Identification of Candida spp. isolated from oral mucosa in patients with leukemias and lymphomas in Iran

  • Sara Sara Hamzehee Student Research Committee, Department of Parasitology and Mycology, School of Medicine, Kerman University of Medical Sciences, Kerman, Iran
  • Davood Kalantar-Neyestanaki Department of Microbiology and Virology, School of Medicine, Kerman University of Medical Sciences, Kerman, Iran
  • Mohammad Ali Mohammadi Research Center for Hydatid Disease in Iran, Kerman University of Medical Sciences, Kerman, Iran
  • Saeed Nasibi Research Center for Hydatid Disease in Iran, Kerman University of Medical Sciences, Kerman, Iran
  • Seyed Amin Ayatollahi Mousavi Department of Medical Mycology and Parasitology, School of Medicine, Kerman University of Medical Sciences, Kerman, Iran
Keywords: Candida spp, Oral candidiasis, Hematologic malignancies, Lymphomas


Background and Objectives: Oral candidiasis is a serious problem for immunocompromised patients, especially patients with hematological malignancies. After becoming a systemic candidiasis it is difficult to diagnose, control and treat in individuals with hematological malignancies. The aim of this study was to diagnose candidiasis in the oral mucosa of patients with leukemias and lymphomas in a timely manner in order to prevent their progression to systemic candidiasis.

Materials and Methods: In this cross sectional study, 50 clinical samples were collected from the mouth of patients with hematological malignancies undergoing chemotherapy from the oncology units of teaching hospitals in Kerman, Iran. Patients were from Kerman, Sistan-Baluchestan and Hormozgan in south-eastern Iran. Sampling was restricted to patients with diagnosed acute lymphoid leukemia (ALL); acute myeloid leukemia (AML); chronic lymphoid leukemia (CLL); chronic myeloid leukemia (CML); Hodgkin’s lymphoma (HL) and non-Hodgkin’s lymphoma (NHL). Presumptive species identification of fungi was performed using conventional methods like colony characteristics on CHROMagar Candida medium, germ tube production, and assessing the morphology fungi on corn meal agar. Confirmation of presumptive candida isolates was performed using PCR-RFLP.

Results: From a total of 50, 14 patients (28%) had positive oral candidiasis. Candida albicans (57.14%) was the most common species followed by Candida glabrata (14.28%), Candida parapsilosis (14.28%), Candida krusei (7.14%) and Candida kefyr (7.14%). Candida albicans had the highest rate of oral infection in ALL (35.71%) and then NHL (28.57%) patients.

Conclusion: The results indicate that oral candidiasis is a prevalent fungal infection in the patients with hematologic malignancies with C. albicans being the main etiological agent. However, other species of Candida cause similar infections in these patients.


1. Sharifynia S, Falahati M, Akhlaghi L, Foroumadi A, Fateh R. Molecular identification and antifungal susceptibility profile of Candida species isolated from patients with vulvovaginitis in Tehran, Iran. J Res Med Sci 2017; 22: 132.
2. Franco MP, Green JS, Young J-AH. Evaluation and management of bacterial and fungal infections in patients with a hematological malignancy: A 2018 update. Neoplastic Diseases of the Blood 2018: 1063-1078.
3. Guo F, Yang Y, Kang Y, Zang B, Cui W, Qin B, et al. Invasive candidiasis in intensive care units in China: a multicentre prospective observational study. J Antimicrob Chemother 2013; 68: 1660-1668.
4. Gonzalez Gravina H, Gonzalez de Moran E, Zambrano O, Lozano Chourio M, Rodriguez de Valero S, Robertis S, et al. Oral Candidiasis in children and adolescents with cancer: Identification of Candida spp. Med Oral Patol Oral Cir Bucal 2007; 12: E419-423.
5. Hajjeh RA, Sofair AN, Harrison LH, Lyon GM, Arthington-Skaggs BA, Mirza SA, et al. Incidence of bloodstream infections due to Candida species and in vitro susceptibilities of isolates collected from 1998 to 2000 in a population-based active surveillance program. J Clin Microbiol 2004; 42: 1519-1527.
6. Marr KA, Carter RA, Crippa F, Wald A, Corey L. Epidemiology and outcome of mould infections in hematopoietic stem cell transplant recipients. Clin Infect Dis 2002; 34: 909-917.
7. Marr KA, Seidel K, White TC, Bowden RA. Candidemia in allogeneic blood and marrow transplant recipients: evolution of risk factors after the adoption of prophylactic fluconazole. J Infect Dis 2000; 181: 309-316.
8. Martino R, Lopez R, Sureda A, Brunet S, Domingo-Albos A. Risk of reactivation of a recent invasive fungal infection in patients with hematological malignancies undergoing further intensive chemo-radiotherapy. A single-center experience and review of the literature. Haematologica 1997; 82: 297-304.
9. Muhlemann K, Wenger C, Zenhausern R, Tauber MG. Risk factors for invasive aspergillosis in neutropenic patients with hematologic malignancies. Leukemia 2005; 19: 545-550.
10. Nucci M, Spector N, Bueno AP, Solza C, Perecmanis T, Bacha PC, et al. Risk factors and attributable mortality associated with superinfections in neutropenic patients with cancer. Clin Infect Dis 1997; 24: 575-579.
11. Pagano L, Girmenia C, Mele L, Ricci P, Tosti ME, Nosari A, et al. Infections caused by filamentous fungi in patients with hematologic malignancies. A report of 391 cases by GIMEMA infection program. Haematologica 2001; 86: 862-870.
12. Schelenz S, Abdallah S, Gray G, Stubbings H, Gow I, Baker P, et al. Epidemiology of oral yeast colonization and infection in patients with hematological malignancies, head neck and solid tumors. J Oral Pathol Med 2011; 40: 83-89.
13. Badiee P, Kordbacheh P, Alborzi A, Zakernia M, Haddadi P. Early detection of systemic candidiasis in the whole blood of patients with hematologic malignancies. Jpn J Infect Dis 2009; 62: 1-5‏.
14. 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.
15. Chen Y-K, Hou H-A, Chow J-M, Chen Y-C, Hsueh P-R, Tien H-F. The impact of oral herpes simplex virus infection and candidiasis on chemotherapy-induced oral mucositis among patients with hematological malignancies. Eur J Clin Microbiol Infect Dis 2011; 30: 753-759.
16. Epstein JB, Beier Jensen S. Management of hyposalivation and xerostomia: criteria for treatment strategies. Compend Contin Educ Dent 2015; 36: 600-603.
17. Shimada Y, Nakagawa Y, Ide K, Sato I, Hagiwara S, Yamada H, et al. Importance of eliminating potential dental focal infection before the first cycle of chemotherapy in patients with hematologic malignancy. Support Care Cancer 2017; 25: 1379-1381.
18. Telles DR, Karki N, Marshall MW. Oral fungal infections: diagnosis and management. Dent Clin North Am 2017; 61: 319-349.
19. Haron E, Feld R, Tuffnell P, Patterson B, Hasselback R, Matlow A. Hepatic candidiasis: an increasing problem in immunocompromised patients. Am J Med 1987; 83: 17-26.
20. Thaler M, Pastakia B, Shawker TH, Oleary T, Pizzo PA. Hepatic candidiasis in cancer patients: the evolving picture of the syndrome. Ann Intern Med 1988; 108: 88-100.
21. Shokri H, Khosravi AR, Yalfani R. Antifungal efficacy of propolis against fluconazole-resistant Candida glabrata isolates obtained from women with recurrent vulvovaginal candidiasis. Int J Gynaecol Obstet 2011; 114: 158-159‏.
22. Aghadavoudi F, Chabavizadeh J, Dehghan P, Moafi A. The frequency of oral candidiasis in children and adolescents with Leukemia in Isfahan province, Iran‏. JIMS 2017; 35: 151-156.
23. Dahiya MC, Redding SW, Dahiya RS, Eng TY, Kirkpatrick WR, Coco BJ, et al. Oropharyngeal candidiasis caused by non-albicans yeast in patients receiving external beam radiotherapy for head-and-neck cancer. Int J Radiat Oncol Biol Phys 2003; 57: 79-83.
24. Kumar CPG, Sundararajan T, Menon T, Venkatadesikalu M. Candidosis in children with onco-hematological diseases in Chennai, south India. Jpn J Infect Dis 2005; 58: 218-221.
25. Tekeli A, Dolapci I, Cesur S, Tekeli E, Icli F. [Candida dubliniensis studies and isolation of Candida types in oropharyngeal specimens from oncologic patients].Mikrobiyol Bul 2002; 36: 57-63.
26. Bashir H, Ahmad J. Oral Candida colonization and infection in cancer patients and their antifungal susceptibility in a tertiary care hospital. Int J Adv Res 2014; 2: 541-550.
27. Maheronnaghsh M, Tolouei S, Dehghan P, Chadeganipour M, Yazdi M. Identification of Candida species in patients with oral lesion undergoing chemotherapy along with minimum inhibitory concentration to fluconazole. Adv Biomed Res 2016; 5: 132.
28. Shokohi T, Aslani N, Ahangarkani F, Meyabadi MF, Hagen F, Meis JF, et al. Candida infanticola and Candida spencermartinsiae yeasts: Possible emerging species in cancer patients. Microb Pathog 2018; 115: 353-357.
29. Marodi L, Johnston Jr RB. Invasive Candida species disease in infants and children: occurrence, risk factors, management, and innate host defense mechanisms. Curr Opin Pediatr 2007; 19: 693-697.
30. de Morales Rojas T, Zambrano O, Rivera L, Navas R, Chaparro N, Bernardonni C, et al. Oral-disease prevention in children with cancer: testing preventive protocol effectiveness. Med Oral 2001; 6: 326-334.
31. Sepulveda E, Brethauer U, Morales R, Jimenez M. Oral manifestations in pediatric patients wíth oncologic pathologic. Med Oral 2000; 5: 193-197.
How to Cite
Sara Hamzehee S, Kalantar-Neyestanaki D, Mohammadi MA, Nasibi S, Ayatollahi Mousavi SA. Identification of Candida spp. isolated from oral mucosa in patients with leukemias and lymphomas in Iran. Iran J Microbiol. 11(2):114-119.
Original Article(s)