Proteinase activities of Candida spp. isolated from different anatomical sites of healthy women
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Abstract
Superficial and systemic fungal infections caused by Candida have been increasingly reported in recent times. Hydrolytic enzyme production is an important process in fungal pathogenesis and proteases have been identified as important virulence attributes in Candida species. The aim of the study was to determine and compare the in vitro proteinase activity in sixty Candida spp isolated from three different anatomical sites (vagina, oral cavity and skin) of healthy women. Twenty samples per sample source were collected
from apparently healthy female subjects. The recovered Candida isolates were properly identified and screened for proteolytic activity using established procedures. Overall, the recovery rate of Candida albicans was 66.7%, while the non-albicans Candida species represent 25% of the positive samples. Candida albicans recovered from the oral cavity exhibited the highest proteolytic activity (Pz range =
0.41±0.02- 0.65 ± 0.04), followed by skin isolates (Pz = 0.50 ± 0.05 – 0.79 ± 0.06). Isolates from the vagina had the least proteolytic activity (Pz = 0.57 ± 0.03 - 0.95 ± 0.08). The difference in proteolysis was significant between oral and vagina isolates (p = 0.0042), as well as skin and vaginal isolates (p = 0.0364). This study indicates that C. albicans remains the most prevalent species in all the anatomical body sites investigated. Moreover, the secretion of proteases could prove a potent virulence factor during the pathogenesis of the organism in an otherwise immunocompetent host.
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References
Achkar, J.M, and Friesm B.C. (2010). Candida infections of the genitourinary tract. Clinical Microbiology Reviews, 23(2): 253 - 273.
Bradford, L. L. and Ravel, J. (2017). The vaginal mycobiome: A contemporary perspective on fungi in women’s health and diseases. Virulence, 8: 342 – 351.
Buu, L-M. and Chen, Y-C. (2014). Impact of glucose levels on expression of hypha – associated secreted aspartyl proteinases in Candida albicans. Journal of Biomedical Science, 21: 22.
Cassone, A., Vecchiarelli, A. and Hube, B. (2016). Aspartyl proteinases of eukaryotic microbial pathogens: From eating to heating. PLoS Pathogens, 12(12): e1005992.
Galocha, M., Pais, P., Cavalheiro, M., Pereira, D., Viana, R. and Teixeira, M. C. (2019). Divergent approaches to virulence in C. albicans and C. glabrata: Two Sides of the Same Coin. International Journal of Molecular Sciences, 20(9): 2345. doi:10.3390/ijms20092345.
Inci, M., Atalay, M. A., Koc, A.N., Yula, E., Evirgen, O., Durmaz, S. and Demir, G. (2012). Investigating virulence factors of clinical Candida isolates in relation to atmospheric conditions and genotype. Turkish Journal of Medical Sciences, 42(2): 1476 - 1483.
Oksuz, S., Sahin, I., Yildirim, M., Gulcan, A., Yavuz, T., Kaya, D. and Koc, A.N. (2007). Phospholipase and proteinase activities in different Candida spp isolated from anatomically distinct sites of healthy adults. Japanese Journal of Infectious Diseases, 60: 280 - 283.
Angebault, C., Djossou, F., Abelanet, S., Permal, E., Soltana, M. B., Diancourt, L., Bouchier, C., Woerther, P. L., Catzeflis, F., Andremont, A., d'Enfert, C. and Bougnoux, M. E. (2013). Candida albicans is not always the preferential yeast colonizing humans: A study in Wayampi Amerindians. The Journal of Infectious Diseases, 208: 1705 - 1716.
Rafat, Z., Hashemi, S. J., Ahamdikia, K., Ghazvini, R. and Bazvandi, F. (2017). Study of skin and nail Candida species as a normal flora based on age groups in healthy persons in Tehran - Iran. Journal of Medical Mycology, 27(4): 501 - 505.
Jenkinson, H. F. and Douglas, L. J. (2002). Interactions between Candida species and bacteria in mixed infections. In: Brogden, K. A., Guthmiller, J. M, editors: Polymicrobial Diseases. Washington (DC): ASM Press; 2002. Chapter 18.
Nejad, B. S., Rafiei, A. M. and Moosanejad, F. (2011). Prevalence of Candida species in the oral cavity of patients with periodontitis. African Journal of Biotechnology, 10 (15): 2987 - 2990.
Sato, T., Kishi, M., Suda, M., Sakata, K., Shimoda, H., Miura, H., Ogawa, A. and Kobayashi, S. (2017). Prevalence of Candida albicans and non - albicans on the tongue dorsa of elderly people living in a post - disaster area: a cross - sectional survey. BMC Oral Health, 17: 51.
Bajracharyya, B., Bhattacharya, S. and Poudel, P.(2019). Prevalence of Candida species in the oral cavity of oral cancer patients undergoing radiotherapy. Annals of King Edward Medical University, 25(2). Retrieved from https://annals.emu.org/Journal/index.php/annals/article/view 2859.
Singh, A., Verma, R., Murari, A. and Agrawal, A. (2014). Oral candidiasis: An overview. Journal of Oral and Maxillofacial Pathology, 18(1): S81- S85.
Byadarahally, R. S. and Rajappa, S. (2011). Isolation and identification of Candida from oral cavity. ISRN Dentistry, 2011: 487921.
Matic P. S., Radunovic, M., Barac, M., Kuzmanovic, P. J., Pavlica, D., Arsenijevic, V. A. and Pucar, A. (2019). Subgingival areas as potential reservoirs
of different Candida spp in type 2 diabetes patients and healthy subjects. PLoS ONE, 14(1): e0210527.
Farah, C.S., Lynch, N. and McCullough, M. J. (2010). Oral fungal infections: An update for the general practitioner. Australian Dental Journal, 55: s1.
Meira, H. C., Dr Oliveira, B. M., Pereira, I. F., Naves, M. D., Mesquita, R. A. and Santos, V. R. (2017). Oral candidiasis: A retrospective study of 276 Brazilian patients. Journal of Oral and Maxillofacial Pathology, JOMFP, 21(3): 351 - 355.
Patil, S., Rao, R. S., Majumdar, B. and Anil, S. (2015). Clinical appearance of oral Candida infection and therapeutic strategies. Frontiers in Microbiology, 6: 1391.
White, P. L., Williams, D. W., Kuriyama, T., Samad., Lewis, M.A. and Barnes, R.A. (2004). Detection of Candida in concentrated oral rinse cultures by Real - Time PCR. Journal of Clinical Microbiology, 42(5): 2101 - 2107.
Sitterle, E., Maufrais, C., Sertour, N., Palayret, M., d' Enfert, C. and Bougnoux, M.E. (2019). Within - host genomic diversity of Candida albicans in healthy carriers. Scientific Reports, 9: 2563.
Montelongo - Jauregui, D. and Lopez - Ribot, J. L. (2018). Candida interactions with the oral bacterial microbiota. Journal of Fungi, 4: 122.
Szymanska, J., Wojtowicz, A. and Malm, A. (2016). Assessment of Candida spp. frequency in the oral cavity ontocenosis of healthy individuals in different age groups. Journal of Pre - clinical and clinical Research, 10(2): 91 - 94.
Kuhbacher, A., Burger - Kentischer, A. and Rupp, S. (2017). Interaction of Candida species with the skin. Microorganisms, 5(2): 32.
Liam, J. S., Braga, K. R.., Vieira, C. A., Souza, W. W., Chavez – Pavoni, J. H., Araujo, C. and Goulart, L. S. (2018). Genotypic analysis of secreted aspartyl proteinases in vaginal Candida albicans isolates. Journal Brasileiro de Patologia e Medicinal Laboratorial, 54: 1.
Ribeiro, M. A., Dietze, R., Paula, C. R., Da Matta, D. A. and Colombo, A. L. (2001). Susceptibility profile of vaginal yeast isolates from Brazil. Mycopathologia, 151(1): 5 - 10.
Nsofor, C. A., Obijuru, C. E. and Ohalete, C. V. (2016). High prevalence of Candida albicans observed in asymptomatic young women in Owerri, Nigeria. Biomedicine and Biotechnology, 4 (1): 1-4.
Brandolt, T. M., Klafke, G. B., Goncaves, C. V., Bitencourt, L. R., Martinez, A. M., Mendes, J. F., Meireles, M. C. and Xavier, M. O. (2017). Prevalence of
Candida spp. in cervical - vaginal samples and the in vitro susceptibility of isolates. Brazilian Journal of Microbiology, 48(1): 145 - 150.
Makanjuola, O., Bongomin, F. and Fayemiwo, S. A. (2018). An update on the roles of non - albicans Candida species in vulvovaginitis. Journal of Fungi, 4: 21.
Mardegan, R. C., Foglio, M. A., Goncalves, R. B. and Hofling, J. F. (2006). Candida albicans proteinases. Brazilian Journal of Oral Science, 5(16): 944 - 952.
Modrzewska, B., Kurnatowski, P. and Khalid, K. (2016). Comparison of proteolytic activity of Candida spp. Strains depending on their origin. Journal of Medical Mycology, 26 (2): 138 – 147.
Zeng, X., Zhang, Y., Zhang, T., Xue, Y., Xu, H. and An, R. (2018). Risk factors of vulvovaginal candidiasis among women of reproductive age in Xian: A cross - sectional study. Biomed Research International, 2018: 9703754.
Amabebe, E. and Anumba, D. (2018). The vaginal microenvironment: The physiologic role of Lactobacilli. Frontiers in Medicine, 5: 181.
Staniszewska, M., Bondaryk, M., Pilat, J., Siennicka, K., Magda, U. and Kurzarkowski, W. (2012). Virulence factors of Candida albicans. Przeglad
Epidemiologiczny, 66(4): 629 - 633.
Jose, N. V., Mudhigeti, N., Asir, J. and Chandrakesan, S. D. (2015). Detection of virulence factors and phenotypic characterization of Candida isolates from clinical specimens. Journal of Current Research in Scientific Medicine, 1(1): 27 - 31.
Akcaglar, S. Erier, B. and Tore, O. (2011). Acid proteinase enzyme activity in Candida albicans strains: a comparison of spectrophotometry and plate methods. Turkish Journal of Biology, 35: 559 - 567.
Lahkar, V., Saikia, L., Patgiri, S. J., Nath, R., and Das, P. P. (2017). Estimation of biofilm, proteinase and phospholipase production of the Candida species isolated from the oropharyngeal samples in HIV-infected patients. The Indian Journal of Medical Research, 145(5): 635–640.