, Chiang Mai University.
References
[2] Gabler IG, Barbosa AC, Velela RR, Lyon S, Rosa CA. Incidence and anatomic localization of oral candidiasis in patients with AIDS hospitalized in a public hospital in Belo Horizonte, MG, Brazil. J Appl Oral Sci. 2008; 16(4): 247-50.
[3] Wu N, Lin J, Wu L, Zhao J. Distribution of Candida albicans in the oral cavity of children aged 3-5 years of Uygur and Han nationality and their genotype in caries-active groups. Genet Mol Res. 2015; 14(1): 748-57.
[4] da Silva-Rocha WP, Lemos VL, Svidizisnki TI, Milan EP, Chaves GM. Candida species distribution, genotyping and virulence factors of Candida albicans isolated from the oral cavity of kidney transplant recipients of two geographic regions of Brazil. BMC Oral Health. 2014; 14: 20.
[5] Zahir RA, Himratul-Aznita WH. Distribution of Candida in the oral cavity and its differentiation based on the internally transcribed spacer (ITS) regions of rDNA. Yeast. 2013; 30(1): 13-23.
[6] Bassetti M, Righi E, Costa A, Fasce R, Molinari MP, Rosso R, et al. Epidemiological trends in nosocomial candidemia in intensive care. BMC Infect Dis. 2006; 6: 21.
[7] Muadcheingka T, Tantivitayakul P. Distribution of Candida albicans and non-albicans Candida species in oral candidiasis patients: Correlation between cell surface hydrophobicity and biofilm forming activities. Arch Oral Biol. 2015; 60(6): 894-901.
[8] Ramage G, Williams C. The clinical importance of fungal biofilms. Adv Appl Microbiol. 2013; 84: 27-83.
[9] Squier CA, Kremer MJ. Biology of oral mucosa and esophagus. J Natl Cancer Inst Monogr. 2001; 29: 7-15.
[10] Singh A, Verma R, Murari A, Agrawal A. Oral candidiasis: An overview. J Oral Maxillofac Pathol. 2014; 18(Suppl 1): S81-5.
[11] Ramage G, Tomsett K, Wickes BL, Lopez-Ribot JL, Redding SW. Denture stomatitis: a role for Candida biofilms. Oral Surg Oral Med Oral Pathol Oral Radiol Endod. 2004; 98(1): 53-9.
[12] Zarkzewski A, Rouabhia M. Engineered keratinized oral mucosa decreased Candida albicans transition through the production of keratins10, 14, 16, and 19 by oral epithelial cells. The Open Mycol J. 2007; 1: 1-8.
[13] Dongari-Bagtzoglou A, Kashleva H, Dwivedi P, Diaz P, Vasilakos J. Characterization of mucosal Candida albicans biofilms. PLoS One. 2009; 4(11): e7967.
[14] Al-Maskari AY, Al-Maskari MY, Al-Sudairy S. Oral manifestations and complications of diabetes mellitus: A review. Sultan Qaboos Univ Med J. 2011; 11(2): 179-86.
[15] Pongsiriwet S, Chaimano S, Kittikomton R. A comparative study of exfolative cytology and culture in diagnosis of Candidiasis in denture stomatitis patients. CM Dent J. 2001; 22(1): 67-72.
[16] Preechasuth K, Kabchan P, Khumwan C. Use of an Oxidation-Fermentation medium for identification of clinical yeast isolates. J Med Tech Assoc Thailand. 2007;35(3):2105-14.
[17] Carvalho A, Costa-De-Oliveira S, Martins ML, Pina-Vaz C, Rodrigues AG, Ludovico P, et al. Multiplex PCR identification of eight clinically relevant Candida species. Med Mycol. 2007; 45(7): 619-27.
[18] daSilvaI GA, BernardiI TL, SchakerI PDC, Valente MMP. Rapid yeast DNA extraction by boiling and freeze-thawing without using chemical reagents and DNA purification. Braz arch biol technol. 2012; 55(2): 319-27.
[19] Marcos-Zambrano LJ, Escribano P, Bouza E, Guinea J. Production of biofilm by Candida and non-Candida spp. isolates causing fungemia: comparison of biomass production and metabolic activity and development of cut-off points. Int J Med Microbiol. 2014; 304(8): 1192-8.
[20] Pfaller MA, Espinel-Ingroff A, Canton E, Castanheira M, Cuenca-Estrella M, Diekema DJ, et al. Wild-type MIC distributions and epidemiological cutoff values for amphotericin B, flucytosine, and itraconazole and Candida spp. as determined by CLSI broth microdilution. J Clin Microbiol. 2012; 50(6): 2040-6.
[21] Pelletier R, Peter J, Antin C, Gonzalez C, Wood L, Walsh TJ. Emergence of resistance of Candida albicans to clotrimazole in human immunodeficiency virus-infected children: in vitro and clinical correlations. J Clin Microbiol. 2000; 38(4): 1563-8.
[22] Marichal P, Vanden Bossche H, Odds FC, Nobels G, Warnock DW, Timmerman V, et al. Molecular biological characterization of an azole-resistant Candida glabrata isolate. Antimicrob Agents Chemother. 1997; 41(10): 2229-37.
[23] Katiyar SK, Edlind TD. Identification and expression of multidrug resistance-related ABC transporter genes in Candida krusei. Med Mycol. 2001; 39(1) :109-16.
[24] Santiwongkarn P, Kachonboon S, Thanyasrisung P, Matangkasombut O. Prevalence of oral Candida carriage in Thai adolescents. J Investig Clin Dent. 2012; 3(1): 51-5.
[25] Luo G, Samaranayake LP. Candida glabrata, an emerging fungal pathogen, exhibits superior relative cell surface hydrophobicity and adhesion to denture acrylic surfaces compared with Candida albicans. APMIS. 2002; 110(9): 601-10.
[26] Kilic K, Koc AN, Tekinsen FF, Yildiz P, Kilic D, Zararsiz G, et al. Assessment of Candida species colonization and denture-related stomatitis in bar- and locator-retained overdentures. J Oral Implantol. 2014; 40(5): 549-56.
[27] Coco BJ, Bagg J, Cross LJ, Jose A, Cross J, Ramage G. Mixed Candida albicans and Candida glabrata populations associated with the pathogenesis of denture stomatitis. Oral Microbiol Immunol. 2008; 23(5): 377-83.
[28] Silva S, Henriques M, Hayes A, Oliveira R, Azeredo J, Williams DW. Candida glabrata and Candida albicans co-infection of an in vitro oral epithelium. J Oral Pathol Med. 2011; 40(5): 421-7.
[29] Sardi JC, Duque C, Hofling JF, Goncalves RB. Genetic and phenotypic evaluation of Candida albicans strains isolated from subgingival biofilm of diabetic patients with chronic periodontitis. Med Mycol. 2012; 50(5): 467-75.
[30] Rouabhia M, Deslauriers N. Production and characterization of an in vitro engineered human oral mucosa. Biochem Cell Biol. 2002; 80(2): 189-95.
[31] Dodd CL, Greenspan D, Katz MH, Westenhouse JL, Feigal DW, Greenspan JS. Oral candidiasis in HIV infection: pseudomembranous and erythematous candidiasis show similar rates of progression to AIDS. AIDS. 1991; 5(11): 1339-43.
[32] Vale-Silva LA, Sanglard D. Tipping the balance both ways: drug resistance and virulence in Candida glabrata. FEMS Yeast Res. 2015; 15(4): fov025.
[33] Ben-Ami R, Hilerowicz Y, Novikov A, Giladi M. The impact of new epidemiological cutoff values on Candida glabrata resistance rates and concordance between testing methods. Diagn Microbiol Infect Dis. 2014; 79(2): 209-13.