Characterization of Candida species isolated from vulvovaginal candidiasis by MALDI-TOF with in vitro antifungal susceptibility profiles

Document Type : Original Articles

Authors

1 Infectious and Tropical Diseases Research Centre, Tabriz University of Medical Sciences, Tabriz, Iran

2 Department of Obstetrics and Gynecology, School of Medicine, Fasa University of Medical Sciences, Fasa, Iran

3 Department of Medical Mycology and Parasitology, School of Medicine, Fasa University of Medical Sciences, Fasa, Iran

4 Department of Microbiology, Zanjan Branch, Islamic Azad University, Zanjan, Iran

5 Department of Pathobiology, Science and Research Branch, Islamic Azad University, Tehran, Iran

6 HIV/AIDS Research Center, Fasa University of Medical Sciences, Fasa, Iran

10.18502/cmm.7.4.8405

Abstract

Background and Purpose: Vulvovaginal candidiasis (VVC) is an opportunistic
infection due to Candida species, one of the most common genital tract diseases among reproductive-age women. The present study aimed to investigate the prevalence of VVC among non-pregnant women and identify the epidemiology of the involved Candida species with the evaluation of antifungal susceptibilities.
Materials and Methods: Matrix-assisted laser desorption/ionization time-of-flight mass spectrometry (MALDI-TOF MS) was performed to identify Candida species isolated from the genital tract of 350 non-pregnant women. Moreover, antifungal susceptibility testing was performed according to the Clinical and Laboratory Standards Institute broth microdilution method guidelines (M27-A3 and M27-S4).
Results: Vaginal swab cultures of 119 (34%) women yielded Candida species. Candida
albicans was the most frequently isolated species (68%), followed by Candida glabrata
(19.2%). Voriconazole was the most active drug against all tested isolates showing an
MIC50/MIC90 corresponding to 0.016/0.25 µg/mL, followed by posaconazole (0.031/1
µg/mL). Overall, resistance rates to fluconazole, itraconazole, and voriconazole were
2.4%, 4.8% and, 0.8% respectively. However, posaconazole showed potent in vitro activity against all tested isolates.
Conclusion: Results of the current study showed that for the effectual therapeutic
outcome of candidiasis, accurate identification of species, appropriate source control,
suitable antifungal regimens, and improved antifungal stewardship are highly recommended for the management and treatment of infection with Candida, like VVC.
 

Keywords


 1. Ahmad A, Khan AU. Prevalence of Candida species and
potential risk factors for vulvovaginal candidiasis in Aligarh,
India. Eur J Obstet Gynecol Reprod Biol. 2009; 144(1):68-71.
2. 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(3):364-8.
3. Mushi MF, Mmole A, Mshana SE.
Candida vaginitis among
symptomatic pregnant women attending antenatal clinics in
Mwanza, Tanzania. BMC Res Notes. 2019 27; 12(1):1-5.
4. Bitew A, Abebaw Y. Vulvovaginal candidiasis: species
distribution of
Candida and their antifungal susceptibility
pattern. BMC Womens Health. 2018; 18(1):1-10.
5. Donders GG, Vereecken A, Bosmans E, Dekeersmaecker A,
Salembier G, Spitz B. Definition of a type of abnormal vaginal
flora that is distinct from bacterial vaginosis: aerobic vaginitis.
BJOG. 2002; 109(1):34-43.
6. Maraki S, Mavromanolaki VE, Stafylaki D, Nioti E, Hamilos G,
Kasimati A. Epidemiology and antifungal susceptibility patterns
of
Candida isolates from Greek women with vulvovaginal
candidiasis. Mycoses. 2019; 62(8):692-7.
7. Brandao LDS, Boniek D, Resende Stoianoff MA, da Mata FMR,
de Azevedo PRM, Fernandes JV, et al. Prevalence and
antifungal susceptibility of
Candida species among pregnant
women attending a school maternity at Natal, Brazil. Lett Appl
Microbiol. 2018; 67(3):285-91.
8. Fazeli A, Kordbacheh P, Nazari A, Daie Ghazvini R, Mirhendi
H, Safara M, et al. Candiduria in Hospitalized Patients and
Identification of Isolated
Candida Species by Morphological and
Molecular Methods in Ilam, Iran. Iran J Public Health. 2019;
48(1):156-61.
9. Bader O, Weig M, Taverne-Ghadwal L, Lugert R, Gross U,
Kuhns M. Improved clinical laboratory identification of human
pathogenic yeasts by matrix-assisted laser desorption ionization
time-of-flight mass spectrometry. Clin Microbiol Infect. 2011;
17(9):1359-65.
10. Marklein G, Josten M, Klanke U, Muller E, Horre R, Maier T, et
al. Matrix-assisted laser desorption ionization-time of flight
mass spectrometry for fast and reliable identification of clinical
yeast isolates. J Clin Microbiol. 2009; 47(9):2912-7.
11. Shokohi T, Badram L, Badali H, Ataollahi MR, Afsarian MH.
Molecular Identification of Clinically Common and Uncommon
Yeast Species. Jundishapur J Microbiol. 2018; 11(10):e66240.
12. 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(2):230-3.
13. Reference Method for Broth Dlution Antifungal Susceptibility
Testing of yeasts. Approved Standard M27-A3, 3rd ed. Wayne,
PA: Clinical and Laboratory Standards Institute. 2008.
14. Clinical and Laboratory Standards Institute (CLSI). Reference
method for broth dilution antifungal susceptibility testing of
yeasts: fourth informational supplement M27-S4. Wayne: CLSI.
2012.
15. Arastehfar A, Fang W, Al-Hatmi AMS, Afsarian MH,
Daneshnia F, Bakhtiari M, et al. Unequivocal identification of an
underestimated opportunistic yeast species, Cyberlindnera
fabianii, and its close relatives using a dual-function PCR and
literature review of published cases. Med Mycol. 2019;
57(7):833-40.
16. Ghajari A, Ahmadi NA, Nazer Fassihi P, Shahmohammadi N,
Ansari S, Norouzi M, Arab-Mazar Z, et al. Isolation of Different
Species of
Candida in Patients with Vulvovaginal Candidiasis
from Damavand, Iran. Arch Clin Infect Dis. 2018;
13(6):e59291.
17. Roshan R, Badali H. Identification of
Candida species isolated
from vulvovaginal candidiasis using PCR-RFLP. Int J Mol Clin
Microbiol.2018; 11(8):e65359.
18. Lakshmi PM. Isolation and Speciation of
Candida from
Vaginitis Cases attending Gynaecology OPD in a Tertiary Care
Hospital A.P. India. Int J Curr Microbiol Appl Sci. 2016;
5(10):229-232.
19. Hedayati MT, Tahery Z, Galinimoghadam T, Aghili SR,
Yazdani J, Mosayebi E,et al. Isolation of Different Species of
Candida in Patients With Vulvovaginal Candidiasis From Sari,
Iran. Jundishapur J Microbiol. 2015; 8(4):e15992.
20. Roudbary M, Bakhshi B, Farhadi Z, Nikoomanesh F.
  Identification of Candida species isolated from Iranian women
with vaginal candidiasis by PCR-RFLP method Eur J Exp Biol.
2013; 3(6):365-9.
21. Hasanvand S, Kord M, Didehdar M. Molecular Epidemiology
and In Vitro Antifungal Susceptibility of
Candida Isolates from
Women with Vulvovaginal Candidiasis in Northern Cities of
Khuzestan Province, Iran. Jundishapur J Microbiol. 2017;
10(8):e12804.
22. Pouladian S, Mohammadi R. Clinical and Mycological Study of
Vulvovaginal Candidiasis (VVC); Identification of Clinical
Isolates by Polymerase Chain Reaction-Fragment Size
Polymorphyim (PCR-FSP) Technique. Arch Clin Infect Dis.
2017; 12(2):e62761.
23. Kengne M, Shu SV, Nwobegahay JM, Achonduh O. Antifungals
susceptibility pattern of
Candida spp. isolated from female
genital tract at the Yaounde Bethesda Hospital in Cameroon. Pan
Afr Med J. 2017; 28:294 .
24. Luo X, Dong X, Pen Z. Distribution and Drug Susceptibility of
Candida spp. Associated With Female Genital Tract Infection,
Chongqing, China. Jundishapur J Microbiol. 2016; 9(10):
e19386.
25. Rezaei-Matehkolaei A, Zarei-Mahmoudabadi A. Isolation,
Molecular Identification, and Antifungal Susceptibility Profiles
of Vaginal Isolates of
Candida Species. Iran J Microbiol. 2016;
8(6):410-7.
26. Lopes PHS, Pacini VL, Norberg AN. Genital infection by
gardnerella vaginalis and
Candida spp. Among women in Nova
Iguacu city, Rio de Janeiro Province, Brazil. OALib Journal.
2017; 4(3):1-7.
27. Hashemi SE, Shokohi T, Abastabar M, Aslani N, Ghadamzadeh
M, Haghani I. Species distribution and susceptibility profiles of
Candida species isolated from vulvovaginal candidiasis,
emergence of C. lusitaniae. Curr Med Mycol. 2019; 5(4):26-34.
28. Esim Buyukbayrak E, Kars B, Karsidag AY, Karadeniz BI,
Kaymaz O, Gencer S, et al. Diagnosis of vulvovaginitis:
comparison of clinical and microbiological diagnosis. Arch
Gynecol Obstet. 2010; 282(5):515-9.
29. Bonyadpour B, Mohagheghzadeh A. A Descriptive Study on the
Prevalence of Vulvovaginal Infections and Species-specific
Distribution of Vulvovaginal Candidiasis in Married Women of
the South of Iran. J Midwifery Reprod Health. 2016; 4(4):741-7.
30. Gharaghani M, Taheripour Sisakht M, Ilami O, Aramesh S,
Mouhamadi F, Barati Z, et al. Identification of
Candida Species
Isolated from Vulvovaginal Candidiasis Patients by Polymerase
Chain Reaction-Restriction Fragment Length Polymorphism
(PCR-RFLP) in Yasuj Southwestern Iran. Jundishapur J
Microbiol. 2018; 11(8):e65359.
31. 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(2):199-203.
32. Olanrewaju Jimoh HII, Sabo E, Yakubu Steve J, Ankuma
Adebola T Olayinka. Prevalence and Speciation of Non-albican
Vulvovaginal Candidiasis in Zaria. J Nat Sci Res. 2016; 6:51–6.
33. Haleim E, Sayed A, Ismail DK, Sayed AM, Abdella A. Provence
of non albicans species associated with vulvovaginal candidiasis
in Egyptian women. Int j adv health sci. 2015; 12:304-13.
34. 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 J Pathol Microbiol. 2013; 56(2):144-7.
35. Alizadeh M, Kolecka A, Boekhout T, Zarrinfar H, Ghanbari
Nahzag MA, Badiee P, et al. Identification of
Candida species
isolated from vulvovaginitis using matrix assisted laser
desorption ionization-time of flight mass spectrometry. Curr
Med Mycol. 2017; 3(4):21-5.
36. Abbasi Z, Nejat SF, Falahati M, Ashrafi Khozani M, Hosseini F,
Faiazy A, et al. Molecular Identification and Antifungal
Susceptibility Pattern of Non-albicans
Candida Species Isolated
from Vulvovaginal Candidiasis. Iran Biomed J. 2018; 22(1):33-41.
37. Theill L, Dudiuk C, Morano S, Gamarra S, Nardin ME, Mendez
E, et al. 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. Rev Argent Microbiol. 2016; 48(1):43-9.
38. Khadka S, Sherchand JB, Pokhrel BM, Parajuli K, Mishra SK,
Sharma S, et al. Isolation, speciation and antifungal
susceptibility testing of
Candida isolates from various clinical
specimens at a tertiary care hospital, Nepal. BMC Res Notes.
2017; 10(1):218.
39. Taei M, Chadeganipour M, Mohammadi R. An alarming rise of
non-albicans
Candida species and uncommon yeasts in the
clinical samples; a combination of various molecular techniques
for identification of etiologic agents. BMC Res Notes. 2019;
12(1):1-7.
40. Afsarian SM, Badali H, Shokohi T, Najafipour S. Molecular
Diversity of
Candida albicans Isolated from Immunocompromised Patients, Based on MLST Method. Iran J Public
Health. 2015; 44(9):1262-9.
41. Aslani N, Janbabaei G, Abastabar M, Meis JF, Babaeian M,
Khodavaisy S, et al. Identification of uncommon oral yeasts
from cancer patients by MALDI-TOF mass spectrometry. BMC
Infect Dis. 2018; 18(1):1-11.
42. Tamai IA, Pakbin B, Fasaei BN. Genetic diversity and
antifungal susceptibility of
Candida albicans isolates from
Iranian HIV-infected patients with oral candidiasis. BMC Res
Notes. 2021; 14(1):1-7.
43. Shokohi T, Badali H, Amirrajab N, Ataollahi MR, Kouhpayeh
SA, Afsarian MH, et al. In vitro activity of five antifungal agents
against
Candida albicans isolates, Sari, Iran. Curr Med Mycol.
2016; 2(2):34-9.
44. Amirrajab N, Badali H, Didehdar M, Afsarian MH,
Mohammadi R, Lotfi N, Shokohi T, et al. In Vitro Activities of
Six Antifungal Drugs Against
Candida glabrata Isolates:
An Emerging Pathogen. Jundishapur J Microbiol. 2016;
9(5):e36638.
45. Aslani N, Shokohi T, Ataollahi MR, Ansari S, Gholampour Y,
Khani Jeihooni A, et al. In vitro activity of four triazole
antifungal drugs against clinically common and uncommon yeast
species. Curr Med Mycol. 2019; 5(4):14-9.
46. Adjapong G, Hale M, Garrill A. A comparative investigation of
azole susceptibility in
Candida isolates from vulvovaginal
candidiasis and recurrent vulvovaginal candidiasis patients in
Ghana. Med Mycol. 2017; 55(6):686-9.
47. Khan M, Ahmed J, Gul A, Ikram A, Lalani FK. Antifungal
susceptibility testing of vulvovaginal
Candida species among
women attending antenatal clinic in tertiary care hospitals of
Peshawar. Infect Drug Resist. 2018; 11:447-56.
 
Volume 7, Issue 4
December 2021
Pages 6-11
  • Receive Date: 16 August 2021
  • Revise Date: 21 November 2021
  • Accept Date: 28 November 2021
  • First Publish Date: 30 November 2021
  • Publish Date: 01 December 2021