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Influence of cancer treatment on the Candida albicans isolated from the oral cavities of cancer patients

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Abstract

Purpose

Cancer treatment causes mucositis and the manifestation of oral candidiasis. This study investigated the virulence properties and antifungal susceptibilities of Candida albicans isolated from cancer patients undergoing therapy.

Methods

C. albicans were isolated from 49 patients on cancer treatment and 21 healthy individuals and their virulence attributes measured. A correlation was determined between the length of treatment and the fungal counts and their virulence factors.

Results

Although Candida carriage was similar in all the study groups, high quantities of C. albicans and variety of Candida were found in cancer patients. Germ tubes were produced by all the strains. Significantly high number of yeast isolated from radiotherapy and chemotherapy produced large quantities of phospholipase compared to healthy individuals (p < 0.01). The length of chemotherapy was associated with an increase in the phospholipase production (p = 0.03) by the C. albicans. Proteinase production was seen in a significant number of isolates from the radiotherapy group (p < 0.01). Type of cancer treatment had no effect. Resistance to antifungal agents was low.

Conclusions

High quantities of phospholipase were produced by C. albicans in cancer patients on therapy which also increased with the length of chemotherapy suggesting enhanced risk of oral and systemic infection. Therefore, during treatment, prophylactic topical antifungal therapy may be considered.

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References

  1. Bensadoun R-J, Patton LL, Lalla RV, Epstein JB (2011) Oropharyngeal candidiasis in head and neck cancer patients treated with radiation: update. Support Care Cancer 19:737–744

    Article  PubMed  Google Scholar 

  2. Molero G, Diez-Orejas R, Navarro-Garcia F, Monteolivia L, Pla J, Gil C, Sánchez-Pérez M, Nombela C (1998) Candida albicans: genetics, dimorphism and pathogenicity. Int Microbiol 1:95–106

    CAS  PubMed  Google Scholar 

  3. Karskowa-Kuleta, Rapala-Kozik M, Kozik A (2009) Fungi pathogenic to humans: molecular bases of virulence of C. albicans, Cryptococccus neoformans and Aspergillus fumigates. Acta Biochim Pol 56:211–224

    Google Scholar 

  4. Ghannoum MA, Abu-Elteen KH, Motawy MS (1988) Effect of antineoplastic agents and X-irradiation on the adherence of Candida spp. to human buccal epithelial cells in vitro. Mycopathologia 104:171–180

    Article  CAS  PubMed  Google Scholar 

  5. Land GA, Hulme KL, Chaffin WL (1980) The effect of selected antineoplastic agents on the morphology of Candida albicans 5865. Canad J Microbiol 26:812–818

    Article  CAS  Google Scholar 

  6. Moussa NM, Ghannoum MA, Whittaker PA, el-Ezaby MS, Quraman S (1990) Effects of cisplatin and two palladium complexes on Candida albicans. Microbios 62:165–178

    CAS  PubMed  Google Scholar 

  7. Ueta E, Tanida T, Yoneda K, Yamamoto T, Osaki T (2001) Increase of Candida cell virulence by anticancer drugs and irradiation. Oral Microbiol Immunol 16:243–249

    Article  CAS  PubMed  Google Scholar 

  8. Mackenzie DWR (1962) Serum tube identification of Candida albicans. J Clin Pathol 15:563–565

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  9. Patel M, Gulube Z, Dutton M (2009) The effect of Dodonaea viscosa var. angustifolia on C. albicans protein and phospholipase production and adherence to oral epithelial cells. J Ethnopharmacol 124:562–565

    Article  PubMed  Google Scholar 

  10. Ruchel R, Tegeler R, Trost MA (1982) Comparison of secretory proteinase from different strains of Candida albicans. Sabouraudia 20:233–244

    Article  CAS  PubMed  Google Scholar 

  11. Clinical Laboratory Standards Institute M27-A2. (2002). Reference method for broth dilution antifungal susceptibility testing of yeasts, vol 22, No 15.

  12. Pfaller MA, Diekema DJ (2012) Progress in antifungal susceptibility testing of Candida spp. by use of clinical and laboratory standards institute broth microdilution methods, 2010–1012. J Clin Microbiol 50:2846–2856

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  13. Arendrup MC, Cuenca-Estrella M, Donnelly JP, Hope W, Lass-Flörl C, Rodriguez-Tudela J-L (2011) European Committee on antimicrobial susceptibility testing—subcommittee on antifungal susceptibility testing (EUCAST-AFST). EUCAST technical notes on Posaconazole. Clin Microbiol Infect 17:E16–E17

    Article  CAS  PubMed  Google Scholar 

  14. Lass-Flörl C, Arendrup MC, Rodriguez-Tudela J-L, Cuenca-Estrella M, Donnelly JP, Hope W (2011) European Committee on antimicrobial susceptibility testing—subcommittee on antifungal susceptibility testing. EUCAST technical notes on Amphotericin B. Clin Microbiol Infect 17:E27–E29

    Article  PubMed  Google Scholar 

  15. Mañas A, Cerezo L, de la Torre A, García M, Alburquerque H, Ludeña B, Ruiz A, Pérez A, Escribano A, Manso A, Glaria LA, Grupo de Investigación Clinica en Oncologia Radioterápica (GICOR) (2012) Epidemiology and prevalence of oropharyngeal candidiasis in Spanish patients with head and neck tumors undergoing radiotherapy treatment alone or in combination with chemotherapy. Clin Transl Oncol 14:740–746

    Article  PubMed  Google Scholar 

  16. Redding SW, Zellars RC, Kirkpatrick WR, McAfee RK, Caceres MA, Fothergill AW, Lopez-Ribot JL, Bailey CW, Rinaldi MG, Patterson TF (1999) Epidemiology of oropharyngeal Candida colonization and infection in patients receiving radiation for head and neck cancer. J Clin Microbiol 37:3896–3900

    CAS  PubMed  PubMed Central  Google Scholar 

  17. Al Abeid HM, Abu-Elleen KM, Elkarmi AZ, Hamad MA (2004) Isolation and characterization of Candida spp in Jordanian cancer patients: prevalence, pathogenic determinants and antifungal sensitivity. Jpn J Infect Dis 57:279–284

    PubMed  Google Scholar 

  18. Schelenz S, Abdallah S, Gray G, Stubbings H, Gow I, Baker P, Hunter PR (2011) Epidemiology of oral yeast colonization and infection in patients with hematological malignancies, head and neck solid tumors. J Oral Pathol Med 40:83–89

    Article  PubMed  Google Scholar 

  19. Suryawanshi H, Ganvir SM, Hazrey VK, Wanjare VS (2012) Oropharyngeal candidosis relative frequency in radiotherapy patients for head and neck cancer. J Oral Maxillofac Pathol 16:31–37

    Article  PubMed  PubMed Central  Google Scholar 

  20. Ramirez-Amador V, Silverman S, Mayer P, Tyler M, Quivey J (1997) Candidal colonization and oral candidiasis in patients undergoing oral and pharyngeal radiation therapy. Oral Surg Oral Med Oral Pathol Oral Radiol Endod 84:149–153

    Article  CAS  PubMed  Google Scholar 

  21. Stokman MA, Spijkervet FK, Boezen HM, Schouten JP, Roodenburg JL, de Vries EG (2006) Preventative intervention possibilities in radiotherapy- and chemotherapy-induced oral mucositis: results of meta-analyses. J Dent Res 85:690–700

    Article  CAS  PubMed  Google Scholar 

  22. Ferretti GA, Raybould TP, Brown AT, Macdonald JS, Greenwood M, Maruyama Y, Geil J, Lillich TT, Ash RC (1990) Chlorhexidine prophylaxis for chemotherapy- and radiotherapy-induced stomatitis: a randomized double-blinded trial. Oral Surg Oral Med Oral Pathol 69:331–338

    Article  CAS  PubMed  Google Scholar 

  23. Spijkervet FK, van Saene HK, Panders AK, Vermey A, van Saene JJ, Mehta DM, Fidler V (1991) Effect of chlorhexidine rinsing on the oropharyngeal ecology in patients with head and neck cancer who have irradiation mucositis. Oral Surg Oral Med Oral Pathol 67:154–161

    Article  Google Scholar 

  24. Safdar A, Chaturvedi V, Cross EW, Park S, Bernard EM, Armstrong D, Perlin DS (2001) Prospective study of Candida species in patients at a comprehensive cancer center. Antimicrob Agents Chemother 45:2129–2133

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  25. Liu Y, Shetty AC, Schwartz JA, Bradford LL, Xu W, Phan QT, Kumar P, Mahurkar A, Mitchell AP, Ravel J, Fraser CM, Filler SG, Bruno VM. (2015). New signalling pathways govern the host response to C. albicans infection in various niche. Genome Res.

  26. Wagener J, Mailänder-Sanchez D, Schaller M (2012) Immune responses to Candida albicans in models of in vitro reconstituted human oral epithelium. Methods Mol Biol 845:333–344

    Article  CAS  PubMed  Google Scholar 

  27. Kong EF, Kuchariková S, Van Dijck P, Peters BM, Shirtliff ME, Jabra-Rizk MA (2015) Clinical implications of oral candidiasis: host tissue damage and disseminated bacterial disease. Infect Immun 83:604–613

    Article  PubMed  PubMed Central  Google Scholar 

  28. Gow NA (1997) Germ Tube growth of Candida albicans. Curr Top Med Mycol 8:43–55

    CAS  PubMed  Google Scholar 

  29. Naglik JR, Challacombe SJ, Hube B (2003) Candida albicans secreted aspartyl proteinases in virulence and pathogenesis. Microbiol Mol Biol Rev 67:400–428

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  30. Pemán J, Zaragoza R, Quindós G, Alkorta M, Cuétara MS, Camarena JJ, Ramirez P, Gimennez MJ, Martin-Mazuelos E, Linares-Sicilia MJ, Ponton J, study group (2011) Candida albicans germ tube antibody detection in critically ill patients. Clinical factors associated with a Candida albicans germ tube antibody positive test in intensive care unit patients. BMC Infect Dis 11:60. doi:10.1186/1471-2334-11-60

    Article  PubMed  PubMed Central  Google Scholar 

  31. Kothavade RJ, Panthaki MH (1998) Evaluation of phospholipase activity of Candida albicans and its correlation with pathogenicity in mice. J Med Microbiol 47:99–102

    Article  CAS  PubMed  Google Scholar 

  32. Ibrahim AS, Mirbod F, Filler SG, Banno Y, Cole GT, Kitajima Y, Edwards JE Jr, Nozawa Y, Ghannoum MA (1995) Evidence implicating phospholipase as a virulence factor of Candida albicans. Infect Immun 63:1993–1998

    CAS  PubMed  PubMed Central  Google Scholar 

  33. Ghannoum MA (2000) Potential role of phospholipases in virulence and fungal pathogenesis. Clin Microbiol Rev 13:122–143

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  34. Mukherjee PK, Chandra J, Kuhn DM, Ghannoum MA (2003) Differential expression of Candida albicans phospholipase B (PLB1) under various environmental and physiological conditions. Microbiol 149:261–267

    Article  CAS  Google Scholar 

  35. Kumar CP, Kumar SS, Menon T (2006) Phospholipase and proteinase activities of clinical isolates of Candida from immunocompromised patients. Mycopathologia 161:213–218

    Article  CAS  PubMed  Google Scholar 

  36. Kuriyama T, Williams DW, Lewis MA (2003) In vitro secreted aspartyl proteinase activity of Candida albicans isolated from oral diseases and healthy oral cavities. Oral Microbiol Immunol 18:405–407

    Article  CAS  PubMed  Google Scholar 

  37. Owotade FJ, Patel M (2014) Virulence of oral Candida isolated from HIV positive women with oral candidiasis and asymptomatic carriers. Oral Surg Oral Med Oral Pathol Oral Radiol Endod 118:445–460

    Google Scholar 

  38. Yu DT, Seger, DL, Peterson JF, Kumar RN, Bates DW. (2006). Fluconazole for empiric antifungal therapy in cancer patients with fever and neutropenia. BMC Infect Dis 6:173 or Published online 2006 December 5. doi: 10.1186/1471-2334-6-173.

  39. Hachem R, Hanna H, Kontoyiannis D, Jiang Y, Raad I (2008) The changing epidemiology of invasive candidiasis: Candida glabrata and Candida krusei in hematologic malignancy. Cancer 112:2493–2499

    Article  PubMed  Google Scholar 

  40. Lopez-Ribot JL, McAfee RK, Perea S, Kirkpatrick WR, Rinaldi MG, Patterson TF (1999) Multiple resistant phenotypes of C. albicans coexist during episodes of oropharyngeal candidiasis in HIV-infected patients. Antimicrob Agents Chemother 43:1621–1630

    CAS  PubMed  PubMed Central  Google Scholar 

  41. Lalla RV, Latortue MC, Hong CH, Ariyawardana A, D’ Amato-Palumbo S, Fischer DJ, Martof A, Nicolatou-Galitis O, Patton LL, Elting LS, Spikeryet FK, Brennan MT, Fungal Infections Section, Oral Care study Group. Multinational Association of Supportive Care Cancer (MASCC)/International Society of Oral Oncology (ISOO) (2010) A systematic review of oral fungal infections in patients receiving cancer therapy. Support Care Cancer 18:985–992

    Article  PubMed  PubMed Central  Google Scholar 

  42. Jham BC, Franca EC, Oliveira RR, Santos VR, Kowalski LP, da Silva Freire AR (2007) Candida oral colonization and infection in Brazilian patients undergoing head and neck radiotherapy: a pilot study. Oral Surg Oral Med Oral Pathol Oral Radiol Endod 103:355–358

    Article  PubMed  Google Scholar 

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Acknowledgements

We wish to thank Prof F. Owotade for the statistical guidance. We also thank the Faculty Research Committee, Faculty of Health Sciences, and University of The Witwatersrand for the financial support.

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Authors and Affiliations

  1. Division of Oral Microbiology, Department of Oral Biological Sciences, School of Oral Health Sciences, Faculty of Health Sciences, University of The Witwatersrand, 7 York Road, Parktown, Johannesburg, 2050, South Africa

    Shilpa Ramla & Mrudula Patel

  2. Radiation Oncology, Charlotte Maxeke Johannesburg Academic Hospital, Faculty of Health Sciences, University of the Witwatersrand, Johannesburg, South Africa

    Vinay Sharma

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  1. Shilpa Ramla
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Correspondence to Mrudula Patel.

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Relevance

High quantities of phospholipase produced by C. albicans in cancer patients on therapy indicate enhanced risk of oral and systemic infection and therefore, during treatment prophylactic topical antifungal therapy may be considered.

Conflict of interest

The authors declare that they have no competing interests.

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Ramla, S., Sharma, V. & Patel, M. Influence of cancer treatment on the Candida albicans isolated from the oral cavities of cancer patients. Support Care Cancer 24, 2429–2436 (2016). https://doi.org/10.1007/s00520-015-3035-8

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  • DOI: https://doi.org/10.1007/s00520-015-3035-8

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