Iranian Journal of Microbiology 2016. 8(6):410-417.

Isolation, molecular identification, and antifungal susceptibility profiles of vaginal isolates of Candida species
Ali Rezaei-Matehkolaei, Shokoofe Shafiei, Ali Zarei Mahmoudabadi

Abstract


Background and Objectives: Vulvovaginal candidiasis is a common fungal infection among women during reproductive ages. Although, Candida albicans is accounted as the main etiologic agent of vaginitis, non-albicans species have arisen during last years. Resistant to antifungal drugs especially, fluconazole has been more reported by researchers from around the World. The aims of this study were to determine the prevalence of vulvovaginal candidiasis among suspected patients with vaginitis, the frequency of Candida species, and the susceptibility profiles of isolates to caspofungin, fluconazole and clotrimazole.

Materials and Methods: One hundred and twenty suspected women with vaginitis were examined by specialist physician and sampled using moisture swabs. Swabs were inoculated on CHROMagar Candida plates, incubated at 35ºC and detected all isolated Candida species using morphological, microcopy and molecular methods. The antifungal susceptibility tests with caspofungin, fluconazole and clotrimazole were applied using microdilution and Resazurin dye methods against all isolated yeasts.

Results: The cultures were positive for 34(28.3%) samples and three Candida species including; C. albicans (88.2%), C. glabrata (8.8%) and C. kefyr (2.9%). Our study shows that only one isolate of C. albicans was resistant to caspofungin at the concentration of 2 μg/ml after 24h incubation that increased to 2 isolates after 48h incubation. All isolates were sensitive to fluconazole at the MIC ranges of 1-0.25 μg/ml, while 88.2% of them were inhibited at 0.25 μg/mL of clotrimazole. Candida albicans remains the most common agent of fungal vaginitis.

Conclusion: Although all of Candida isolates were susceptible to fluconazole in vitro, it should be used with caution for empirical therapy due to more resistant rates in clinic. In addition, due to valuable sensitivity of all tested strains to caspofungin, it potentially can be presented as the first line therapy for Candida vaginitis.

Keywords: Caspofungin, Fluconazole, Clotrimazole, Candida vaginitis, Candida albicans


Keywords


Caspofungin; Fluconazole; Clotrimazole; Candida vaginitis; Candida albicans

Full Text:

PDF

References


Shokri H, Khosravi AR, Yalfani R. Antifungal effica- cy of propolis against fluconazole-resistant Candida glabrata isolates obtained from women with recur- rent vulvovaginal candidiasis. Int J Gynaecol Obstet 011;114:158-159.

Zarei Mahmoudabadi A, Najafyan M, Alidadi M. Clin- ical study of Candida vaginitis in Ahvaz, Iran and sus- ceptibility of agents to topical antifungal. Pak J Med Sci 2010;26:607-610.

Diba K, Namaki A, Ayatolahi H, Hanifian H. Rapid identification of drug resistant Candida species caus- ing recurrent vulvovaginal candidiasis. Med Mycol J 2012;53:193-198.

Ray A, Ray S, George AT, Swaminathan N. Interven- tions for prevention and treatment of vulvovaginal candidiasis in women with HIV infection. Cochrane Database Syst Rev 2011(8):CD008739.

Mendling W, Brasch J, German Society for G, Ob- stetrics, Working Group for I, Infectimmunology in G, et al. Guideline vulvovaginal candidosis (2010) of the German society for gynecology and obstetrics, the working group for infections and infectimmunology in gynecology and obstetrics, the German society of dermatology, the board of German dermatologists and the German speaking mycological society. Mycoses

;55 Suppl 3:1-13.

Mohamadi J, Havasian MR, Panahi J, Pakzad I. Anti- fungal drug resistance pattern of Candida. spp isolated from vaginitis in Ilam-Iran during 2013-2014. Bioinfor- mation 2015;11:203-206.

Hedayati MT, Taheri Z, Galinimoghadam T, Aghili SR, Yazdani Cherati J, Mosayebi E. Isolation of differ- ent species of Candida in patients with vulvovaginal candidiasis from Sari, Iran. Jundishapur J Microbiol 2015;8(4):e15992.

Shi XY, Yang YP, Zhang Y, Li W, Wang JD, Huang WM, et al. Molecular identification and antifungal susceptibility of 186 Candida isolates from vulvovag- inal candidiasis in southern China. J Med Microbiol 2015;64(Pt 4):390-393.

Rasti S, Asadi MA, Taghriri A, Behrashi M, Mousav- ie G. Vaginal candidiasis complications on pregnant women. Jundishapur J Microbiol. 2014;7(2):e10078.

Mendling W, Brasch J, Cornely OA, Effendy I, Friese K, Ginter-Hanselmayer G, et al. Guideline: vulvovagi- nal candidosis (AWMF 015/072), S2k (excluding chron- ic mucocutaneous candidosis). Mycoses 2015;58 Suppl 1:1-15.

Gamarra S, Morano S, Dudiuk C, Mancilla E, Nardin ME, de Los Angeles Mendez E, et al. Epidemiology and antifungal susceptibilities of yeasts causing vul- vovaginitis in a teaching hospital. Mycopathologia 2014;178(3-4):251-258.

Zarei Mahmoudabadi A, Najafyan M, Moghimipour E, Alwanian M, Seifi Z. Lamisil versus clotrimazole in the treatment of vulvovaginal candidiasis. Iran J Mi- crobiol 2013;5:86-90

Shan Y, Fan S, Liu X, Li J. Prevalence of Candida al-bicans-closely related yeasts, Candida africana and Candida dubliniensis, in vulvovaginal candidiasis. Med Mycol 2014;52:636-640.

Seifi Z, Zarei Mahmoudabadi A, Zarrin M. Extra- cellular enzymes and susceptibility to fluconazole in Candida strains isolated from patients with vaginitis and healthy individuals. Jundishapur J Microbiol 2015;8(3):e20162.

Li J, Shan Y, Fan S, Liu X. Prevalence of Candida ni- variensis and Candida bracarensis in vulvovaginal Candidiasis. Mycopathologia 2014;178(3-4):279-283.

Alfouzan W, Dhar R, Ashkanani H, Gupta M, Rachel C, Khan ZU. Species spectrum and antifungal suscep- tibility profile of vaginal isolates of Candida in Kuwait. J Mycol Med 2015;25:23-28.

Wang FJ, Zhang D, Liu ZH, Wu WX, Bai HH, Dong HY. Species distribution and In vitro antifungal sus- ceptibility of vulvovaginal Candida isolates in China. Chin Med J 2016;129:1161-1165.

Liu XP, Fan SR, Peng YT, Zhang HP. Species distribu- tion and susceptibility of Candida isolates from patient with vulvovaginal candidiasis in Southern China from 2003 to 2012. J Mycol Med 2014;24:106-111.

Nasrollahi Z, Yadegari MH, Roudbar Mohammadi S, Roudbary M, Hosseini Poor M, Nikoomanesh F, et al. Fluconazole resistance Candida albicans in fe- males with recurrent vaginitis and Pir1 overexpression. Jundishapur J Microbiol 2015;8(9):e21468.

Villanueva A, Gotuzzo E, Arathoon EG, Noriega LM, Kartsonis NA, Lupinacci RJ, et al. A randomized dou- ble-blind study of caspofungin versus fluconazole for the treatment of esophageal candidiasis. Am J Med 2002;113:294-299.

Veroux M, Macarone M, Fiamingo P, Cappello D, Gagliano M, Di Mare M, et al. Caspofungin in the treatment of azole-refractory esophageal candidia- sis in kidney transplant recipients. Transplant Proc 2006;38:1037-1039.

Mihu MR, Pattabhi R, Nosanchuk JD. The impact of antifungals on toll-like receptors. Front Microbiol 2014;5:99.

Leon-Gil C, Ubeda-Iglesias A, Loza-Vazquez A, de la Torre MV, Raurich-Puigdevall JM, Alvarez-Sanchez B, et al. Efficacy and safety of caspofungin in critically ill patients. ProCAS Study. Revista Espanola de Quim- ioterapia 2012;25:274-282.

Maertens J, Raad I, Petrikkos G, Boogaerts M, Sell- eslag D, Petersen FB, et al. Efficacy and safety of caspofungin for treatment of invasive aspergillosis in patients refractory to or intolerant of conventional anti- fungal therapy. Clin Infect Dis 2004;39:1563-1571.

Zarei Mahmoudabadi A, Rezaei-Matehkolaei A, Gha- navati F. The susceptibility patterns of Candida species isolated from urine samples to posaconazole and caspo-fungin. Jundishapur J Mmicrobiol 2015;8(3):e24298.

White TJ, Bruns T, Lee S, Taylor J (1990). Amplifica- tion and direct sequencing of fungal ribosomal RNA genes for phylogenetics. In: nPCR - Protocols and Ap- plications - A Laboratory Manual. Academic Press, Cambridge, Massachusetts, USA pp.315-3322.

Mohammadi R, Mirhendi H, Rezaei-Matehkolaei A, Ghahri M, Shidfar MR, Jalalizand N, et al. Molecu- lar identification and distribution profile of Candida species isolated from Iranian patients. Med Mycol 2013;51:657-663.

Elshikh M, Ahmed S, Funston S, Dunlop P, McGaw M, Marchant R, et al. Resazurin-based 96-well plate mi- crodilution method for the determination of minimum inhibitory concentration of biosurfactants. Biotechnol Lett 2016;38:1015-1019.

Rex JH, Alexander BD, Andes D, Arthington-Skaggs B, Brown SD, Chaturvedi V, et al. Refrence method for broth dilution abtifungal suceptibility testing of yeasts; approved standard-third edition. M27-A3 2008;28(14).

Guzel AB, Aydin M, Meral M, Kalkanci A, Ilkit M.Clinical characteristics of Turkish women with Can- dida krusei vaginitis and antifungal susceptibility of the C. krusei isolates. Infect Dis Obstet Gynecol 2013;2013:698736.

Donders GG, Bellen G, Mendling W. Management of recurrent vulvo-vaginal candidosis as a chronic illness. Gynecol Obstet Invest 2010;70:306-321.

Zhu YX, Li T, Fan SR, Liu XP, Liang YH, Liu P.Health-related quality of life as measured with the Short-Form 36 (SF-36) questionnaire in patients with recurrent vulvovaginal candidiasis. Health Qual Life Outcomes 2016;14:65.

Sobel JD. Recurrent vulvovaginal candidiasis. Am J Obstet Gynecol 2016;214:15-21.

Akimoto-Gunther L, Bonfim-Mendonca Pde S, Takahachi G, Irie MM, Miyamoto S, Consolaro ME, et al. Highlights regarding host predisposing fac- tors to recurrent vulvovaginal candidiasis: chronic stress and reduced antioxidant capacity. PloS One 2016;11(7):e0158870.

Fornari G, Vicente VA, Gomes RR, Muro MD, Pin- heiro RL, Ferrari C, et al. Susceptibility and molecu- lar characterization of Candida species from patients with vulvovaginitis. Brazil J Microbiol 2016;47(2):373-380.

Malazy OT, Shariat M, Heshmat R, Majlesi F, Alimo- hammadian M, Tabari NK, et al. Vulvovaginal candi- diasis and its related factors in diabetic women. Taiwan J Obstet Gynecol 2007;46(4):399-404.

Mahmoudi Rad M, Zafarghandi S, Abbasabadi B, Ta- vallaee M. The epidemiology of Candida species as- sociated with vulvovaginal candidiasis in an Iranian patient population. Eur J Obstet Gynecol Reprod Biol 2011;155(2):199-203.

Singh S, Sobel JD, Bhargava P, Boikov D, Vazquez JA.Vaginitis due to Candida krusei: epidemiology, clini- cal aspects, and therapy. Clin Infect Dis 2002;35:1066-1070.

Mohanty S, Xess I, Hasan F, Kapil A, Mittal S, Tolo- sa JE. Prevalence and susceptibility to fluconazole of Candida species causing vulvovaginitis. Indian J Med Res 2007;126:216-219.

Bennett JE, Izumikawa K, Marr KA. Mechanism of increased fluconazole resistance in Candida glabra- ta during prophylaxis. Antimicrob Agents Chemother 2004;48:1773-1777.

Khoursandi M, Modares Gilani M, Khosravi A. Re- covery and recurrence of vaginal candidiasis after oraland intravaginal treatment. J Qazvin Univ Med Sci2000(14):25-29.

Diaz MC, Camponovo R, Araya I, Cerda A, Santander MP, Carrillo-Munoz AJ. [Identification and in vitro an- tifungal susceptibility of vaginal Candida spp. isolates to fluconazole, clotrimazole and nystatin]. Revista Es- panola de Quimioterapia 2016;29:151-154.

Moges B, Bitew A, Shewaamare A. Spectrum and the In Vitro Antifungal Susceptibility Pattern of Yeast Iso- lates in Ethiopian HIV Patients with Oropharyngeal Candidiasis. Int J Microbiol 2016;2016:3037817.

Balashov SV, Park S, Perlin DS. Assessing resistance to the echinocandin antifungal drug caspofungin in Candida albicans by profiling mutations in FKS1. An- timicrob Agents Chemother 2006;50:2058-2063.


Refbacks

  • There are currently no refbacks.


Creative Commons Attribution-NonCommercial 3.0

This work is licensed under a Creative Commons Attribution-NonCommercial 3.0 Unported License which allows users to read, copy, distribute and make derivative works for non-commercial purposes from the material, as long as the author of the original work is cited properly.