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Yeast Oropharyngeal Colonization in Human Immunodeficiency Virus-Infected Patients in Central Taiwan

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Abstract

A prospective, cross-sectional study was conducted at a medical center in central Taiwan to understand the prevalence, associated factors, and microbiologic features for oropharyngeal yeast colonization in human immunodeficiency virus-infected outpatients. Oral yeast colonization was detected in 127 (45 %) patients, including 21 (16.5 %) colonized by more than one species. Of the 154 isolates, Candida albicans was the most common species (114, 74 %), followed by Candida dubliniensis (10, 6.5 %), Candida glabrata (10, 6.5 %), Candida tropicalis (7, 4.5 %), and 13 others. We found that receiving antituberculous drug (p = 0.046) or atazanavir (p = 0.045) was two predictors for patients colonized by non-C. albicans species (p = 0.005) and risking mixed yeast colonization (p = 0.009). Even though our data showed that clinical antifungal drugs remained effective in vitro against the colonizing yeasts, the increased mixed yeast colonization indicates a potential issue for controlling mixed infections in hospital settings.

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References

  1. Samaranayake LP. Oral mycoses in HIV infection. Oral Surg Oral Med Oral Pathol. 1992;73:171–80.

    Article  CAS  PubMed  Google Scholar 

  2. Sangeorzan JA, Bradley SF, He X, Zarins LT, Ridenour GL, Tiballi RN, et al. Epidemiology of oral candidiasis in HIV-infected patients: colonization, infection, treatment, and emergence of fluconazole resistance. Am J Med. 1994;97:339–46.

    Article  CAS  PubMed  Google Scholar 

  3. Costa CR, de Lemos JA, Passos XS, de Araujo CR, Cohen AJ, Souza LK, et al. Species distribution and antifungal susceptibility profile of oral candida isolates from HIV-infected patients in the antiretroviral therapy era. Mycopathologia. 2006;162:45–50.

    Article  CAS  PubMed  Google Scholar 

  4. Traeder C, Kowoll S, Arasteh K. Candida infection in HIV positive patients 1985–2007. Mycoses. 2008;51(Suppl 2):58–61.

    Article  PubMed  Google Scholar 

  5. Chen YM, Kuo SH. HIV-1 in Taiwan. Lancet. 2007;369:623–5.

    Article  PubMed  Google Scholar 

  6. Liu JY, Lin HH, Liu YC, Lee SS, Chen YL, Hung CC, et al. Extremely high prevalence and genetic diversity of hepatitis C virus infection among HIV-infected injection drug users in Taiwan. Clin Infect Dis. 2008;46:1761–8.

    Article  CAS  PubMed  Google Scholar 

  7. Chen YC, Chang SC, Tai HM, Hsueh PR, Luh KT. Molecular epidemiology of Candida colonizing critically ill patients in intensive care units. J Formos Med Assoc. 2001;100:791–7.

    CAS  PubMed  Google Scholar 

  8. Li SY, Yang YL, Chen KW, Cheng HH, Chiou CS, Wang TH, et al. Molecular epidemiology of long-term colonization of Candida albicans strains from HIV-infected patients. Epidemiol Infect. 2006;134:265–9.

    Article  CAS  PubMed Central  PubMed  Google Scholar 

  9. Miranda LN, van der Heijden IM, Costa SF, Sousa AP, Sienra RA, Gobara S, et al. Candida colonisation as a source for candidaemia. J Hosp Infect. 2009;72:9–16.

    Article  CAS  PubMed  Google Scholar 

  10. Voss A, Hollis RJ, Pfaller MA, Wenzel RP, Doebbeling BN. Investigation of the sequence of colonization and candidemia in nonneutropenic patients. J Clin Microbiol. 1994;32:975–80.

    CAS  PubMed Central  PubMed  Google Scholar 

  11. Vargas KG, Joly S. Carriage frequency, intensity of carriage, and strains of oral yeast species vary in the progression to oral candidiasis in human immunodeficiency virus-positive individuals. J Clin Microbiol. 2002;40:341–50.

    Article  PubMed Central  PubMed  Google Scholar 

  12. Lin JN, Lin CC, Lai CH, Yang YL, Chen HT, Weng HC, et al. Predisposing factors for oropharyngeal colonization of yeasts in human immunodeficiency virus-infected patients: a prospective cross-sectional study. J Microbiol Immunol Infect. 2013;46:129–35.

    Article  PubMed  Google Scholar 

  13. Wu CJ, Lee HC, Yang YL, Chang CM, Chen HT, Lin CC, et al. Oropharyngeal yeast colonization in HIV-infected outpatients in southern Taiwan: CD4 count, efavirenz therapy and intravenous drug use matter. Clin Microbiol Infect. 2012;18:485–90.

    Article  CAS  PubMed  Google Scholar 

  14. Yang YL, Hung CC, Wang AH, Tseng FC, Leaw SN, Tseng YT, et al. Oropharyngeal colonization of HIV-infected outpatients in Taiwan by yeast pathogens. J Clin Microbiol. 2010;48:2609–12.

    Article  PubMed Central  PubMed  Google Scholar 

  15. Hung CC, Yang YL, Lauderdale TL, McDonald LC, Hsiao CF, Cheng HH, et al. Colonization of human immunodeficiency virus-infected outpatients in Taiwan with Candida species. J Clin Microbiol. 2005;43:1600–3.

    Article  PubMed Central  PubMed  Google Scholar 

  16. 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;62:230–3.

    Article  CAS  PubMed  Google Scholar 

  17. Leaw SN, Chang HC, Barton R, Bouchara JP, Chang TC. Identification of medically important Candida and non-Candida yeast species by an oligonucleotide array. J Clin Microbiol. 2007;45:2220–9.

    Article  CAS  PubMed Central  PubMed  Google Scholar 

  18. Leaw SN, Chang HC, Sun HF, Barton R, Bouchara JP, Chang TC. Identification of medically important yeast species by sequence analysis of the internal transcribed spacer regions. J Clin Microbiol. 2006;44:693–9.

    Article  CAS  PubMed Central  PubMed  Google Scholar 

  19. Clinical Laboratory Standard Institute. Reference method for broth dilution antifungal susceptibility testing of yeasts; approved standard-third edition. CLSI document M27-A3. Wayne, PA; 2008.

  20. Clinical Laboratory Standard Institute. Reference method for broth dilution antifungal susceptibility testing of yeasts; Fourth informational supplement. Clinical Laboratory Standards Institute document M27-S4. Wayne, PA; 2012.

  21. Pfaller MA, Andes D, Diekema DJ, Espinel-Ingroff A, Sheehan D. Wild-type MIC distributions, epidemiological cutoff values and species-specific clinical breakpoints for fluconazole and Candida: time for harmonization of CLSI and EUCAST broth microdilution methods. Drug Resist Updat. 2010;13:180–95.

    Article  CAS  PubMed  Google Scholar 

  22. Pfaller MA, Espinel-Ingroff A, Canton E, Castanheira M, Cuenca-Estrella M, Diekema DJ, et al. Wild-type MIC distributions and epidemiological cutoff values for amphotericin B, flucytosine, and itraconazole and Candida spp. as determined by CLSI broth microdilution. J Clin Microbiol. 2012;50:2040–6.

    Article  CAS  PubMed Central  PubMed  Google Scholar 

  23. Campisi G, Pizzo G, Milici ME, Mancuso S, Margiotta V. Candidal carriage in the oral cavity of human immunodeficiency virus-infected subjects. Oral Surg Oral Med Oral Pathol Oral Radiol Endod. 2002;93:281–6.

    Article  PubMed  Google Scholar 

  24. Delgado AC, de Jesus Pedro R, Aoki FH, Resende MR, Trabasso P, Colombo AL, et al. Clinical and microbiological assessment of patients with a long-term diagnosis of human immunodeficiency virus infection and Candida oral colonization. Clin Microbiol Infect. 2009;15:364–71.

    Article  CAS  PubMed  Google Scholar 

  25. Girish Kumar CP. Menon T, Rajasekaran S, Sekar B, Prabu D. Carriage of Candida species in oral cavities of HIV infected patients in South India. Mycoses. 2009;52:44–8.

    Article  PubMed  Google Scholar 

  26. Ohmit SE, Sobel JD, Schuman P, Duerr A, Mayer K, Rompalo A, et al. Longitudinal study of mucosal Candida species colonization and candidiasis among human immunodeficiency virus (HIV)-seropositive and at-risk HIV-seronegative women. J Infect Dis. 2003;188:118–27.

    Article  PubMed  Google Scholar 

  27. Yang YL, Leaw SN, Wang AH, Chen HT, Cheng WT, Lo HJ. Characterization of yeasts colonizing in healthy individuals. Med Mycol. 2011;49:103–6.

    Article  PubMed  Google Scholar 

  28. Li X, Lei L, Tan D, Jiang L, Zeng X, Dan H, et al. Oropharyngeal Candida colonization in human immunodeficiency virus infected patients. APMIS. 2012;121:375–402.

    Article  PubMed  Google Scholar 

  29. Luque AG, Biasoli MS, Tosello ME, Binolfi A, Lupo S, Magaro HM. Oral yeast carriage in HIV-infected and non-infected populations in Rosario, Argentina. Mycoses. 2009;52:53–9.

    Article  CAS  PubMed  Google Scholar 

  30. Schoofs AG, Odds FC, Colebunders R, Ieven M, Goossens H. Cross-sectional study of oral Candida carriage in a human immunodeficiency virus (HIV)-seropositive population: predisposing factors, epidemiology and antifungal susceptibility. Mycoses. 1998;41:203–11.

    Article  CAS  PubMed  Google Scholar 

  31. Yang YL, Li SY, Cheng HH, Lo HJ. Susceptibilities to amphotericin B and fluconazole of Candida species in TSARY 2002. Diagn Microbiol Infect Dis. 2005;51:179–83.

    Article  CAS  PubMed  Google Scholar 

  32. Yang YL, Wang AH, Wang CW, Cheng WT, Li SY, Lo HJ, et al. Susceptibilities to amphotericin B and fluconazole of Candida species in TSARY 2006. Diagn Microbiol Infect Dis. 2008;61:175–80.

    Article  CAS  PubMed  Google Scholar 

  33. Blignaut E, Pujol C, Joly S, Soll DR. Racial distribution of Candida dubliniensis colonization among South Africans. J Clin Microbiol. 2003;41:1838–42.

    Article  CAS  PubMed Central  PubMed  Google Scholar 

  34. Arribas JR, Hernandez-Albujar S, Gonzalez-Garcia JJ, Pena JM, Gonzalez A, Canedo T, et al. Impact of protease inhibitor therapy on HIV-related oropharyngeal candidiasis. AIDS. 2000;14:979–85.

    Article  CAS  PubMed  Google Scholar 

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Acknowledgments

We would like to thank Bristol Myers Squibb for supplying the amphotericin B and Pfizer for fluconazole and voriconazole. This study was supported by the grant NHRI ID-099-PP-04 and 00A1-ID-PP-04-014.

Conflict of interest

The authors report no conflicts of interest.

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Authors and Affiliations

  1. Section of Infectious Diseases, Department of Internal Medicine, China Medical University Hospital, Taichung, Taiwan

    Mao-Wang Ho, Chih-Yu Chi, Po-Chang Lin, Chia-Hui Chou & Chiou-Pyng Wu

  2. Institute of Molecular Medicine and Bioengineering, National Chiao Tung University, Hsinchu, Taiwan

    Yun-Liang Yang

  3. Department of Biological Science and Technology, National Chiao Tung University, Hsinchu, Taiwan

    Yun-Liang Yang & Hui-Ting Chen

  4. National Institute of Infectious Diseases and Vaccinology, National Health Research Institutes, 35, Keyan Road, Zhunan Town, Miaoli County, Taiwan

    Chih-Chao Lin, Hui-Ting Chen, Li-Yun Hsieh, Wen-Li Chu, Tsai-Ling Lauderdale & Hsiu-Jung Lo

  5. School of Dentistry, China Medical University, Taichung, Taiwan

    Hsiu-Jung Lo

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  1. Mao-Wang Ho
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Correspondence to Hsiu-Jung Lo.

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Ho, MW., Yang, YL., Lin, CC. et al. Yeast Oropharyngeal Colonization in Human Immunodeficiency Virus-Infected Patients in Central Taiwan. Mycopathologia 177, 309–317 (2014). https://doi.org/10.1007/s11046-014-9753-5

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  • DOI: https://doi.org/10.1007/s11046-014-9753-5

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