CC BY 4.0 · J Pediatr Infect Dis 2023; 18(03): 132-138
DOI: 10.1055/s-0043-1767737
Original Article

Investigation of Oral and Fecal Colonization with Candida Species and Associated Factors in Human Immunodeficiency Virus-Infected Children in Türkiye

1   Department of Medical Microbiology, Istanbul Faculty of Medicine, Istanbul University, Istanbul, Türkiye
,
1   Department of Medical Microbiology, Istanbul Faculty of Medicine, Istanbul University, Istanbul, Türkiye
,
2   Division of Pediatric Infectious Diseases, Department of Pediatrics, Istanbul Faculty of Medicine, Istanbul University, Istanbul, Türkiye
,
3   Division of Pediatric Infectious Diseases, Department of Pediatrics, Marmara University School of Medicine, Istanbul, Türkiye
,
2   Division of Pediatric Infectious Diseases, Department of Pediatrics, Istanbul Faculty of Medicine, Istanbul University, Istanbul, Türkiye
,
4   Department of Biostatistics and Medical Informatics, Kocaeli University Faculty of Medicine, Kocaeli, Türkiye
,
2   Division of Pediatric Infectious Diseases, Department of Pediatrics, Istanbul Faculty of Medicine, Istanbul University, Istanbul, Türkiye
,
1   Department of Medical Microbiology, Istanbul Faculty of Medicine, Istanbul University, Istanbul, Türkiye
,
1   Department of Medical Microbiology, Istanbul Faculty of Medicine, Istanbul University, Istanbul, Türkiye
› Institutsangaben
Funding This work was supported by the Research Fund of Istanbul University, Project No: 26586.

Abstract

Objective The risk of endogenous infections in human immunodeficiency virus (HIV)-infected individuals increases with Candida species colonized in mouth and intestinal areas. The predisposing factors for colonization and the prevalence of different Candida spp. in HIV-infected Turkish children remain unknown. This study aimed to determine the colonization frequency and risk factors of colonization with Candida species in oral and fecal samples of HIV-infected pediatric patients in relation to a control group.

Methods Oral and feces samples of 22 HIV-infected and 52 healthy children were plated onto CHROMagar and CHROM-Pal-agar. Yeasts were identified by conventional methods, and strains with insufficient identification were identified by molecular techniques.

ResultsCandida spp. were detected in oral/fecal samples of 50%/68.2% HIV-infected and 36.5%/73.1% healthy children. The most common species was Candida albicans in oral and fecal samples of HIV-infected (31.8 and 31.8%) and healthy (26.9 and 48.1%) children. The most frequently non-albicans species in oral samples was Candida dubliniensis (18.2%) in HIV-infected children and Candida parapsilosis (3.8%) in healthy children. In feces samples, C. parapsilosis, Candida glabrata, and Candida krusei were most frequent (13.6%, each) in HIV-infected patients, and Candida kefyr (11.5%) was most frequent in controls. There was a significant association between oral C. dubliniensis colonization and HIV infection (p = 0.006). Yeast carriage was not associated with gender and viral load in HIV-infected patients.

Conclusion The isolation of C. dubliniensis from oral and fecal samples of pediatric HIV patients was done for the first time in Türkiye in the present study. Additional studies are needed to clarify the factors associated with oral and fecal Candida colonization in these children.



Publikationsverlauf

Eingereicht: 19. Oktober 2022

Angenommen: 22. Februar 2023

Artikel online veröffentlicht:
31. März 2023

© 2023. The Author(s). This is an open access article published by Thieme under the terms of the Creative Commons Attribution License, permitting unrestricted use, distribution, and reproduction so long as the original work is properly cited. (https://creativecommons.org/licenses/by/4.0/)

Georg Thieme Verlag KG
Rüdigerstraße 14, 70469 Stuttgart, Germany

 
  • References

  • 1 UNICEF data. (2021): HIV statistics-global and regional trends. Accessed September 7, 2022 at: https://data.unicef.org/topic/hivaids/global-regional-trends
  • 2 Türkiye HIV/AIDS Control Program (2019–2024). Turkish Ministry of Health Publication; 2019. ;1131, Ankara
  • 3 Cerqueira DF, Portela MB, Pomarico L, de Araújo Soares RM, de Souza IPR, Castro GF. Oral Candida colonization and its relation with predisposing factors in HIV-infected children and their uninfected siblings in Brazil: the era of highly active antiretroviral therapy. J Oral Pathol Med 2010; 39 (02) 188-194
  • 4 Costa CR, Cohen AJ, Fernandes OF. et al. Asymptomatic oral carriage of Candida species in HIV-infected patients in the highly active antiretroviral therapy era. Rev Inst Med Trop São Paulo 2006; 48 (05) 257-261
  • 5 Blignaut E. Oral candidiasis and oral yeast carriage among institutionalised South African paediatric HIV/AIDS patients. Mycopathologia 2007; 163 (02) 67-73
  • 6 Scerpella EG, Gould SS, Mathewson JJ, DuPont HL, Dupont LH. Methods for detection of an intestinal secretory immunoglobulin A response to Candida spp. and their preliminary application in human immunodeficiency virus-infected patients with chronic diarrhea. Clin Diagn Lab Immunol 1995; 2 (02) 246-248
  • 7 Domaneschi C, Massarente DB, de Freitas RS. et al. Oral colonization by Candida species in AIDS pediatric patients. Oral Dis 2011; 17 (04) 393-398
  • 8 Awoyeni A, Olaniran O, Odetoyin B. et al. Isolation and evaluation of Candida species and their association with CD4+ T cells counts in HIV patients with diarrhoea. Afr Health Sci 2017; 17 (02) 322-329
  • 9 Tooyama H, Matsumoto T, Hayashi K. et al. Candida concentrations determined following concentrated oral rinse culture reflect clinical oral signs. BMC Oral Health 2015; 15: 150
  • 10 Esebelahie NO, Enweani IB, Omoregie R. Candida colonisation in asymptomatic HIV patients attending a tertiary hospital in Benin City, Nigeria. Libyan J Med 2013; 8 (01) 20322
  • 11 White PL, Williams DW, Kuriyama T, Samad SA, Lewis MA, Barnes RA. Detection of Candida in concentrated oral rinse cultures by real-time PCR. J Clin Microbiol 2004; 42 (05) 2101-2107
  • 12 Sahand IH, Maza JL, Eraso E. et al. Evaluation of CHROM-Pal medium for the isolation and direct identification of Candida dubliniensis in primary cultures from the oral cavity. J Med Microbiol 2009; 58 (Pt 11): 1437-1442
  • 13 Walsh TH, Hayden RT, Larone DH. Larone's Medically Important Fungi: A Guide to Identification. Washington DC: ASM Press; 2018
  • 14 Pongsiriwet S, Iamaroon A, Kanjanavanit S, Pattanaporn K, Krisanaprakornkit S. Oral lesions and dental caries status in perinatally HIV-infected children in Northern Thailand. Int J Paediatr Dent 2003; 13 (03) 180-185
  • 15 Pomarico L, Cerqueira DF, de Araujo Soares RM. et al. Associations among the use of highly active antiretroviral therapy, oral candidiasis, oral Candida species and salivary immunoglobulin A in HIV-infected children. Oral Surg Oral Med Oral Pathol Oral Radiol Endod 2009; 108 (02) 203-210
  • 16 Leibovitz E, Rigaud M, Chandwani S. et al. Disseminated fungal infections in children infected with human immunodeficiency virus. Pediatr Infect Dis J 1991; 10 (12) 888-894
  • 17 Chiou CC, Groll AH, Gonzalez CE. et al. Esophageal candidiasis in pediatric acquired immunodeficiency syndrome: clinical manifestations and risk factors. Pediatr Infect Dis J 2000; 19 (08) 729-734
  • 18 Pongsiriwet S, Iamaroon A, Sriburee P, Pattanaporn K, Krisanaprakornkit S. Oral colonization of Candida species in perinatally HIV-infected children in northern Thailand. J Oral Sci 2004; 46 (02) 101-105
  • 19 Jabra-Rizk MA, Falkler Jr WA, Enwonwu CO, Onwujekwe Jr DI, Merz WG, Meiller TF. Prevalence of yeast among children in Nigeria and the United States. Oral Microbiol Immunol 2001; 16 (06) 383-385
  • 20 Alves TP, Simões AC, Soares RM, Moreno DS, Portela MB, Castro GF. Salivary lactoferrin in HIV-infected children: correlation with Candida albicans carriage, oral manifestations, HIV infection and its antifungal activity. Arch Oral Biol 2014; 59 (08) 775-782
  • 21 Erköse G, Erturan Z. Oral Candida colonization of human immunodeficiency virus infected subjects in Türkiye and its relation with viral load and CD4+ T-lymphocyte count. Mycoses 2007; 50 (06) 485-490
  • 22 Mushi MF, Bader O, Taverne-Ghadwal L, Bii C, Groß U, Mshana SE. Oral candidiasis among African human immunodeficiency virus-infected individuals: 10 years of systematic review and meta-analysis from sub-Saharan Africa. J Oral Microbiol 2017; 9 (01) 1317579
  • 23 Samaranayake LP, MacFarlane TW, Lamey PJ, Ferguson MM. A comparison of oral rinse and imprint sampling techniques for the detection of yeast, coliform and Staphylococcus aureus carriage in the oral cavity. J Oral Pathol 1986; 15 (07) 386-388
  • 24 Castillo-Martínez NA, Mouriño-Pérez RR, Cornejo-Bravo JM, Gaitán-Cepeda LA. [Factors related to oral candidiasis in HIV children and adolescents, species characterization and antifungal susceptibility]. Rev Chilena Infectol 2018; 35 (04) 377-385
  • 25 Loreto ES, Scheid LA, Nogueira CW, Zeni G, Santurio JM, Alves SH. Candida dubliniensis: epidemiology and phenotypic methods for identification. Mycopathologia 2010; 169 (06) 431-443
  • 26 Sano A, Vilela MM, Takahashi I. et al. Isolation of Candida dubliniensis from the oral cavity of an HIV-positive child in Brazil. Nippon Ishinkin Gakkai Zasshi 2000; 41 (03) 177-181
  • 27 Brown DM, Jabra-Rizk MA, Falkler Jr WA, Baqui AA, Meiller TF. Identification of Candida dubliniensis in a study of HIV-seropositive pediatric dental patients. Pediatr Dent 2000; 22 (03) 234-238
  • 28 Portela MB, Souza IP, Costa EM, Hagler AN, Soares RM, Santos AL. Differential recovery of Candida species from subgingival sites in human immunodeficiency virus-positive and healthy children from Rio de Janeiro, Brazil. J Clin Microbiol 2004; 42 (12) 5925-5927
  • 29 Perea S, López-Ribot JL, Wickes BL. et al. Molecular mechanisms of fluconazole resistance in Candida dubliniensis isolates from human immunodeficiency virus-infected patients with oropharyngeal candidiasis. Antimicrob Agents Chemother 2002; 46 (06) 1695-1703
  • 30 Jabra-Rizk MA, Brenner TM, Romagnoli M. et al. Evaluation of a reformulated CHROMagar Candida. J Clin Microbiol 2001; 39 (05) 2015-2016
  • 31 Klein RS, Arnsten JH, Sobel JD. Oropharyngeal Candida colonization and human immunodeficiency virus type 1 infection. J Infect Dis 2000; 181 (02) 812-813
  • 32 de Brito Costa EM, dos Santos AL, Cardoso AS. et al. Heterogeneity of metallo and serine extracellular proteinases in oral clinical isolates of Candida albicans in HIV-positive and healthy children from Rio de Janeiro, Brazil. FEMS Immunol Med Microbiol 2003; 38 (02) 173-180
  • 33 Koffi-Akoua G, Ferly-Therizol M, Kouassi-Beugre MT. et al. [Cryptosporidium and candida in pediatric diarrhea in Abidjan]. Bull Soc Pathol Exot 1989; 82 (04) 451-457
  • 34 Chaudhury A, Nath G, Shukla B, Panda S, Singh TB. Diarrhoea associated with Candida spp.: incidence and seasonal variation. J Diarrhoeal Dis Res 1996; 14 (02) 110-112
  • 35 Rossit AR, de Almeida MT, Nogueira CA. et al. Bacterial, yeast, parasitic, and viral enteropathogens in HIV-infected children from São Paulo State, Southeastern Brazil. Diagn Microbiol Infect Dis 2007; 57 (01) 59-66
  • 36 Samé-Ekobo A, Lohoué J, Mbassi A. [A clinical and biological study of parasitic and fungal diarrhea in immunosuppressed patients in an urban and suburban area of Yaoundé]. Sante 1997; 7 (06) 349-354