1887

Abstract

Purpose. Up to 75 % of all women develop vulvovaginal candidiasis (VVC), with symptoms such as vulvar erythema, pruritus and abnormal vaginal discharge. Despite the global distribution of Candida africana, its role in recurrent vulvovaginal candidiasis (RVVC) is still unclear and requires further investigation. Here, we report on the frequency of C. africana among clinical isolates from patients with RVVC in Bushehr in southern Iran.

Methodology. Isolated Candida strains were identified by ITS-PCR-RFLP. Hyphal wall protein 1 (HWP1) was amplified to differentiate C. africana and the resulting sequences were subjected to phylogenetic analyses with a view to identifying similarities and differences in nucleotides.

Results. Ten out of 119 strains originally identified as C. albicans turned out to be C. africana. Pairwise nucleotide alignment of HWP1 DNA sequences showed 100 % similarity between C. africana strains. Inter-species variation between Iranian C. africana HWP1 sequences and the only three available C. africana type sequences in GenBank revealed 99.7–100 % nucleotide similarity. Phylogenetic analysis of the HWP1 DNA sequences of 10 Iranian C. africana isolates, the 3 C. africana sequences available in GenBank and 2 representative Iranian C. albicans sequences revealed that all 11 Iranian C. africana strains formed a well-supported cluster separated from the remaining C. africana.

Conclusion. In our sample, C. africana was only isolated from 7.8 % of the patients with RVVC. While size polymorphisms in HPW1 genes allowed us to differentiate C. africana from C. albicans, no evidence of sequence variation within the Iranian C. africana isolates was observed.

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2018-10-04
2019-10-13
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References

  1. Consolaro ME, Albertoni TA, Svidzinski AE, Peralta RM, Svidzinski TI. Vulvovaginal candidiasis is associated with the production of germ tubes by Candida albicans. Mycopathologia 2005;159:501–507 [CrossRef][PubMed]
    [Google Scholar]
  2. Matheson A, Mazza D. Recurrent vulvovaginal candidiasis: a review of guideline recommendations. Aust N Z J Obstet Gynaecol 2017;57:139–145 [CrossRef][PubMed]
    [Google Scholar]
  3. Blostein F, Levin-Sparenberg E, Wagner J, Foxman B. Recurrent vulvovaginal candidiasis. Ann Epidemiol 2017;27:575.e3–582.e3 [CrossRef][PubMed]
    [Google Scholar]
  4. Hong E, Dixit S, Fidel PL, Bradford J, Fischer G. Vulvovaginal candidiasis as a chronic disease: diagnostic criteria and definition. J Low Genit Tract Dis 2014;18:31–38 [CrossRef][PubMed]
    [Google Scholar]
  5. Giraldo PC, Polpeta NC, Juliato CR, Yoshida LP, do Amaral RL et al. Evaluation of sexual function in Brazilian women with recurrent vulvovaginal candidiasis and localized provoked vulvodynia. J Sex Med 2012;9:805–811 [CrossRef][PubMed]
    [Google Scholar]
  6. Ehrström S, Kornfeld D, Rylander E. Perceived stress in women with recurrent vulvovaginal candidiasis. J Psychosom Obstet Gynaecol 2007;28:169–176 [CrossRef][PubMed]
    [Google Scholar]
  7. Foxman B, Barlow R, D'Arcy H, Gillespie B, Sobel JD. Candida vaginitis: self-reported incidence and associated costs. Sex Transm Dis 2000;27:230–235[PubMed]
    [Google Scholar]
  8. Emmanuel NN, Romeo O, Mebi AG, Scordino F, Bessie EI et al. Lack of Candida bracariensis and Candida nivariensis in vaginal Candida glabrata isolates in Jos, Plateau State. Afr J Microbiol Res 2013;7:4480–4482
    [Google Scholar]
  9. Córdoba S, Vivot W, Bosco-Borgeat ME, Taverna C, Szusz W et al. Species distribution and susceptibility profile of yeasts isolated from blood cultures: results of a multicenter active laboratory-based surveillance study in Argentina. Rev Argent Microbiol 2011;43:176–185 [CrossRef][PubMed]
    [Google Scholar]
  10. Nnadi NE, Ayanbimpe GM, Scordino F, Okolo MO, Enweani IB et al. Isolation and molecular characterization of Candida africana from Jos, Nigeria. Med Mycol 2012;50:765–767 [CrossRef][PubMed]
    [Google Scholar]
  11. Alcoba-Flórez J, Méndez-Alvarez S, Cano J, Guarro J, Pérez-Roth E et al. Phenotypic and molecular characterization of Candida nivariensis sp. nov., a possible new opportunistic fungus. J Clin Microbiol 2005;43:4107–4111 [CrossRef][PubMed]
    [Google Scholar]
  12. Sullivan DJ, Westerneng TJ, Haynes KA, Bennett DE, Coleman DC. Candida dubliniensis sp. nov.: phenotypic and molecular characterization of a novel species associated with oral candidosis in HIV-infected individuals. Microbiology 1995;141:1507–1521 [CrossRef][PubMed]
    [Google Scholar]
  13. Romeo O, Tietz H-J, Criseo G. Candida africana: is it a fungal pathogen?. Curr Fungal Infect Rep 2013;7:192–197 [CrossRef]
    [Google Scholar]
  14. Chowdhary A, Hagen F, Sharma C, Al-Hatmi AMS, Giuffrè L et al. Whole genome-based amplified fragment length polymorphism analysis reveals genetic diversity in Candida africana. Front Microbiol 2017;8: [CrossRef][PubMed]
    [Google Scholar]
  15. Sharma C, Muralidhar S, Xu J, Meis JF, Chowdhary A. Multilocus sequence typing of Candida africana from patients with vulvovaginal candidiasis in New Delhi, India. Mycoses 2014;57:544–552 [CrossRef][PubMed]
    [Google Scholar]
  16. Romeo O, Criseo G. Candida africana and its closest relatives. Mycoses 2011;54:475–486 [CrossRef][PubMed]
    [Google Scholar]
  17. Gumral R, Sancak B, Guzel AB, Saraçlı MA, Ilkit M. Lack of Candida africana and Candida dubliniensis in vaginal Candida albicans isolates in Turkey using HWP1 gene polymorphisms. Mycopathologia 2011;172:73–76 [CrossRef][PubMed]
    [Google Scholar]
  18. Rodríguez-Leguizamón G, Fiori A, López LF, Gómez BL, Parra-Giraldo CM et al. Characterising atypical Candida albicans clinical isolates from six third-level hospitals in Bogotá, Colombia. BMC Microbiol 2015;15:199 [CrossRef][PubMed]
    [Google Scholar]
  19. Ngouana TK, Krasteva D, Drakulovski P, Toghueo RK, Kouanfack C et al. Investigation of minor species Candida africana, Candida stellatoidea and Candida dubliniensis in the Candida albicans complex among Yaoundé (Cameroon) HIV-infected patients. Mycoses 2015;58:33–39 [CrossRef][PubMed]
    [Google Scholar]
  20. Taylor JW, Jacobson DJ, Kroken S, Kasuga T, Geiser DM et al. Phylogenetic species recognition and species concepts in fungi. Fungal Genet Biol 2000;31:21–32 [CrossRef][PubMed]
    [Google Scholar]
  21. Ahmadi B, Mirhendi H, Shidfar MR, Nouripour-Sisakht S, Jalalizand N et al. A comparative study on morphological versus molecular identification of dermatophyte isolates. J Mycol Med 2015;25:29–35 [CrossRef][PubMed]
    [Google Scholar]
  22. Mirhendi H, Makimura K, Khoramizadeh M, Yamaguchi H. A one-enzyme PCR-RFLP assay for identification of six medically important Candida species. Nihon Ishinkin Gakkai Zasshi 2006;47:225–229 [CrossRef][PubMed]
    [Google Scholar]
  23. Romeo O, Criseo G. First molecular method for discriminating between Candida africana, Candida albicans, and Candida dubliniensis by using hwp1 gene. Diagn Microbiol Infect Dis 2008;62:230–233 [CrossRef][PubMed]
    [Google Scholar]
  24. Hall TA. BioEdit: a user-friendly biological sequence alignment editor and analysis program for Windows 95/98/NT. In Nucleic Acids Symposium Series London: Information Retrieval Ltd.; 1999; pp.c1979–c2000
    [Google Scholar]
  25. Wayne P. Clinical and Laboratory Standards Institute. Reference Method for Broth Dilution Antifungal Susceptibility Testing of Yeasts CLSI M27-S4 and Fourth Informational 2012
    [Google Scholar]
  26. Wayne P. Clinical and Laboratory Standards Institute: Reference Method for Broth Dilution Antifungal Susceptibility Testing of Yeasts; Approved Standard CLSI Document M27-A3 and Supplement 2008
    [Google Scholar]
  27. Borman AM, Szekely A, Linton CJ, Palmer MD, Brown P et al. Epidemiology, antifungal susceptibility, and pathogenicity of Candida africana isolates from the United Kingdom. J Clin Microbiol 2013;51:967–972 [CrossRef][PubMed]
    [Google Scholar]
  28. Romeo O, de Leo F, Criseo G. Adherence ability of Candida africana: a comparative study with Candida albicans and Candida dubliniensis. Mycoses 2011;54:e57e61 [CrossRef][PubMed]
    [Google Scholar]
  29. Czaika GKH. Empfindlichkeitsmuster Der Neuen Spezies Candida africana 2004
    [Google Scholar]
  30. Fotedar R, Al-Hedaithy SS. Identification of chlamydospore-negative Candida albicans using CHROMagar Candida medium. Mycoses 2003;46:96–103[PubMed]
    [Google Scholar]
  31. Cross EW, Park S, Perlin DS. Cross-Resistance of clinical isolates of Candida albicans and Candida glabrata to over-the-counter azoles used in the treatment of vaginitis. Microb Drug Resist 2000;6:155–161 [CrossRef][PubMed]
    [Google Scholar]
  32. Ying C, Zhang H, Tang Z, Chen H, Gao J et al. Antifungal susceptibility and molecular typing of 115 Candida albicans isolates obtained from vulvovaginal candidiasis patients in 3 Shanghai maternity hospitals. Med Mycol 2016;54:394–399 [CrossRef][PubMed]
    [Google Scholar]
  33. de Pádua RF, Guilhermetti E, Svidzinski TE. In vitro activity of antifungal agents on yeasts isolated from vaginal secretion. Acta Scientiarum 2003;25:51–54
    [Google Scholar]
  34. Ribeiro MA, Dietze R, Paula CR, da Matta DA, Colombo AL. Susceptibility profile of vaginal yeast isolates from Brazil. Mycopathologia 2001;151:5–10 [CrossRef][PubMed]
    [Google Scholar]
  35. Tietz HJ, Küssner A, Thanos M, de Andrade MP, Presber W et al. Phenotypic and genotypic characterization of unusual vaginal isolates of Candida albicans from Africa. J Clin Microbiol 1995;33:2462–2465[PubMed]
    [Google Scholar]
  36. Mintz JD, Martens MG. Prevalence of non-albicans candida infections in women with recurrent vulvovaginal symptomatology. Adv Infect Dis 2013;3:238
    [Google Scholar]
  37. Hedayati MT, Taheri Z, Galinimoghadam T, Aghili SR, Yazdani Cherati J et al. Isolation of different species of Candida in patients with vulvovaginal candidiasis from Sari, Iran. Jundishapur J Microbiol 2015;8: [CrossRef][PubMed]
    [Google Scholar]
  38. Mohammadi R, Mirhendi H, Rezaei-Matehkolaei A, Ghahri M, Shidfar MR et al. Molecular identification and distribution profile of Candida species isolated from Iranian patients. Med Mycol 2013;51:657–663 [CrossRef][PubMed]
    [Google Scholar]
  39. Seifi Z, Zarei Mahmoudabadi A, Zarrin M. Extracellular enzymes and susceptibility to fluconazole in Candida strains isolated from patients with vaginitis and healthy individuals. Jundishapur J Microbiol 2015;8: [CrossRef][PubMed]
    [Google Scholar]
  40. Mahmoudi Rad M, Zafarghandi S, Abbasabadi B, Tavallaee M. The epidemiology of Candida species associated with vulvovaginal candidiasis in an Iranian patient population. Eur J Obstet Gynecol Reprod Biol 2011;155:199–203 [CrossRef][PubMed]
    [Google Scholar]
  41. Nyirjesy P, Seeney SM, Grody MH, Jordan CA, Buckley HR. Chronic fungal vaginitis: the value of cultures. Am J Obstet Gynecol 1995;173:820–823 [CrossRef][PubMed]
    [Google Scholar]
  42. Chong PP, Lee YL, Tan BC, Ng KP. Genetic relatedness of Candida strains isolated from women with vaginal candidiasis in Malaysia. J Med Microbiol 2003;52:657–666 [CrossRef][PubMed]
    [Google Scholar]
  43. Richter SS, Galask RP, Messer SA, Hollis RJ, Diekema DJ et al. Antifungal susceptibilities of Candida species causing vulvovaginitis and epidemiology of recurrent cases. J Clin Microbiol 2005;43:2155–2162 [CrossRef][PubMed]
    [Google Scholar]
  44. Guzel AB, Ilkit M, Akar T, Burgut R, Demir SC. Evaluation of risk factors in patients with vulvovaginal candidiasis and the value of chromID Candida agar versus CHROMagar Candida for recovery and presumptive identification of vaginal yeast species. Med Mycol 2011;49:16–25 [CrossRef][PubMed]
    [Google Scholar]
  45. Dharwad S, Dominic S. Species identification of Candida isolates in various clinical specimens with their antifungal susceptibility patterns. J Clin Diagn Res 2011;5:1177–1181
    [Google Scholar]
  46. Bankar S, Patil S, Powar R, Kalthur S. Prevalence of non-albican candida infection in Maharashtrian women with leucorrhea. ATMPH 2012;5:119 [CrossRef]
    [Google Scholar]
  47. Moreira D, Auler ME, Ruiz Ldas, Silva Ehda, Hahn RC et al. Species distribution and antifungal susceptibility of yeasts isolated from vaginal mucosa. Revista de Patologia Tropical 2014;43:48–56 [CrossRef]
    [Google Scholar]
  48. Kennedy MA, Sobel JD. Vulvovaginal candidiasis caused by non-albicans Candida species: new insights. Curr Infect Dis Rep 2010;12:465–470 [CrossRef][PubMed]
    [Google Scholar]
  49. Deorukhkar S, Saini S. Vulvovaginal candidiasis due to non albicans Candida: its species distribution and antifungal susceptibility profile. Int J Curr Microbiol App Sci 2013;2:323–328
    [Google Scholar]
  50. Loreto ES, Scheid LA, Nogueira CW, Zeni G, Santurio JM et al. Candida dubliniensis: epidemiology and phenotypic methods for identification. Mycopathologia 2010;169:431–443 [CrossRef][PubMed]
    [Google Scholar]
  51. Babin D, Kotigadde S, Rao PS, Rao T, Babin MD. Clinico-mycological profile of vaginal candidiasis in a tertiary care hospital in Kerala. Int J Res Biol Sci 2013;3:55–59
    [Google Scholar]
  52. Mahmoudabadi AZ, Najafyan M, Alidadi M. Clinical study of Candida vaginitis in Ahvaz, Iran and susceptibility of agents to topical antifungal. Pak J Med Sci 2010;26:607–610
    [Google Scholar]
  53. Ameen F, Moslem M, Al Tami M, Al-Ajlan H, Al-Qahtani N. Identification of Candida species in vaginal flora using conventional and molecular methods. J Mycol Med 2017;27:364–368 [CrossRef][PubMed]
    [Google Scholar]
  54. Ilkit M, Guzel AB. The epidemiology, pathogenesis, and diagnosis of vulvovaginal candidosis: a mycological perspective. Crit Rev Microbiol 2011;37:250–261 [CrossRef][PubMed]
    [Google Scholar]
  55. Wei YP, Feng J, Luo ZC. Isolation and genotyping of vaginal non-albicans Candida spp. in women from two different ethnic groups in Lanzhou, China. Int J Gynaecol Obstet 2010;110:227–230 [CrossRef][PubMed]
    [Google Scholar]
  56. Yazdanparast SA, Khodavaisy S, Fakhim H, Shokohi T, Haghani I et al. Molecular characterization of highly susceptible Candida africana from vulvovaginal candidiasis. Mycopathologia 2015;180:317–323 [CrossRef][PubMed]
    [Google Scholar]
  57. Solimani P, Salari S, khalizadeh S, Hassanzad M, Khodavaisy S et al. Use of PCR-RFLP and PCR-HWP1 for identification of Candida species isolated from cystic fibrosis patients. Res Mol Med 2014;2:23–27 [CrossRef]
    [Google Scholar]
  58. Borman AM, Linton CJ, Miles SJ, Johnson EM. Molecular identification of pathogenic fungi. J Antimicrob Chemother 2008;61:i7–i12 [CrossRef][PubMed]
    [Google Scholar]
  59. Ciardo DE, Schär G, Böttger EC, Altwegg M, Bosshard PP. Internal transcribed spacer sequencing versus biochemical profiling for identification of medically important yeasts. J Clin Microbiol 2006;44:77–84 [CrossRef][PubMed]
    [Google Scholar]
  60. Alonso-Vargas R, Elorduy L, Eraso E, Cano FJ, Guarro J et al. Isolation of Candida africana, probable atypical strains of Candida albicans, from a patient with vaginitis. Med Mycol 2008;46:167–170 [CrossRef][PubMed]
    [Google Scholar]
  61. Sampaio P, Nogueira E, Loureiro AS, Delgado-Silva Y, Correia A et al. Increased number of glutamine repeats in the C-terminal of Candida albicans Rlm1p enhances the resistance to stress agents. Antonie van Leeuwenhoek 2009;96:395–404 [CrossRef][PubMed]
    [Google Scholar]
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