Main Article Content
Candida parapsilosis, although, is a human commensal of epithelial and mucosal tissues. This species is also frequently isolated from environments. C. parapsilosis is notable for the ability to form biofilms on medical devices. Therefore, it is frequently associated with nosocomial outbreaks. In addition, ability of C. parapsilosis producing secrete proteinase and phospholipase can causes more severe infection. The present study aimed to determine biofilm formation using crystal violet staining and hydrolytic enzyme production using spot assay on relevant agar medium of C. parapsilosis isolated from environment. In total, 8 of 30 yeast isolates (26.66 %) obtained from environment were C. parapsilosis. Biofilm formation of the isolated C. parapsilosis was variable. All of the isolates revealed the higher biofilm formation at room temperature (30 °C) compared to 37 °C. All the isolates showed moderate to high activity of proteinase but no activity of phospholipase. In contrast to biofilm formation, proteinase production of the isolates was increased at 37 °C. In conclusion, temperature is one important factor affecting biofilm formation and proteinase production. The formation of the biofilm is possibly beneficial for the isolates to live in the hostile environment. However, production of proteinase may play important role for C. parapsilosis to cause infection in human.
Boonyasiri, A., Jearanaisilavong, J. and Assanasen, S., 2013, Candidemia in Siriraj Hospital: epidemiology and factors associated with mortality, J. Med. Assoc. Thai 96(suppl. 2): S91-97.
Bougnoux, M.E., Brun, S. and Zahar, J.R., 2018, Healthcare-associated fungal outbreaks: New and uncommon species, new molecular tools for investigation and prevention, Antimicrob. Resist. Infect. Control 7: 45.
Brillowska-Dabrowska, A., Schön, T., Pannanusorn, S., Lönnbro, N., Bernhoff, L., Bonnedal, J., Häggström, J., Wistedt, A., Fernandez, V. and Arendrup, M.C., 2009, A nosocomial outbreak of Candida parapsilosis in southern sweden verified by genotyping, Scand. J. Infect. Dis. 41: 135-142.
Bruzual, I., Riggle, P., Hadley, S. and Kumamoto, C.A., 2007, Biofilm formation by fluconazole-resistant Candida albicans strains is inhibited by fluconazole, J. Antimicrob. Chemother. 59: 441-450.
Chow, B.D.W., Linden, J.R. and Bliss, J.M., 2012, Candida parapsilosis and the neonate: Epidemiology, virulence and host defense in a unique patient setting, Expert Rev. Anti-infect. Ther. 10: 935-946.
Cisterna, R., Ezpeleta, G., Telleria, O., Guinea, J., Regueiro, B., Garcia-RodrÃguez, J., Esperalba, J. and Group, T.S.C.S., 2010, Nationwide sentinel surveillance of bloodstream Candida infections in 40 tertiary care hospitals in spain, J. Clin. Microbiol. 48: 4200-4206.
Cordeiro, R.A., Brilhante, R.S., Pantoja, L.D., Moreira Filho, R.E., Vieira, P.R., Rocha, M.F., Monteiro, A.J. and Sidrim, J.J., 2010, Isolation of pathogenic yeasts in the air from hospital environments in the city of Fortaleza, northeast Brazil, Braz. J. Infect. Dis. 14: 30-34.
Costerton, J.W., Lewandowski, Z., Caldwell, D.E., Korber, D.R. and Lappinscott, H.M., 1995, Microbial biofilms, Annu. Rev. Microbiol. 49: 711-745.
d'Enfert, C., 2006, Biofilms and their role in the resistance of pathogenic Candida to antifungal agents, Curr. Drug Targets 7: 465-470.
da Silva Ruiz, L., Montelli, A.C., Sugizaki Mde, F., Da Silva, E.G., de Batista, G.C., Moreira, D. and Paula, C.R., 2013, Outbreak of fungemia caused by Candida parapsilosis in a neonatal intensive care unit: Molecular investigation through microsatellite analysis, Rev. Iberoam. Micol. 30: 112-115.
de Toro, M., Torres, M.J., Maite, R. and Aznar, J., 2011, Characterization of Candida parapsilosis complex isolates, Clin. Microbiol. Infect. 17: 418-424.
Dizbay, M., Kalkanci, A., Sezer, B.E., Aktas, F., Aydogan, S., Fidan, I., Kustimur, S. and Sugita, T., 2008, Molecular investigation of a fungemia outbreak due to Candida parapsilosis in an intensive care unit, Braz. J. Infect. Dis. 12: 395-399.
Döğen, A., Sav, H., Gonca, S., Kaplan, E., Ilkit, M., Novak Babič, M., Gunde-Cimerman, N. and de Hoog, G.S., 2017, Candida parapsilosis in domestic laundry machines, Med. Mycol. 55: 813-819.
Donlan, R.M., 2001, Biofilm formation: A clinically relevant microbiological process, Clin. Infect. Dis. 33: 1387-1392.
Estivill, D., Arias, A., Torres-Lana, A., Carrillo-Muñoz, A.J. and Arévalo, M.P., 2011, Biofilm formation by five species of Candida on three clinical materials, J. Microbiol. Methods 86: 238-242.
Faksri, K., Kaewkes, W., Chaicumpar, K., Chaimanee, P. and Wongwajana, S., 2014, Epidemiology and identification of potential fungal pathogens causing invasive fungal infections in a tertiary care hospital in northeast Thailand, Med. Mycol. 52: 810-818.
Finkel, J.S. and Mitchell, A.P., 2011, Genetic control of Candida albicans biofilm development, Nat. Rev. Micro. 9: 109-118.
Frade, J.P. and Arthington-Skaggs, B.A., 2010, Effect of serum and surface characteristics on Candida albicans biofilm formation, Mycoses 54: e154-e162.
Ge, Y.P., Lu, G.X., Shen, Y.N. and Liu, W.D., 2011, In vitro evaluation of phospholipase, proteinase, and esterase activities of Candida parapsilosis and Candida metapsilosis, Mycopathologia 172: 429-438.
Hasan, F., Xess, I., Wang, X., Jain, N. and Fries, B.C., 2009, Biofilm formation in clinical Candida isolates and its association with virulence, Microb. Infect. 11: 753-761.
Hernández-Castro, R., Arroyo-Escalante, S., Carrillo-Casas, E., Moncada-Barrón, D., Álvarez-Verona, E., Hernández-Delgado, L., Torres-Narváez, P. and Lavalle-Villalobos, A., 2010, Outbreak of Candida parapsilosis in a neonatal intensive care unit: A health care workers source, Eur. J. Pediatr. 169: 783-787.
Marcos-Arias, C., Eraso, E., Madariaga, L., Aguirre, J.M. and Quindos, G., 2011, Phospholipase and proteinase activities of Candida isolates from denture wearers, Mycoses 54: e10-16.
Marra, A.R., Camargo, L.F., Pignatari, A.C., Sukiennik, T., Behar, P.R., Medeiros, E.A., Ribeiro, J., Girao, E., Correa, L., Guerra, C., Brites, C., Pereira, C.A., Carneiro, I., Reis, M., de Souza, M.A., Tranchesi, R., Barata, C.U., Edmond, M.B. and Brazilian, S.S.G., 2011, Nosocomial bloodstream infections in Brazilian hospitals: Analysis of 2,563 cases from a prospective nationwide surveillance study, J. Clin. Microbiol. 49: 1866-1871.
Melo, A.S., Bizerra, F.C., Freymuller, E., Arthington-Skaggs, B.A. and Colombo, A.L., 2011, Biofilm production and evaluation of antifungal susceptibility amongst clinical Candida spp. isolates, including strains of the Candida parapsilosis complex, Med. Mycol. 49: 253-262.
Novak Babič, M., Zalar, P., Ženko, B., Džeroski, S. and Gunde-Cimerman, N., 2016, Yeasts and yeast-like fungi in tap water and groundwater, and their transmission to household appliances, Fungal Ecol. 20: 30-
Odds, F.C., Hanson, M.F., Davidson, A.D., Jacobsen, M.D., Wright, P., Whyte, J.A., Gow, N.A.R. and Jones, B.L., 2007, One year prospective survey of Candida bloodstream infections in Scotland, J. Med. Microbiol. 56: 1066-1075.
Pannanusorn, S., Fernandez, V. and Römling, U., 2013, Prevalence of biofilm formation in clinical isolates of Candida species causing bloodstream infection, Mycoses 56: 264-272.
Pannanusorn, S., Ramírez-Zavala, B., Lünsdorf, H., Agerberth, B., Morschhäuser, J. and Römling, U., 2014, Characterization of biofilm formation and the role of Bcr1 in clinical isolates of Candida parapsilosis, Eukaryot. Cell 13: 438-451.
Pereira, L., Silva, S., Ribeiro, B., Henriques, M. and Azeredo, J., 2015, Influence of glucose concentration on the structure and quantity of biofilms formed by Candida parapsilosis, FEMS Yeast Res. 15: fov043.
Pfaller, M.A., Messer, S.A., Moet, G.J., Jones, R.N. and Castanheira, M., 2011, Candida bloodstream infections: Comparison of species distribution and resistance to echinocandin and azole antifungal agents in intensive care unit (ICU) and non-ICU settings in the SENTRY antimicrobial surveillance program (2008-2009), Int. J. Antimicrob. Agents 38: 65-69.
Pharkjaksu, S., Chongtrakool, P., Suwannakarn, K. and Ngamskulrungroj, P., 2018, Species distribution, virulence factors, and antifungal susceptibility among Candida parapsilosis complex isolates from clinical specimens at Siriraj Hospital, Thailand, from 2011 to 2015, Med. Mycol. 56: 426-433.
Reiss, E., Lasker, B.A., Iqbal, N.J., James, M.J. and Arthington-Skaggs, B.A., 2008, Molecular epidemiology of Candida parapsilosis sepsis from outbreak investigations in neonatal intensive care units, Infect. Genet. Evol. 8: 103-109.
Sabino, R., Sampaio, P., Rosado, L., Videira, Z., Grenouillet, F. and Pais, C., 2015, Analysis of clinical and environmental Candida parapsilosis isolates by microsatellite genotyping – A tool for hospital infection surveillance, Clin. Microbiol. Infect. 21: 954.e1-954.e8.
Sandven, P., Bevanger, L., Digranes, A., Haukland, H.H., Mannsaker, T. and Gaustad, P., 2006, Candidemia in Norway (1991 to 2003): Results from a nationwide study, J. Clin. Microbiol. 44: 1977-1981.
Sanitá, P.V., Zago, C.E., Pavarina, A.C., Jorge, J.H., Machado, A.L. and Vergani, C.E., 2014, Enzymatic activity profile of a Brazilian culture collection of Candida albicans isolated from diabetics and non-diabetics with oral candidiasis, Mycoses 57: 351-357.
Sarvikivi, E., Lyytikäinen, O., Soll, D.R., Pujol, C., Pfaller, M.A., Richardson, M., Koukila-Kähkölä, P., Luukkainen, P. and Saxén, H., 2005, Emergence of fluconazole resistance in a Candida parapsilosis strain that caused infections in a neonatal intensive care unit, J. Clin. Microbiol. 43: 2729-2735.
Shirkhani, S., Sepahvand, A., Mirzaee, M. and Anbari, K., 2016, Phospholipase and proteinase activities of Candida spp. isolates from vulvovaginitis in Iran, J. Mycol. Med. 26: 255-260.
Soldini, S., Posteraro, B., Vella, A., De Carolis, E., Borghi, E., Falleni, M., Losito, A.R., Maiuro, G., Trecarichi, E.M., Sanguinetti, M. and Tumbarello, M., 2018, Microbiologic and clinical characteristics of biofilm-forming Candida parapsilosis isolates associated with fungaemia and their impact on mortality, Clin. Microbiol. Nfect. 24: 771-777.
Storti, L.R., Pasquale, G., Scomparim, R., Galastri, A.L., Alterthum, F., Gambale, W. and Rodrigues Paula, C., 2012, Candida spp. isolated from inpatients, the environment, and health practitioners in the Pediatric Unit at the Universitary Hospital of the Jundiai Medical College, State of Sao Paulo, Brazil, Rev. Soc. Bras. Med. Trop. 45: 225-231.
Takakura, S., Fujihara, N., Saito, T., Kudo, T., Iinuma, Y., Ichiyama, S. and Group, t.J.I.M.S.S., 2004, National surveillance of species distribution in blood isolates of Candida species in Japan and their susceptibility to six antifungal agents including voriconazole and micafungin, J. Antimicrob. Chemother. 53: 283-289.
Tan, T.Y., Tan, A.L., Tee, N.W.S., Ng, L.S.Y. and Chee, C.W.J., 2010, The increased role of non-albicans species in candidaemia: Results from a 3-year surveillance study, Mycoses 53: 515-521.
Tortorano, A.M., Kibbler, C., Peman, J., Bernhardt, H., Klingspor, L. and Grillot, R., 2006, Candidaemia in Europe: Epidemiology and resistance, Int. J. Antimicrob. Agents 27: 359-366.
Trofa, D., Gacser, A. and Nosanchuk, J., 2008, Candida parapsilosis, an emerging fungal pathogen, Clin. Microbiol. Rev. 21: 606-625.
Wang, H., Zhang, L., Kudinha, T., Kong, F., Ma, X.J., Chu, Y.Z., Kang, M., Sun, Z.Y., Li, R.Y., Liao, K., Lu, J., Zou, G.L., Xiao, M., Fan, X. and Xu, Y.C., 2016, Investigation of an unrecognized large-scale outbreak of Candida parapsilosis sensu stricto fungaemia in a tertiary-care hospital in China, Sci. Rep. 6: 27099.
Welsh, R.M., Bentz, M.L., Shams, A., Houston, H., Lyons, A., Rose, L.J. and Litvintseva, A.P., 2017, Survival, persistence, and isolation of the emerging multidrug-resistant pathogenic yeast Candida auris on a plastic health care surface, J. Clin. Microbiol. 55: 2996-3005.
Zalar, P., Novak, M., de Hoog, G.S. and Gunde-Cimerman, N., 2011, Dishwashers – A man-made ecological niche accommodating human opportunistic fungal pathogens, Fungal Biol. 115: 997-1007.
Ziccardi, M., Souza, L.O.P., Gandra, R.M., Galdino, A.C.M., Baptista, A.R.S., Nunes, A.P.F., Ribeiro, M.A., Branquinha, M.H. and Santos, A.L.S., 2015, Candida parapsilosis (sensu lato) isolated from hospitals located in the southeast of Brazil: Species distribution, antifungal susceptibility and virulence attributes, Int. J. Med. Microbiol. 05: 848-859.
Zupančič, J., Novak Babič, M., Zalar, P. and Gunde-Cimerman, N., 2016, The black yeast Exophiala dermatitidis and other selected opportunistic human fungal pathogens spread from dishwashers to kitchens, PLoS ONE 11: e0148166.