Bifonazole in vitro activity and its azole-parallel resistance in clinical yeast isolates

V.A. Czaika, H.J. Tietz, A.F. Schmalreck

Abstract


The susceptibility/resistance profile of bifonazole (BFZ) in 170 dermatophyte strains including azole parallel-resistance in 324 clinical yeast isolates was determined, additionally with impact on patient-relevant factors. Overall susceptibility to four azoles tested in parallel was 70%, with differences to both, the azoles, and species-specific for isolates from patients with superficial or invasive/systemic infections. 86% of the C. glabrata (n=166) isolates were susceptible to bifonazole, 76% were BFZ-susceptible to fluconazole-resistant C. glabrata (n=184) isolates, whereas 45% of the bifonazole-resistant strains (n=82) were susceptible to FLC. However, compared to voriconazole most of the other non-C. albicans Candida, and non-Candida species were less susceptible (< 50%) to bifonazole. As the other azoles tested, BFZ showed bimodular MIC-distribution. Susceptibility pattern analysis (SPA) demonstrated that isolates from antifungal agent pretreated patients had zero to significant less complete susceptible isolates (SP: SSSS) compared to non-treated patients. Furthermore, SPA revealed zero to fourfold parallel-resistance, species-specifically distributed, most prominently in C. glabrata and C. parapsilosis. Evaluation of azole susceptibility and two-way hierarchical clustering revealed a high grade of diversity and heterogeneity among the clinical C. glabrata isolates. A modified MIC assessment system was introduced to achieve a more realistic, well-arranged, and therapy oriented reporting of MIC in vitro data.

Keywords


azoles;bifonazole;yeasts;C. glabrata;cross-resistance;MAR indexing

Full Text:

PDF

References


} Hector, R.F., and Braun P.C. 1987 The Effects of Bifonazole on Chitin Synthesis in Candida albicans. In: Recent Trends in the Discovery, Development and Evaluation of Antifungal Agents. R.A. Fromtling (ed.), pp. 369-382. J.R. Prous Science Publishers, S.A., Barcelona, Spain. [2] Hector, R.F. 1993. Compounds active against cell-wall active fungi. Clinical Microbiology Reviews, 6, 1-21. DOI: 10.1128/CMR.6.1.1. http://cmr.asm.org/content/6/1/1.full.pdf. [3] Bayer patient information: https://www.medicines.org.uk/EMC/medicine/26554/SPC/ Canesten+Bifonazole+Once+Daily+1++w+w+Cream/#INDICATIONS. [4] Mantry, S., Patnaik, A., Sriram, N., and Raju, V.B. 2013. Formulation and Evaluation of Bifonazole Organogel as a Novel Topical Drug Delivery System. International Journal of Pharmacy, 3, 1-8. http://www.ijpjournal.org/File_Folder/1-8.pdf. [5] Plempel, M., Regel, E., and Büchel, K.H. 1983. Antimycotic efficacy of bifonazole in vitro and in vivo. ArzneimittelForschung, 33, 17-524. [6] Crawford F., and Hollis, S. 2007. Topical treatments for fungal infections of the skin and nails of the foot. A Cochrane review, prepared and maintained by The Cochrane Collaboration and published in The Cochrane Library 2007, Issue 3. Copyright © 2009. The Cochrane Collaboration. Published by John Wiley & Sons, Ltd. http://onlinelibrary.wiley.com/doi/10.1002/14651858.CD001434.pub2/pdf/standard. [7] Chen, S., Zhou, D., Hsin, L.-Y., Kanaya, N., Wong, C., Yip, R., Sakamuru, S., Xia, M., Yuan, Y.-C., Witt, K., and Teng, C. 2014. AroER Tri-Screen is a Biologically Relevant Assay for Endocrine Disrupting Chemicals Modulating the Activity of Aromatase and/or the Estrogen Receptor. Toxicological Sciences, DOI: 10.1093/toxsci/kfu023. [8] Stylianou, M., Kulesskiy, E., Lopes, J.P., Granlund, M., Wennerberg, K., and Urban, C.F. 2013. Antifungal Application of Nonantifungal Drugs. Antimicrobial Agents and Chemotherapy, 58, 1055-1062. http://dx.doi.org/10.1128/AAC.01087-1. http://urn.kb.se/resolve?urn=urn:nbn:se:umu:diva-86824. [9] Czaika, V., Nenoff, P, Glöckner, 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. doi:10.1155/2013/703905. [10] Spampinato, C., and Leonardi D. 2013. Molecular Fingerprints to Identify Candida Species. BioMed Research International, Vol. 2013, Article ID 923742, 10 pages. doi:10.1155/2013/923742. [11] Fich, F., Abarzúa-Araya, A., Pérez, M., Nauhm, Y., and León E. 2014. Candida parapsilosis and Candida guilliermondii: Emerging Pathogens in Nail Candidiasis. Indian Journal of Dermatology, 59, 24–29. doi: 10.4103/0019-5154.123485. http://www.ncbi.nlm.nih.gov/pmc/articles/PMC3884923/?report=printable. [12 de la Rosa-García, E., Miramontes-Zapata, M., Sánchez-Vargas, L.O., and Mondragón-Padilla A. 2013. Oral colonisation and infection by Candida sp. in diabetic and non-diabetic patients with chronic kidney disease on dialysis. Nefrologia, 33, 764-70. doi:10.3265/Nefrologia.pre2013.Aug.11790. http://www.revistanefrologia.com/revistas/P1-E562/P1-E562-S4403-A11790-EN.pdf. [13] Merenstein, D., Hu, H., Wang, C., Hamilton, P., Blackmon, M., Chen, H., Calderone, R., and Li, D. 2013. Colonization by Candida Species of the Oral and Vaginal Mucosa in HIV-Infected and Noninfected Women. AIDS Research and Human Retroviruses, 29, 30-34. doi:10.1089/aid.2012.0269. [14] Pfaller, M.A., Pappas, P.G., and Wingard, J.R. 2009. Invasive Fungal Pathogens: Current Epidemiological Trends. Clinical Infectious Diseases, 43, Supplement 1, S3-S14. [15] Dabas, S. 2013. An approach to etiology, diagnosis and management of different types of candidiasis. Journal of Yeast and Fungal Research, 4(6), 63-74. DOI:10.5897/JYFR2013.0113. http://www.academicjournals.org/article/article1380027510_Dabas.pdf. [16] Papon, N., Courdavault, V, Clastre, M., and Bennett, R.J. 2013. Emerging and Emerged Pathogenic Candida Species: Beyond the Candida albicans Paradigm. PLoS Pathogens, 9: e1003550. doi:10.1371/journal.ppat.1003550. [17] Hamad, M., Kazandji, N., Awadallah., S, and Allam, H. 2014. Prevalence and epidemiological characteristics of vaginal candidiasis in the UAE. Mycoses, 57, 184-190. doi: 10.1111/myc.12141. [18] Adjapong, G., Hale, M., and Garrill, A. 2014. An investigation of the distribution of Candida species in genitourinary candidiasis and pelvic inflammatory disease from three locations in Ghana. African Journal of Microbiology Research, 8, 470-475. DOI: 10.5897/AJMR2013.6407. http://www.academicjournals.org/article/article1391683401_Adjapong%20et%20al.pdf [19] Colombo, A.L., Guimarães, T., Camargo, L.F.A., Richtmann, R., de Queiroz-Telles, F., Salles, M.J.C., da Cunha, C.A., Yasuda, M.A.S., Moretti, M.L., and Nucci, M. 2013. Brazilian guidelines for the management of candidiasis – a joint meeting report of three medical societies: Sociedade Brasileira de Infectologia, Sociedade Paulista de Infectologia and Sociedade Brasileira de Medicina Tropical. The Brazilian Journal of Infectious Diseases, 17(3), 283-312. http://www.scielo.br/pdf/bjid/v17n3/v17n3a01.pdf. [20] Pfaller, M.A., Diekema, D.J., Gibbs, D.L., Newell, V.A., Nagy, E., Dobiasova, S., Rinaldi, M., Barton, R., and Veselov A, Global Antifungal Surveillance Group. 2008. Candida krusei, a multidrug-resistant opportunistic fungal pathogen: geographic and temporal trends from the ARTEMIS DISK Antifungal Surveillance Program, 2001 to 2005. Journal of Clinical Microbiology, 46, 515–521. doi:10.1128/JCM.01915-07. http://www.ncbi.nlm.nih.gov/pmc/articles/PMC2238087/pdf/1915-07.pdf [21] Li, L., Redding, S., and Dongari-Bagtzoglou A. 2007. Candida glabrata, an Emerging Oral Opportunistic Pathogen. Journal of Dental Research, 85, 204-215. doi: 10.1177/154405910708600304. [22] Deorukhkar, S.C., and Saini S. 2013. Vulvovaginal Candidiasis due to non albicans Candida: its species distribution and antifungal susceptibility profile. Int. J. Curr. Microbiol. App. Sci. 2, 323-328. http://ijcmas.com/vol-2-12/Sachin%20C%20Deorukhkar%20and%20%20Santosh%20Saini.pdf. [23] Schaller, M., Mailhammer, R., Grassl, G., Sander, C.A., Hube, and B., Korting, H.C. 2002. Infection of Human Oral Epithelia with Candida Species Induces Cytokine Expression Correlated to the Degree of Virulence. Journal of Investigative Dermatology, 118, 652–657. doi:10.1046/j.1523-1747.2002.01699.x [24] Wilson, D., and Hube B. 2010. Hgc1 Mediates Dynamic Candida albicans-Endothelium Adhesion Events during Circulation. Eukaryot. Cell, 9, 278–287. doi: 10.1128/EC.00307-09. http://www.ncbi.nlm.nih.gov/pmc/articles/PMC2823009/pdf/zek278.pdf. [25] Sardi, J.C.O., Scorzoni, L., Bernardi, T., Fusco-Almeida, A.M., and Giannini, M.J.S. 2013. Candida species: current epidemiology, pathogenicity, biofilm formation, natural antifungal products and new therapeutic options. Journal of Medical Microbiology, 62, 10–24. http://jmm.sgmjournals.org/content/62/Pt_1/10.full.pdf+html. [26] Deorukhkar, S.C., Saini, S, and Mathew S. 2014. Virulence Factors Contributing to Pathogenicity of Candida tropicalis and Its Antifungal Susceptibility Profile. International Journal of Microbiology, vol. 2014, Article ID 456878, 6 pages. doi:10.1155/2014/456878. [27] Paswan, A.K., Raju, D.C., Singh, D.K., Dubey, R.K., and Mishra P.K. 2013. An observational study of the risk factors and incidence of invasive fungal infections in ICU patients. Anaesthesia, Pain & Intensive Care, 17(2), 136-140. [28] Pappas, P.G. 2006. Invasive candidiasis. Infect Dis Clin North Am. 20, 485-506. [29] Yapar, N. 2014. Epidemiology and risk factors for invasive candidiasis. Ther. Clin. Risk. Manag. 10, 95–105. PMCID: PMC3928396. doi: 10.2147/TCRM.S40160. http://www.ncbi.nlm.nih.gov/pmc/articles/PMC3928396/. [30] Yamamoto, M., Takakura, S., Hotta, G., Matsumura, Y., Matsushima, A., Nagao, M., Ito, Y., and Ichiyama, Y. 2013. Clinical characteristics and risk factors of non-Candida fungaemia. BMC Infectious Diseases, 13, 247. doi:10.1186/14712334-13-247. http://www.biomedcentral.com/1471-2334/13/247. [31] Shigemura, K., Osawa, K., Jikimot, T., Yoshida, H., Hayama, B., Ohji, G., Iwata, K., Fujisawa, M., and Arakawa S. 2014. Comparison of the clinical risk factors between Candida albicans and Candida non-albicans species for bloodstream infection. The Journal of Antibiotics 67, 311-314.| doi:10.1038/ja.2013.141. [32] Fidel, P.L. jr., Vazquez, J.A., and Sobel, J.D. 1999. Candida glabrata: review of epidemiology, pathogenesis, and clinical disease with comparison to C. albicans. Clinical Microbiology Reviews, 12, 1: 80–96. [33] Spinillo, A., Nicola, S., Colonna, L., Marangoni, E., Cavanna, C., and Michelone, G. 1994. Frequency and significance of drug resistance in vulvovaginal candidiasis. Gynecologic and Obstetric Investigation, 38, 2, 130–133. [34] Holland, J., Young, M.L., Lee, O., and Chen, S. C.-A. 2003. Vulvovaginal carriage of yeasts other than Candida albicans. Sexually Transmitted Infections, 79, 3: 249–250. http://sti.bmj.com/content/79/3/249.full.pdf+html. [35] Abu-Elteen, K.H. 2001. Increased incidence of vulvovaginal candidiasis caused by Candida glabrata in Jordan. Japanese Journal of Infectious Diseases, 54, 3: 103-107. [36] Spinillo, A., Capuzzo, E., Gulminetti, R., Marone, P., Colonna, L., and Piazzi, G. 1997. Prevalence of and risk factors for fungal vaginitis caused by non-albicans species. American Journal of Obstetrics and Gynecology, 176, 138–141. [37] Nelson, M., Wanjiru, W., and Margare, M. 2013. Identification and Susceptibility Profile of Vaginal Candida Species to Antifungal Agents among Pregnant Women Attending the Antenatal Clinic of Thika District Hospital, Kenya. Open Journal of Medical Microbiology, 3, Article ID:41023,9 pages. DOI:10.4236/ojmm.2013.34036. http://www.scirp.org/journal/PaperInformation.aspx?paperID=41023. [38] Aher, C.S. 2014. Species distribution, virulence factors and antifungal susceptibility profile of Candida isolated from Oropharyngeal lesions of HIV infected patients. Int. J. Curr. Microbiol. App. Sci., 3(1), 453-460. http://ijcmas.com/vol-31/Changdeo%20S.%20Aher.pdf. [39] Kothari, A. and Sagar, V. 2009. Epidemiology of Candida bloodstream infections in a tertiary care institute in India. Indian J Med Microbiol 27, 171–172. [40] Pahwa, N., Kumar, R., Nirkhiwale, S., and Bandi, A. 2014. Species distribution and drug susceptibility of Candida in clinical isolates from a tertiary care centre at Indore. Indian Journal of Medical Microbiology, 32, 44-48. [41] Yang, Y.-L., Ho, A., Cheng, H.H., Ho, M., and Lo, H,-J. 2004. Susceptibilities of Candida species to amphotericin B and fluconazole: the emergence of fluconazole resistance in Candida tropicalis. Infection Control and Hospital Epidemiology. 25, 60–64. [42] Kothavade, R.J., Kura, M.M., Valand, A.G., and Panthaki, M.H. 2010. Candida tropicalis: its prevalence, pathogenicity and increasing resistance to fluconazole. Journal of Medical Microbiology, 59, 873-880. doi: 10.1099/jmm.0.013227-0. http://jmm.sgmjournals.org/content/59/8/873.full.pdf+html. [43] Marchial, P., and Van den Bossche H., 1995. Mechanism of resistance to azole antifungals. Acta Biochimica Polonica, 42, 4: 509–516. [44] Van den Bossche, H. 199. Mechanism of antifungal resistance. Rev. Iberoam Micol, 14: 44–49. [45] Sobel, J.D. 1999. Vulvovaginitis in healthy women. Compr. Ther. 25, 335-346. [46] Mathema, B., Cross, E., Dun, E., Park, S., Bedell, J., Slade, B., Williams, M., Riley, L., Chaturvedi, V., and Perlin D.S. 2010. Prevalence of Vaginal Colonization by Drug-Resistant Candida Species in College-Age Women with Previous Exposure to Over-the-Counter Azole Antifungals. Clinical Infectious Diseases, 33, e23-e27. http://cid.oxfordjournals.org/content/33/5/e23.full.pdf+html. [47] Mulu, A., Kassu, A., Anagaw, B., Moges, B., Gelaw, A., Alemayehu, M., Belyhun, Y., Biadglegne, F., Hurissa, Z., Moges, F., and Isogai, E. 2013. Frequent detection of „azole‟ resistant Candida species among late presenting AIDS patients in northwest Ethiopia. BMC Infectious Diseases, 13, 82 doi:10.1186/1471-2334-13-82. http://www.biomedcentral.com/14712334/13/82. [48] Spampinato, C., and Leonardi, D. 2013. Candida Infections, Causes, Targets, and Resistance Mechanisms: Traditional and Alternative Antifungal Agents. BioMed Research International, vol. 2013, Article ID 204237, 13 pages. doi:10.1155/2013/204237. http://www.hindawi.com/journals/bmri/2013/204237/cta/. [49] Rodrigues, C.F., Silva, S., and Henriques M. 2013. Candida glabrata: a review of its features and resistance. Eur. J. Clin. Microbiol. Infect. Dis. DOI 10.1007/s10096-013-2009-3. [50] Spellberg, B.J., Filler, S.G., and Edwards, J.E. Jr. 2006. Current treatment strategies for disseminated candidiasis. Clin. Infect. Dis., 42, 244-251. http://www.ncbi.nlm.nih.gov/pubmed/16355336. [51] Sanguinetti, M., Posteraro, B., Fiori, B., Ranno, S., Torelli R., and Fadda, G. 2005. Mechanisms of azole resistance in clinical isolates of Candida glabrata collected during a hospital survey of antifungal resistance. Antimicrobial Agents and Chemotherapy, 49(2), 668-679. http://aac.asm.org/content/49/2/6. [52] Martinez, L., and Falson, P. 2014. Multidrug resistance ATP-binding cassette membrane transportes as targets for improving oropharyngeal candidiasis treatment. Advances in Cellular and Molecular Otolaryngology, 2, 23955. http://www.dx.doi.org.103402./acamo.v2.23955 [53] Morschhäuser, J., 2010, Regulation of multidrug resistance in pathogenic fungi. Fungal Genet. Biol. 47:94-106. [54] Rawal, M.K., Khan, M.F., Kapoor, K., Goyal, N., Sen, S., Saxena, A.K., Lynn, A.M., Tyndall, J.D., Monk, B.C., Cannon, R.D., Komath, S.S., Prasad, R. 2013. Insight into pleiotropic drug resistance ATP-binding cassette pump drug transport through mutagenesis of Cdr1p transmembrane domains. J. Biol. Chem. 288, 2480-2493. doi: 10.1074/jbc.M113.488353. 55 Cross, E.W., Park, andS., Perlin, D.S. 2000. Cross-Resistance of Clinical Isolates of Candida albicans and Candida glabrata to Over-the-Counter Azoles used in the treatment of vaginitis. International Federation of Gynecology and Obstetrics, 6, 2: 155–161. 56 Anderson, J.B., Sirjusingh, C., Parsons, A.B., Boone, C., Wickens, C., Cowen, L. E., and Kohn, L.M. 2003. Mode of Selection and Experimental Evolution of Antifungal Drug Resistance in Saccharomycescs cerevisiae . Genetics. 163, 1287–1298. 57 Salehei, Z., Seifi, Z., and Mahmoudabadi, A. 2012. Sensitivity of Vaginal Isolates of Candida to Eight Antifungal Drugs Isolated From Ahvaz, Iran. Jundishapur Journal of Microbiology, 5, 574-577. DOI: 10.5812/jjm.4556. http://jjmicrobiol.com/?page=article&article_id=4556. 58 Panackal, A.A., Gribskov, J.L., Staab, JF, Kirby K.A., Rinaldi M., and Marr K.A. 2006. Clinical significance of azole antifungal drug cross-resistance in Candida glabrata. J Clin Microbiol. 44, 1740-1743. 59 Pfaller, M.A., Castanheira, M., Lockhart, S.R., Ahlquist A.M., Messer S.A., Jones R.N. 2012. Frequency of decreased susceptibility and resistance to echinocandins among fluconazole-resistant bloodstream isolates of Candida glabrata. J. Clin. Microbiol. 50, 1199-1203. http://www.ncbi.nlm.nih.gov/pmc/articles/PMC3318516/. 60 Paul, S., and Moye-Rowley W.S. 2014. Multidrug resistance in fungi: regulation of transporter-encoding gene expression. Frontiers in Physiology, 16 April 2014. doi: 10.3389/fphys.2014.00143. http://journal.frontiersin.org/Journal/10.3389/fphys.2014.00143/full. 61 Verweij, P.D., Warris, A. 2013. Update on Antifungal Resistance in Children: Epidemiology and Recommendations. The Pediatric Infectious Disease Journal, 32 (5), 556-557. http://journals.lww.com/pidj/Documents/May%2013%20ESPID%20Update_on_Antifungal_Resistance_in_Children_.24.pd f. 62 Cuenca-Estrella, M. 2013. Antifungal Drug Resistance Mechanisms in Pathogenic Fungi: From Bench to Bedside. doi: 10.1111/1469-0691.12495. 63 Krogh-Madsen, M., Arendrup, M.C., Heslet, L., Knudsen, J.D. 2006. Amphotericin B and caspofungin resistance in Candida glabrata isolates recovered from a critically ill patient. Clin. Infect. Dis. 42, 938-944. http://cid.oxfordjournals.org/content/42/7/938.full. 64 Hull, C.M., Parker, J.E., Bader, O., Weig, M., Gross, U., Warrilow, A.G.S, Kelly, D.E., and Kelly,S.L. 2012. Facultative sterol uptake in an ergosterol deficient clinical isolate of Candida glabrata harboring a missense mutation in ERG11 and exhibiting cross-resistance to azoles and amphotericin B. Antimicrob. Agents Chenother. 56, 4223-4232. 65 Schmalreck, A.F., Czaika, V., Fegeler, W., and Becker, K. 2014. „Correlation of azole susceptibility with phenotype and genotype in Candida glabrata?‟ Submitted for publication. 66 Schmalreck, A.F., Willinger, B., Haase, G., Blum, G., Lass-Flörl, C., Fegeler, W., Becker, K., and the Antifungal Susceptibility Testing (AFST) Study Group. 2012. Species and susceptibility distribution of 1062 clinical yeast isolates to azoles, echinocandins, flucytosine and amphotericin B from a multi-centre study. Mycoses. 55, e124–e137. DOI: 10.1111/j.1439-0507.2011.02165.x 67 Schmalreck, A.F., Lackner, M., Becker, K., Fegeler, W., Czaika, V., Ulmer, H., and Lass-Flörl, C. 2014. Phylogenetic Relationships Matter: Antifungal Susceptibility among Clinically Relevant Yeasts. Antimicrob. Agents Chemother. 58, 1575-1585. 68 Index Fungorum., accessed August 2014. http://www.indexfungorum.org/names/names.asp. 69 MycoBank, accessed August 2014. www.mycobank.org. 70 EUCAST. 2012. Document E.DEF 7.2: Method for the determination of broth dilution of antifungal agents for fermentative yeasts; revised March, European Committee an Antifungal Susceptibiklity Testing. http://www.eucast.org/fileadmin/src/media/PDFs/EUCAST_files/AFST/EUCAST_EDef_7_2_revision.pdf. 71 EUCAST clinical breakpoints – fungi v6.1. 2013, The European Committee on Antimicrobial Susceptibility Testing ( EUCAST). http://www.eucast.org/antifungal_susceptibility_testing_afst/. 72 Arendrup, M.C., Garcia-Effron, G., Lass-Flörl, C., Gomez Lopez, A., Rodriguez-Tudela, J.-L., Cuenca-Estrella, M., and Perlin D.S. 2009. Susceptibility testing of Candida species to echinocandins: comparison of EUCAST EDef 7.1, CLSI M27A3, Etest, disk diffusion and agar-dilution using RPMI and IsoSensitest medium. Antimicrob. Agents Chemother. 54, 426439. 73 Grimm H. 1991. In-vitro-Empfindlichkeit gegenüber Ciprofloxacin in Klinik und Praxis - Aktueller Vergleich mit anderen Wirkstoffen. FAC Fortschritte Antimikrob. Antineoplast. Chemother. 10, 233-251. (Article in German). 74 Fegeler, W., D. Lintz, D., and Ritzerfeld, W. 1998. Resistance Pattern Analysis - A step Towards Predictable Differentiated Antibiotic Therapy. Zentralbl. Bakteriol. A, 270, 153-159. 75 Schmalreck, A.F., Willinger, B., Czaika, V., Fegeler, W., Becker, K., Blum, K, and Lass-Flörl, C. (2012) Susceptibility Screening of Hyphae-Forming Fungi with a New, Easy, and Fast Inoculum Preparation Method. Mycopathologia, 174:9770-9577, Available at: DOI 10.1007/s11046-012-9570-7. 76 Krumperman, P. H. 1983. Appl. Environ. Microbiol., 46, 165-170. 77 Santolaya, M.E., de Queiroz Telles, F., Matute, T.A., Colombo, A.L., Zurita, J., Tirabosch, I.N., Cortes, J.A., ThompsonMoya, L., Guzman-Blanco, M., Sifuentes, J., Echevarría, J., and Nucci M. 2013. Recommendations for the management of candidemia in children in Latin America. Revista Iberoamericana de Micología, 30, 171–178. http://dx.doi.org/10.1016/j.riam.2013.05.011. http://www.captura.uchile.cl/bitstream/handle/2250/133442/Recommendations%20for%20the%20management.pdf?seque nce=178 Gómez , J., García-Vázquez, E., Espinosa, C., Ruiz, J., Canteras, M., Hernández-Torres, A., Baños, V., Herrero, J.A., and Valdés, M. 2009. Nosocomial candidemia at a general hospital: the change of epidemiological and clinical characteristics. A comparative study of 2 cohorts (1993-1998 versus 2002-2005). Revista Iberoamericana de Micologia, 26(3):184-188. DOI: 10.1016/j.riam.2009.02.003. 79 Giri, S., Kindo, A. J., and Kalyani, J. 2013. Candidemia in intensive care unit patients: A one year study from a tertiary care center in South India. Journal of Postgraduate Medicine, 59(3), 190-195. http://www.jpgmonline.com/article.asp?issn=0022-3859;year=2013;volume=59;issue=3;spage=190; epage=195;aulast=Giri. 80 Papon, N., Courdavault, V., Clastre, M., and Bennett, R.J. 2013. Emerging and Emerged Pathogenic Candida Species: Beyond the Candida albicans Paradigm. PLoS Pathog 9(9): e1003550. doi:10.1371/journal.ppat.1003550. http://www.ploscollections.org/article/fetchObject.action?uri=info%3Adoi%2F10.1371%2Fjournal.ppat.1003550&represent ation=PDF. 81 Meyer, E., Geffers, C., Gastmeier, P., and Schwab, F. 2013. No increase in primary nosocomial candidemia in 682 German intensive care units during 2006 to 2011. Eurosurveillance, Volume 18, Article 5. http://www.eurosurveillance.org/ViewArticle.aspx?ArticleId=20505. 82 Puig-Asensio, M., Pemán, J., Zaragoza, R., Garnacho-Montero, J., Martín-Mazuelos, E., Cuenca-Estrella, M., and Almirante B; on behalf of the Prospective Population Study on Candidemia in Spain (CANDIPOP) Project, Hospital Infection Study Group (GEIH) and Medical Mycology Study Group (GEMICOMED) of the Spanish Society of Infectious Diseases and Clinical Microbiology (SEIMC), and Spanish Network for Research in Infectious Diseases. 2014. Impact of Therapeutic Strategies on the Prognosis of Candidemia in the ICU. Crit. Care. Med. 2014 Feb 19. [Epub ahead of print]. 83 Escribano, P., Rodríguez-Créixems, M., Sánchez-Carrillo, C., Muñoz, P., Bouza, E., and Guinea J. 201. Endemic Genotypes of Candida albicans Causing Fungemia Are Frequent in the Hospital. J. Clin. Microbiol. 51, 2118-2123. doi: 10.1128/JCM.00516-13. http://jcm.asm.org/content/51/7/2118.full.pdf+html. 84 Imran, Z.K., and Al Ghalibi, H. 2014. Genotypic Identification of Candida spp. Isolated from Onychocandidiasis Patients by Phenotypic Methods, PCR and RAPAD-PCR. American Medical, Journal 5, 1-7. doi:10.3844/amjsp.2014.1.7.thescipub.com/pdf/10.3844/amjsp. 2014.1.7 85 Gunther, L.S.A., Martins, H.P.R., Gimenes, F., de Abreu, A., Consolaro, M.E.L., and Svidzinski T.I.E. 2014. Prevalence of Candida albicans and non-albicans isolates from vaginal secretions: comparative evaluation of colonization, vaginal candidiasis and recurrent vaginal candidiasis in diabetic and non-diabetic women. Sao Paulo Med. J. 132( 2 ): 116-120. http://dx.doi.org/10.1590/1516-3180.2014.1322640. http://www.scielo.br/scielo.php?script=sci_arttext&pid=S1516-31802014000200116&lng=en. 86 Kumari, V., Banerjee T., Kumar, P., Pandey, S., Tilak, R. 2013. Emergence of non-albicans Candida among candidal vulvovaginitis cases and study of their potential virulence factors, from a tertiary care center, North India. Indian J. Pathol. Microbiol. 56, 144-147. http://www.ijpmonline.org/text.asp?2013/56/2/144/118703. 87 Makene, V.A. 2014. Identification of Non-albicans Candida Yeasts Associated with Vulvovaginal Candidiasis in Tanzania Using a Combination of Multiplex PCR and DNA Sequence Divergence of the 26S LSU rDNA. Scholars Academic Journal of Biosciences (SAJB), 2, 124-131. http://saspublisher.com/wp-content/uploads/2014/03/SAJB-22124-131.pdf. 88 Roetzer, A., Gabald, T., and Schuller C. 2011. From Saccharomyces cerevisiae to Candida glabrata in a few easy steps: important adaptations for an opportunistic pathogen. FEMS Microbiol. Lett. 314, 1–9. DOI:10.1111/j.1574-6968.2010.02102.x 89 Hof, H. 2010. Mycoses in the elderly. Eur J Clin Microbiol. 29, 5–13. 90 Martí-Carrizosa, M., Sánchez-Reus, F., March, F., and Coll P. 2014. Fungemia in a Spanish hospital: the role of Candida parapsilosis over a 15-year period. Scandinavian Journal of Infectious Diseases, Ahead of Print: Pages 1-8. doi:10.3109/00365548.2014.900190. 91 Flevari, A., Theodorakopoulou, M., Velegraki, A., Armaganidis, A.,and Dimopoulos, G. 2013. Treatment of invasive candidiasis in the elderly: a review. Clin. Interv. Aging. 8, 1199–1208. doi: 10.2147/CIA.S39120 hhttp://www.dovepress.com/treatment-of-invasive-candidiasis-in-the-elderly-a-review-peer-reviewed-article-CIA. 92 Ghahri, M., Mirhendi, H., Zomorodian, K., and Kondori, N. 2013. Identification and Antifungal Susceptibility Patterns of Candida Strains Isolated From Blood Specimens in Iran. Arch. Clin. Infect.. Dis. 8, e14529. archcid.com/26878.pdf 93 Taj-Aldeen, S. 2013. Epidemiology of candidemia in Qatar: Performance of MALDI-TOF MS for identification of Candida species, species distribution, outcome and susceptibility pattern. Qatar Foundation Annual Research Forum Proceedings: Vol. 2013, BIOP 096. DOI: 10.5339/qfarf.2013.BIOP-096. http://www.qscience.com/doi/abs/10.5339/qfarf.2013.BIOP-096 94 Yapar, N. 2014. Epidemiology and risk factors for invasive candidiasis. Ther. Clin. Risk. Manag. 10, 95–105. doi: 10.2147/TCRM.S40160. http://europepmc.org/articles/PMC3928396. 95 Montagna, M.T., Lovero, G., Borghi, E., Amato, G., Andreoini, S., Campion, L., Locasico, G., Lombardi, G., Luzarro, F., Manso, E., Mussap, M., Pecile, P., Perin, S., Tangorra, E., Tronci, M., Iatta, R., and Morac, G. 2014. Candedemia in intensive care unit: a nationwide prospective survey (GISA-3 study) and review of the European literature from 2000 to 2013. European Review for Medical and Pharmacological Sciences, 18, 661-674. http://www.europeanreview.org/wp/wp-content/uploads/661-674.pdf. 96 Berg, D., Regel, E., Harenberg, H.E., Plempel, M. 1984. Bifonazole and clotrimazole. Their mode of action and the possible reason for the fungicidal behaviour of bifonazole. Arzneimittelforschung, 34, 139-146. 97 Wächtler, B., Wilson, D., and Hube, B. 2011. Candida albicans Adhesion to and Invasion and Damage of Vaginal Epithelial Cells: Stage-Specific Inhibition by Clotrimazole and Bifonazole. Antimicrob. Agents Chemother. 55, 4436-4439. doi: 10.1128/AAC.00144-11. http://www.ncbi.nlm.nih.gov/pmc/articles/PMC3165311/pdf/zac4436.pdf 98 Berg, D. and Plempel, M. 1984. Bifonazole, a biochemist's view. Dermatologica, 169 Suppl 1, 3-9. 99 Shadomy, S., Dixon D.M., and May, R. 1982. A comparison of bifonazole (BAY H 4502) with clotrimazole in vitro. Sabouraudia, 20, 313-323. 100 Schwartz, J.R., DeAngelis, Y.M., and Dawson, jr. T.L. 2004. Dandruff and Seborrheic Dermatitis: A Head Scratcher. In: Baran R, Maibach HI (eds.). Textbook of Cosmetic Dermatology. London: Martin Dunitz, Ltd; Chapter 12, pp. 259-272. http://www.pgscience.com/files/pdf/Dr._Thomas_Dawson/TRI_book_chapter_Ch12_Dandruff.pdf. 101 Zienicke, H., Korting, H.C., Braun-Falco, O., Effendy, I., Hagedorn, M., Küchmeister, B., and Meisel, C. 1993. Comparative efficacy and safety of bifonazole 1% cream and the corresponding base preparation in the treatment of seborrhoeic dermatitis. Mycoses. 36, 325-331. 102 Van Gerven, F., and Odds, F.C. 1995. The anti-Malassezia furfur activity in vitro and in experimental dermatitis of six imidazole antifungal agents: bifonazole, clotrimazole, flutrimazole, ketoconazole, miconazole and sertaconazole. Mycoses, 38, 389-393. 103 Nenoff, P., Herrmann, J., Krüger, C., and Becker, N. 2012. Bifonazol - In vitro-Wirksamkeit gegenüber Corynebacterium minutissimum – ein Update zur Diagnostik und Therapie des Erythrasmas. Akt Dermatol., 38, 316-322. http://www.ccsenet.org/journal/index.php/gjhs/article/view/20198/14340. 104 Hanel, H., Abrams, B., Dittmar, W., and Ehlers, G. 1988. A comparison of bifonazole and ciclopiroxolamine: in vitro, animal and clinical studies. Mycoses, 31, 632-640. 105 Schaller, M., Borelli, C., Berger, U., Walker, B., Schmidt, S,., Weindl, G., Jaeckel, A. 2009. Susceptibility testing of amorolfine, bifonazole and ciclopiroxolamine against Trichophyton rubrum in an in vitro model of dermatophyte nail infection. Medical Mycology 47, 753–758. DOI 10.3109/13693780802577892. 106 Bari, A.A.A. 2012. Comparison of Superficial Mycosis treatment using Butenafine and Bifonazole nitrate Clinical Efficacy. Global Journal of Health Science, 5. DOI: 10.5539/gjhs.v5n1p150. 107 Tietz, H.-J., Hay, R., Querner, S., Delcker, A., Kurka, P., and Merk, H.F. 2013. Efficacy of 4 weeks topical bifonazole treatment for onychomycosis after nail ablation with 40% urea: a double-blind, randomized, placebo-controlled multicenter study. Mycoses. 56, 414-421. 108 Beggs, W.H. 1990. Potential of bifonazole for direct lethal action. Drugs Exp. Clin. Res. 16, 543-547. 109 Sahoo, C.K., Satyanarayana, K., Bomma, N.G., Modugu, K.R., Nayak, P.K., Sarangi, D.K., andSahoo, T.K. 2013. Formulation and evaluation of bifonazole organogel for the application of topical drug delivery system. Der. Pharmacia Sinica, 4, 67-74. http://pelagiaresearchlibrary.com/der-pharmacia-sinica/vol4-iss3/DPS-2013-4-3-67-74.pdf. 110 Korting, H. C., Kresimon, J., and Rychli R. 2004. Comparative Evaluation of the Activity and Clinical Effectiveness of Terbinafine and Bifonazole Preparations in the Treatment of Pedal Mycosis. Akt Dermatol 2004; 30(6): 210-217. DOI: 10.1055/s-2004-814541. (Article in German). https://www.thieme-connect.com/products/ejournals/html/10.1055/s-2004-814541. 111 Yamaguchi, H., Hiratani, T., and Plempel, M. 1983. In vitro studies of a new imidazole antimycotic, bifonazole, in comparison with clotrimazole and miconazole. Arzneimittelforsch. 33, 546–551. 112 Czaika, V., Nenoff, P., Glöckner, G., Becker, K., Fegeler, W., Lass-Flörl, C., and Schmalreck AF. 2014. Detection of azole susceptibility-patterns in clinical yeast strains isolated from 1997 to 2009. Newmicrobiologica. Accepted for publication. 113 Carrillo-Muñozm, A.J., and Torres-Rodriguez, J.M. 1995. In-vitro antifungal activity of sertaconazole, econazole, and bifonazole against Candida spp. J Antimicrob Chemother. 36(4):713-6. 114 Dota, K.F.D., Freitas, A.R., Consolaro, M.E.L., Svidzinski ,T.I.E. 2011. A Challenge for Clinical Laboratories: Detection of Antifungal Resistance in Candida species Causing Vulvovaginal Candidiasis. Labmedicine, 42, 87-92. 115 Cauwenberg, G. 1990. Vaginal Candidiasis: Evolving trends in the incidence and treatment of non-Candida albicans infection. Curr. Probl. Obstet. Gynecol. Fertil. 8, 241-245. [116] Achkar, J.M., and Fries, B.C. 2010. Candida Infections of the Genitourinary Tract. Clin. Microbiol. Rev. 23, 253-273. doi: 10.1128/CMR.00076-09. http://cmr.asm.org/content/23/2/253.full. [117] Bondaryk, M., Kurzatkowski, W., Staniszewska, M. 2013. Antifungal agents commonly used in the superficial and mucosal candidiasis treatment: mode of action and resistance development. Postep. Derm. Alergol. 5, 293-301. http://www.researchgate.net/publication/259387987_Antifungal_agents_commonly_used_in_the_superficial_and_mucosal _candidiasis_treatment_mode_of_action_and_resistance_development. [118] Carrillo-Mufloz, A.J., Tur, C., and Torres, J. 1996. In-vitro antifungal activity of sertaconazole, bifonazole, ketoconazole, and miconazole against yeasts of the Candida genus. Journal of Antimicrobial Chemotherapy, 37,815-819. http://jac.oxfordjournals.org/content/37/4/815.full.pdf. [119] Carrillo-Muñoz, A.J., and Tur-Tur, C. 1997. Comparative Study of Antifungal Activity of Sertaconazole, Terbinafine, and Bifonazole against Clinical Isolates of Candida spp., Cryptococcus neoformans and Dermatophytes. Chemotherapy, 43, 387-392. DOI:10.1159/000239596. [120] Tietz H.-J. 2010. Treatment of chronic vulvovaginal candidiasis with posaconazole and ciclopiroxolamine. Health 2: 513518. DOI: 10.4236/health.2010.26077. http://file.scirp.org/Html/1997.html [121] Watson, C., and Calabretto, H. 2007. Comprehensive review of conventional and non-conventional methods of management of recurrent vulvovaginal candidiasis. Aust. N. Z. J. Obstet. Gnyaecol. 47, 262-272. [122] Ringdahl, E.N. 2000. Treatment of Recurrent Vulvovaginal Candidiasis. Am. Fam. Phycisian, 61, 3306-3312. [123] Vermitzky, J.-P., Self, M.J., Chadwick, S.G., Trama, J.P., Adelson, M.W., Mordechai, E., and Gyax S.E. 2008. Survey of Vaginal-Flora Candida Species Isolates from Woman of Different Age Groups by Use of Species-Specific PCR Detection. J. Clin. Microbiol. 46, 1501-1503. Doi: 10.1128(JCM.02485-07. [124] Buitrón-García-Figueroa, R., Araiza-Santibáñez, J., Basurto-Kuba, E., and Bonifaz-Trujillo, A. Candida glabrata: an emergent opportunist in vulvovaginitis. Cir. Ciruj. 77, 423-427. [125] Tumbarello, M., Sanguinetti, M., Trecarichi, E.M., La Sorda, M., Rossi, M., de Carolis, E., de Gaetano Donati, K., Fadda, G., Roberto, Cauda R., and Posteraro, B. 2008. Fungaemia caused by Candida glabrata with reduced susceptibility to fluconazole due to altered gene expression: risk factors, antifungal treatment and outcome. J. Antimicrob. Chemother. 62 (6): 1379-1385. [126] Sobel, J.D. 2014. Candida vulvovaginitis. UpToDate, http://www.uptodate.com/contents/candida-vulvovaginitis. [127] Posteraro, B., Tumbarello, M., La Sorda, M., Spanu, T., Trecarichi, E.M., De Bernardis, F., Scoppettuolo, G., Sanguinetti, M., and Fadda G. 2006. Azole Resistance of Candida glabrata in a Case of Recurrent Fungemia. J. Clin. Microbiol. 44, 3046-3047. http://www.ncbi.nlm.nih.gov/pmc/articles/PMC1594598/pdf/0526-06.pdf. [128] Lin, M.Y., Carmeli, Y., Zumsteg, J., Flores, E.L., Tolentino, J., Sreeramju, P., and Weber, S.G. 2005. Prior Antimicrobial Therapy and Risk for Hospital-Acquired Candida glabrata ab Candida krusei Fungemia: a Case-Case-Control Study. Antimicrob. Agents Chemother. 49, 4555-4560. Doi: 10.1128/AAC.49.114555-4560.2005. [129] Ruhnke, M., Rickerts, V., Cornely, OA., Buchheidt, D., Glö̈ ckner, A., Heinz, W., Höhl, R., Horre, R., Karthaus, M., Kujath, R., Willinger, B., Presterl, E., Rath, P., Ritter, R., Glasmacher, A., Lass-Flö̈ rl, C., and Groll, A.H. 2011. Diagnosis and therapy of Candida infections: joint recommendations of the German Speaking Mycological Society and the Paul-EhrlichSociety for Chemotherapy. Mycoses, 54: 279–231. :10.1111/j.1439-0507.2011.02040.x. http://www.dmykg.de/fileadmin/download/Leitlinien/Candida.pdf [130] CLSI M27A3. 2008. Reference Method for Broth Dilution Antifungal Susceptibility Testing of Yeasts; Approved StandardThird Edition, M27-A3. Clinical and Laboratory Standards Institute, Wayne, PA, USA. [131] Odds, F.C., and Abbott, A.B. 1984. Relative inhibition factors - a novel approach to the assessment of antifungal antibiotics in vitro. J. Antimicrob. Chemother. 13, 31-43. doi: 10.1093/jac/13.1.31. [132] Odds, F.C., Webster, C.E., and Abbott, A.B. 1984. Antifungal relative inhibition factors: BAY 1–9139, bifonazole, butoconazole, isoconazole, itraconazole (R 51211), oxiconazole, Ro 14–4767/002, sulconazole, terconazole and vibunazole (BAY n-7133) compared in vitro with nine established antifungal agents. J. Antimicrob. Chemother. 14, 105114. doi:10.1093/jac/14.2.105 [133] Van Minnebruggen, G., François, I.E.J.A., Cammue, B.P.A., Thevissen, K., Vroome, V., Borger,s M., and Shroot, B. A general Overview on Past, Present and Future Antimycotics”, The Open Mycology Journal 01/2010; 4:22-32. [134] Sasse, C., Dunkel, N., Schafer, T., Schneider, S., Dierolf, F., Ohlsen, K., and Morschhäuser J. 2012. The stepwise acquisition of fluconazole resistance mutations causes a gradual loss of fitness in Candida albicans. Mol. Microbiol. 86, 539-556. doi:10.1111/j.1365-2958.2012.08210.x. [135] Rathod, V.S., Raut, J.S., and Karruppayil, M. 2012. In vitro antifungal susceptibility reveals occurrence of azole resistance among clinical isolates of Candida albicans. Asian J. Pharmaceut. Clin. Res. 5, 170-173. [136] Peters, B.M., Yano, J., Noverr, M.C., and Fidel, P.L. jr. 2014. Candida Vaginitis: When Opportunism Knocks, the Host Responds. PLoS Pathog 10(4): e1003965. doi:10.1371/journal.ppat.1003965. http://www.plospathogens.org/article/info%3Adoi%2F10.1371%2Fjournal.ppat.1003965. [137] Scott, M.T., Rose, J.B., Jenkins ,T.M., Forrah, S.R., and Lukasik, J. 2002. Microbial source tracing: Current methodology and future directions. Appl. Env. Microbiol. 68, 5796-5803. [138] Cross, E.W., Park, S., and Perlin, D.S. 2000. Cross-Ressistane of Clinical Isolates of Candida albicans and Candida glabrata to Over-the-Counter Azoles Used in the Treatment of Vaginitis. Microbial Drug Resistance, 6, 155-161. Doi: 10.1089/107662900419474. [139] Czaika, V.A., and Schmalreck A.F. 2014. In vitro susceptibility testing of dermatophytes with their fragmented mycelia as inoculum. J. Adv. Biol. In press


Refbacks

  • There are currently no refbacks.


Creative Commons License
This work is licensed under a Creative Commons Attribution 4.0 International License.

Copyright © 2007 Journal of Advances in Biology - All Rights Reserved