American Journal of Microbiological Research
ISSN (Print): 2328-4129 ISSN (Online): 2328-4137 Website: Editor-in-chief: Apply for this position
Open Access
Journal Browser
American Journal of Microbiological Research. 2017, 5(4), 78-85
DOI: 10.12691/ajmr-5-4-2
Open AccessResearch Article

Prevalence of Vaginal Infection by Multidrug Resistant Candida Species among Different Ages in Egypt

Mohammad. H. A. Hassan1, Mady. A. Ismail1 and Ahmed. M. Moharram Ahmed. M. Shoreit1,

1Department of Botany and Microbiology, Faculty of Science, Assiut University, Egypt

Pub. Date: August 22, 2017
(This article belongs to the Special Issue Antibiotic Resistance & Drug development)

Cite this paper:
Mohammad. H. A. Hassan, Mady. A. Ismail and Ahmed. M. Moharram Ahmed. M. Shoreit. Prevalence of Vaginal Infection by Multidrug Resistant Candida Species among Different Ages in Egypt. American Journal of Microbiological Research. 2017; 5(4):78-85. doi: 10.12691/ajmr-5-4-2


During 12 months’ the period of study from December 2015 to November 2016, one hundred and sixty women were clinically examined for vaginal yeast infection. Result revealed that 100 cases (62.5%) proved to have vaginal infection. The mean age (±SD) of the participants was 27.70±5.79 years. Most of the positive cases with high count belonged to the age group1 (19-25 year) followed by group 2 (26-30 year) representing 39 and 32 cases respectively (71 % of the total cases). Phenotypic and genotypic characterization of the yeast isolates showed that C. albicans were the predominant Candida species 258 cfu out of 410 cfu represent (62.9%) followed by C. lusitaniae (56 cfu, 13.7%), C. krusei (44 cfu 10.7%), C. glabrata (26 cfu, 6.3%), C. tropicalis (18 cfu, 4.4%) and C. Parapsilosis (8 cfu, 2.0%) respectively. In-vitro sensitivity test showed high resistance to the tested antifungals; whereas 73 isolates out of 128 (57.3%) were resistant to more than one type of tested antifungal agents, including 14 isolates showed resistance to all antifungal agents (Multidrug resistant strains). C. albicans represented by 67 isolates, showed resistance to one or more of the tested antifungal agents such as Fluconazole (61.2 %), Ketoconazole (56.7 %), Amphotericin B (52.2), Itraconazole and Nystatin (43.3 %). In case of non- albicans isolate (61 isolate) the most effective antifungal agent was Nystatin were it susceptible 65 % form C. lusitaniae isolates, 62.5 % from C. tropicalis and 60 % from C. Krusei isolates. The relation between risk factors, such as pregnancy, diabetes mellitus, history of antibiotic uses, and contraceptive methods, was recorded.

vulvovaginal candidiasis antifungal agents multidrug resistant phenotypic and genotypic characterization

Creative CommonsThis work is licensed under a Creative Commons Attribution 4.0 International License. To view a copy of this license, visit


Figure of 5


[1]  Sobel, JD., Vazquez JA. Symptomatic vulvovaginitis due to fluconazole-resistant Candida albicans in a female who was not infected with human immunodeficiency virus. Clinical infectious diseases 1996, 22(4):726-727.
[2]  Ghannoum, MA., Radwan SS. Candida adherence to epithelial cells: CRC Press; 1990.
[3]  Falagas, ME., Betsi GI., Athanasiou S. Probiotics for prevention of recurrent vulvovaginal candidiasis: a review. Journal of Antimicrobial Chemotherapy 2006, 58(2):266-272.
[4]  Akinbiyi, A., Watson R., Feyi-Waboso P. Prevalence of Candida albicans and bacterial vaginosis in asymptomatic pregnant women in South Yorkshire, United Kingdom. Archives of gynecology and obstetrics 2008, 278(5):463-466.
[5]  Mayer, FL., Wilson D., Hube B. Candida albicans pathogenicity mechanisms. Virulence 2013, 4(2):119-128.
[6]  Gandhi, TN., Patel MG., Jain MR. Prospective study of vaginal discharge and prevalence of Vulvovaginal candidiasis in a tertiary care hospital. International Journal of Current Research and Review 2015, 7(1):34.
[7]  Roshan, R., Sabokbar A., Badali H. Identification of Candida species isolated from vulvovaginal candidiasis using PCR-RFLP. International Journal of Molecular and Clinical Microbiology 2014, 4(2): 406-410.
[8]  Achkar, JM., Fries BC. Candida infections of the genitourinary tract. Clinical microbiology reviews 2010, 23(2):253-273.
[9]  Foxman, B., Muraglia R., Dietz J-P., Sobel JD., Wagner J. Prevalence of recurrent vulvovaginal candidiasis in 5 European countries and the United States: results from an internet panel survey. Journal of lower genital tract disease 2013, 17(3):340-345.
[10]  Sobel, JD. Genital candidiasis. In: Sexually Transmitted Infections and Sexually Transmitted Diseases. Springer; 2011: 613-624.
[11]  Nyirjesy, P., Sobel JD. Genital mycotic infections in patients with diabetes. Postgraduate medicine 2013, 125(3): 33-46.
[12]  Bauters, TG., Dhont MA., Temmerman MI., Nelis HJ. Prevalence of vulvovaginal candidiasis and susceptibility to fluconazole in women. American journal of obstetrics and gynecology 2002, 187(3):569-574.
[13]  Corsello, S., Spinillo A., Osnengo G., Penna C., Guaschino S., Beltrame A., Blasi N., Festa A. An epidemiological survey of vulvovaginal candidiasis in Italy. European journal of obstetrics & gynecology and reproductive biology 2003, 110(1):66-72.
[14]  [Wang, F-J., Zhang D., Liu Z-H., Wu W-X., Bai H-H., Dong H-Y. Species distribution and in vitro antifungal susceptibility of vulvovaginal Candida isolates in China. Chinese medical journal 2016, 129(10):1161.
[15]  Organization, WH. Antimicrobial resistance: 2014 global report on surveillance: World Health Organization; 2014.
[16]  Sievert, DM., Ricks P., Edwards JR., Schneider A., Patel J., Srinivasan A., Kallen A., Limbago B., Fridkin S. Antimicrobial-resistant pathogens associated with healthcare-associated infections summary of data reported to the National Healthcare Safety Network at the Centers for Disease Control and Prevention, 2009-2010. Infection Control & Hospital Epidemiology 2013, 34(01): 1-14.
[17]  Zhang, JY., Liu JH., Liu FD., Xia YH., Wang J., Liu X., Zhang ZQ., Zhu N., Ying Y., Huang XT. Vulvovaginal candidiasis: species distribution, fluconazole resistance and drug efflux pump gene overexpression. Mycoses 2014, 57(10): 584-591.
[18]  Nagashima, M., Yamagishi Y., Mikamo H. Antifungal susceptibilities of Candida species isolated from the patients with vaginal candidiasis. Journal of Infection and Chemotherapy 2016, 22(2): 124-126.
[19]  Mårdh, P-A., Rodrigues AG., Genç M., Novikova N., Martinez-de-Oliveira J., Guaschino S. Facts and myths on recurrent vulvovaginal candidosis--a review on epidemiology, clinical manifestations, diagnosis, pathogenesis and therapy. In.: SAGE Publications Sage UK: London, England; 2002.
[20]  Pappas, PG., Kauffman CA., Andes DR., Clancy CJ., Marr KA., Ostrosky-Zeichner L., Reboli AC., Schuster MG., Vazquez JA., Walsh TJ. Clinical practice guideline for the management of candidiasis: 2016 update by the Infectious Diseases Society of America. Clinical Infectious Diseases 2015: civ933.
[21]  Theill, L., Dudiuk C., Morano S., Gamarra S., Nardin ME., Méndez E., Garcia-Effron G. Prevalence and antifungal susceptibility of Candida albicans and its related species Candida dubliniensis and Candida africana isolated from vulvovaginal samples in a hospital of Argentina. Revista Argentina de Microbiología 2016, 48(1): 43-49.
[22]  Papon, N., Courdavault V., Clastre M., Bennett RJ. Emerging and emerged pathogenic Candida species: beyond the Candida albicans paradigm. PLoS Pathog 2013, 9(9): e1003550.
[23]  Richter, SS., Galask RP., Messer SA., Hollis RJ., Diekema DJ., Pfaller MA. Antifungal susceptibilities of Candida species causing vulvovaginitis and epidemiology of recurrent cases. Journal of Clinical Microbiology 2005, 43(5):2155-2162.
[24]  Consolaro, M., Albertoni T., Svidzinski A., Peralta R., Svidzinski T. Vulvovaginal candidiasis is associated with the production of germ tubes by Candida albicans. Mycopathologia 2005, 159(4): 501-507.
[25]  Alexander, BD., Johnson MD., Pfeiffer CD., Jiménez-Ortigosa C., Catania J., Booker R., Castanheira M., Messer SA., Perlin DS., Pfaller MA. Increasing echinocandin resistance in Candida glabrata: clinical failure correlates with presence of FKS mutations and elevated minimum inhibitory concentrations. Clinical infectious diseases 2013, 56(12): 1724-1732.
[26]  Fekkar, A., Dannaoui E., Meyer I., Imbert S., Brossas J., Uzunov M., Mellon G., Nguyen S., Guiller E., Caumes E. Emergence of echinocandin-resistant Candida spp. in a hospital setting: a consequence of 10 years of increasing use of antifungal therapy? European journal of clinical microbiology & infectious diseases 2014, 33(9):1489-1496.
[27]  Apalata, T., Longo-Mbenza B., Sturm A., Carr W., Moodley P. Factors associated with symptomatic vulvovaginal candidiasis: A study among women attending a primary healthcare clinic in Kwazulu-Natal, South Africa. Annals of medical and health sciences research 2014, 4(3):410-416.
[28]  Deorukhkar, SC., Saini S., Mathew S. Virulence factors contributing to pathogenicity of Candida tropicalis and its antifungal susceptibility profile. International journal of microbiology 2014, 2014.
[29]  Sobel, JD., Faro S., Force RW., Foxman B., Ledger WJ., Nyirjesy PR., Reed BD., Summers PR. Vulvovaginal candidiasis: epidemiologic, diagnostic, and therapeutic considerations. American journal of obstetrics and gynecology 1998, 178(2): 203-211.
[30]  Ellis, D., Davis S., Alexiou H., Handke R., Bartley R. Descriptions of medical fungi. Nexus Print Solutions, Adelaide, South Australia, Australia 2007.
[31]  Shettar, SK., Patil AB., Nadagir SD., Shepur T., Mythri B., Gadadavar S. Evaluation of HiCrome differential agar for speciation of candida. Journal of Academy of Medical Sciences 2012, 2(3):101.
[32]  White, TJ., Bruns T., Lee S., Taylor J. Amplification and direct sequencing of fungal ribosomal RNA genes for phylogenetics. PCR protocols: a guide to methods and applications 1990, 18(1): 315-322.
[33]  Wayne, P. Clinical and Laboratory Standards Institute: Reference method for broth dilution antifungal susceptibility testing of yeasts; approved standard-; CLSI document M27-A3. CLSI 2008a 2008, 28: 6-12.
[34]  Nurat, AA., Babalola GO., Shittu MO., Tijani MA., Adekola SA. Detection and epidemiology of vulvovaginal candidiasis among asymptomatic pregnant women attending a tertiary hospital in Ogbomoso, Nigeria. International Journal of Biomedical Research 2015, 6(7):518-523.
[35]  Benchellal, M., Guelzim K., Lemkhente Z., Jamili H., Dehainy M., Moussaoui DR., El Mellouki W., Idrissi KS., Lmimouni B. La candidose vulvo-vaginale à l’hôpital militaire d’instruction Mohammed V (Maroc). Journal de Mycologie Médicale/Journal of Medical Mycology 2011, 21(2): 106-112.
[36]  Holland, J., Young M., Lee O., Chen SC. Vulvovaginal carriage of yeasts other than Candida albicans. Sexually transmitted infections 2003, 79(3): 249-250.
[37]  Kent, HL. Epidemiology of vaginitis. American journal of obstetrics and gynecology 1991, 165(4): 1168-1176.
[38]  Kanagal, D., Vineeth V., Kundapur R., Shetty H., Rajesh A. Prevalence of Vaginal Candidiasis in Pregnancy among Coastal South Indian Women. J Womens Health, Issues Care 3 2014, 6:2.
[39]  Nelson, M., Wanjiru W., Margaret MW. Prevalence of vaginal candidiasis and determination of the occurrence of Candida species in pregnant women attending the antenatal clinic of Thika District Hospital, Kenya. Open Journal of Medical Microbiology 2013, 2013.
[40]  Aslam, M., Hafeez R., Ijaz S., Tahir M. Vulvovaginal Candidiasis in pregnancy. Biomedica 2008, 24: 54-56.
[41]  Paulitsch, A., Weger W., Ginter‐Hanselmayer G., Marth E., Buzina W. A 5‐year (2000–2004) epidemiological survey of Candida and non‐Candida yeast species causing vulvovaginal candidiasis in Graz, Austria. Mycoses 2006, 49(6): 471-475.
[42]  Vermitsky, J-P., Self MJ., Chadwick SG., Trama JP., Adelson ME., Mordechai E., Gygax SE. Survey of vaginal-flora Candida species isolates from women of different age groups by use of species-specific PCR detection. Journal of clinical Microbiology 2008, 46(4): 1501-1503.
[43]  Goswami, D., Goswami R., Banerjee U., Dadhwal V., Miglani S., Lattif AA., Kochupillai N. Pattern of Candida species isolated from patients with diabetes mellitus and vulvovaginal candidiasis and their response to single dose oral fluconazole therapy. Journal of Infection 2006, 52(2): 111-117.
[44]  Shi, X-Y., Yang Y-P., Zhang Y., Li W., Wang J-D., Huang W-M., Fan Y-M. Molecular identification and antifungal susceptibility of 186 Candida isolates from vulvovaginal candidiasis in southern China. Journal of medical microbiology 2015, 64(4): 390-393.
[45]  Yang, Z-T., Wu L., Liu X-Y., Zhou M., Li J., Wu J-Y., Cai Y., Mao E-Q., Chen E-Z., Lortholary O. Epidemiology, species distribution and outcome of nosocomial Candida spp. bloodstream infection in Shanghai. BMC infectious diseases 2014, 14(1): 241.
[46]  Gunther, LSA., Martins HPR., Gimenes F., Abreu ALPd., Consolaro MEL., Svidzinski TIE. 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. São paulo medical journal 2014, 132(2):116-120.
[47]  Kumari, V., Banerjee T., Kumar P., Pandey S., Tilak R. Emergence of non-albicans Candida among candidal vulvovaginitis cases and study of their potential virulence factors, from a tertiary care center, North India. Indian Journal of Pathology and Microbiology 2013, 56(2): 144.
[48]  Deorukhkar, SC., Saini S., Mathew S. Non-albicans Candida infection: an emerging threat. Interdisciplinary perspectives on infectious diseases 2014, 2014.
[49]  Ng, KP., Kuan CS., Kaur H., Na SL., Atiya N., Velayuthan RD. Candida species epidemiology 2000–2013: a laboratory‐based report. Tropical Medicine & International Health 2015, 20(11): 1447-1453.
[50]  Nyirjesy, P., Seeney SM., Grody MHT., Jordan CA., Buckley HR. Chronic fungal vaginitis: the value of cultures. American journal of obstetrics and gynecology 1995, 173(3): 820-823.
[51]  Liu, X., Fan S., Peng Y., Zhang H. Species distribution and susceptibility of Candida isolates from patient with vulvovaginal candidiasis in Southern China from 2003 to 2012. Journal de Mycologie Médicale/Journal of Medical Mycology 2014, 24(2): 106-111.