Top

Clinical Oral Investigations

Published in:

01-11-2016 | Original Article

Prevalence of Candida albicans and Candida dubliniensis in caries-free and caries-active children in relation to the oral microbiota—a clinical study

Authors: A. Al-Ahmad, T. M. Auschill, R. Dakhel, A. Wittmer, K. Pelz, C. Heumann, E. Hellwig, N. B. Arweiler

Published in: Clinical Oral Investigations | Issue 8/2016

Abstract

Objectives

The correlation between caries and the oral prevalence of Candida spp. in children is contradictory in literature. Thereby, authors focused on Candida albicans as the most isolated Candida species from the oral cavity. Therefore, the aim of the present study was to compare caries-free and caries-bearing children regarding their oral carriage of Candida spp.

Material and methods

Twenty-six caries-free (CF group) and 26 caries-active children (CA group) were included into this study. Three different types of specimens were assessed, saliva and plaque, and in the case of caries, infected dentine samples were microbiologically analyzed for aerobic and anaerobic microorganisms and their counts. Special attention was given to the differentiation between C. albicans and Candida dubliniensis. Additionally, different biochemical tests, VITEK 2 (VITEK®2, bioMérieux, Marcy-l’Etoile, France) and 16S and 18S ribosomal DNA (rDNA) sequencing, were applied for identification.

Results

The detection of C. albicans did not differ between the CF and CA groups. C. dubliniensis was never detected in any specimen of the CF group, but occurred in one quarter of the CA group (27 % in plaque, 23 % in saliva), thus leading to a statistically significant difference between the two groups (p < 0.05). In six of these cases, C. dubliniensis was detected concomitantly in saliva and plaque and once only in plaque. CA group harbored statistically more Streptococcus mutans than the control group revealing a correlation between S. mutans and C. dubliniensis regarding the caries group.

Conclusions

This is the first study reporting a frequent detection of C. dubliniensis in caries-active children, which could have been underestimated so far due to difficulties in differentiation between this yeast species and C. albicans.

Clinical relevance

Microbiological diagnostic—especially of oral Candida species—is an important determinant for identifying etiological factors of dental caries in children.

Bliss JM, Wong AY, Bhak G, Laforce-Nesbitt SS, Taylor S, Tan S, Stoll BJ, Higgins RD, Shankaran S and Benjamin DK, Jr. (2012) Candida virulence properties and adverse clinical outcomes in neonatal candidiasis. J Pediatr 161:441–447.e2. doi:10.1016/j.jpeds.2012.02.051

Leibovitz E (2012) Strategies for the prevention of neonatal candidiasis. Pediatr Neonatol 53:83–89. doi:10.1016/j.pedneo.2012.01.004 PubMed

Gammelsrud KW, Sandven P, Hoiby EA, Sandvik L, Brandtzaeg P, Gaustad P (2011) Colonization by Candida in children with cancer, children with cystic fibrosis, and healthy controls. Clin Microbiol Infect 17:1875–1881. doi:10.1111/j.1469-0691.2011.03528.x PubMed

Grotz KA, Genitsariotis S, Vehling D, Al-Nawas B (2003) Long-term oral Candida colonization, mucositis and salivary function after head and neck radiotherapy. Support Care Cancer 11:717–721. doi:10.1007/s00520-003-0506-0 PubMed

Nagao M, Saito T, Doi S, Hotta G, Yamamoto M, Matsumura Y, Matsushima A, Ito Y, Takakura S, Ichiyama S (2012) Clinical characteristics and risk factors of ocular candidiasis. Diagn Microbiol Infect Dis 73:149–152. doi:10.1016/j.diagmicrobio.2012.03.006 PubMed

Rautemaa R, Ramage G (2011) Oral candidosis—clinical challenges of a biofilm disease. Crit Rev Microbiol 37:328–336. doi:10.3109/1040841x.2011.585606 PubMed

Siahi-Benlarbi R, Nies SM, Sziegoleit A, Bauer J, Schranz D, Wetzel WE (2010) Caries-, Candida- and Candida antigen/antibody frequency in children after heart transplantation and children with congenital heart disease. Pediatr Transplant 14:715–721. doi:10.1111/j.1399-3046.2008.01115.x PubMed

Sharp AM, Odds FC, Evans EG (1992) Candida strains from neonates in a special care baby unit. Arch Dis Child 67:48–52PubMedPubMedCentral

Marodi L, Johnston Jr RB (2007) Invasive Candida species disease in infants and children: occurrence, risk factors, management, and innate host defense mechanisms. Curr Opin Pediatr 19:693–697. doi:10.1097/MOP.0b013e3282f1dde9

10.

Hacimustafaoglu M, Celebi S (2011) Candida infections in non-neutropenic children after the neonatal period. Expert Rev Anti-Infect Ther 9:923–940. doi:10.1586/eri.11.104 PubMed

11.

de Carvalho FG, Silva DS, Hebling J, Spolidorio LC, Spolidorio DM (2006) Presence of mutans streptococci and Candida spp. in dental plaque/dentine of carious teeth and early childhood caries. Arch Oral Biol 51:1024–1028. doi:10.1016/j.archoralbio.2006.06.001 PubMed

12.

Hossain H, Ansari F, Schulz-Weidner N, Wetzel WE, Chakraborty T, Domann E (2003) Clonal identity of Candida albicans in the oral cavity and the gastrointestinal tract of pre-school children. Oral Microbiol Immunol 18:302–308PubMed

13.

Sardi JC, Duque C, Mariano FS, Peixoto IT, Hofling JF, Goncalves RB (2010) Candida spp. in periodontal disease: a brief review. J Oral Sci 52:177–185PubMed

14.

Waltimo TM, Sen BH, Meurman JH, Orstavik D, Haapasalo MP (2003) Yeasts in apical periodontitis. Crit Rev Oral Biol Med 14:128–137PubMed

15.

Leonhardt A, Renvert S, Dahlen G (1999) Microbial findings at failing implants. Clin Oral Implants Res 10:339–345PubMed

16.

Pye AD, Lockhart DE, Dawson MP, Murray CA, Smith AJ (2009) A review of dental implants and infection. J Hosp Infect 72:104–110. doi:10.1016/j.jhin.2009.02.010 PubMed

17.

Bilhan H, Sulun T, Erkose G, Kurt H, Erturan Z, Kutay O, Bilgin T (2009) The role of Candida albicans hyphae and Lactobacillus in denture-related stomatitis. Clin Oral Investig 13:363–368. doi:10.1007/s00784-008-0240-6 PubMed

18.

Gendreau L, Loewy ZG (2011) Epidemiology and etiology of denture stomatitis. J Prosthodont 20:251–260. doi:10.1111/j.1532-849X.2011.00698.x PubMed

19.

Salerno C, Pascale M, Contaldo M, Esposito V, Busciolano M, Milillo L, Guida A, Petruzzi M, Serpico R (2011) Candida-associated denture stomatitis. Med Oral Patol Oral Cir Bucal 16:e139–e143PubMed

20.

Klinke T, Guggenheim B, Klimm W, Thurnheer T (2011) Dental caries in rats associated with Candida albicans. Caries Res 45:100–106. doi:10.1159/000324809 PubMed

21.

Szabo B, Majoros L, Papp-Falusi E, Szabo Z, Szabo J, Marton I, Kelentey B (2014) Studies on the possible aetiological role of different Candida species in pathogenesis of dentine caries by monitoring the calcium release from tooth particles. Acta Microbiol Immunol Hung 61:11–17. doi:10.1556/AMicr.61.2014.1.2 PubMed

22.

Peretz B, Mazor Y, Dagon N, Bar-Ness Greenstein R (2011) Candida, mutans streptococci, oral hygiene and caries in children. J Clin Pediatr Dent 36:185–188PubMed

23.

Maijala M, Rautemaa R, Jarvensivu A, Richardson M, Salo T, Tjaderhane L (2007) Candida albicans does not invade carious human dentine. Oral Dis 13:279–284. doi:10.1111/j.1601-0825.2006.01279.x PubMed

24.

Akdeniz BG, Koparal E, Sen BH, Ates M, Denizci AA (2002) Prevalence of Candida albicans in oral cavities and root canals of children. ASDC J Dent Child 69(289–92):235

25.

Moalic E, Gestalin A, Quinio D, Gest PE, Zerilli A and Le Flohic AM (2001) The extent of oral fungal flora in 353 students and possible relationships with dental caries. Caries research 35:149–55. doi:47447

26.

Raja M, Hannan A, Ali K (2010) Association of oral candidal carriage with dental caries in children. Caries Res 44:272–276. doi:10.1159/000314675 PubMed

27.

Rozkiewicz D, Daniluk T, Zaremba ML, Cylwik-Rokicka D, Stokowska W, Pawinska M, Dabrowska E, Marczuk-Kolada G, Waszkiel D (2006) Oral Candida albicans carriage in healthy preschool and school children. Adv Med Sci 51(Suppl 1):187–190PubMed

28.

Signoretto C, Burlacchini G, Faccioni F, Zanderigo M, Bozzola N, Canepari P (2009) Support for the role of Candida spp. in extensive caries lesions of children. New Microbiol 32:101–107PubMed

29.

Yang XQ, Zhang Q, Lu LY, Yang R, Liu Y, Zou J (2012) Genotypic distribution of Candida albicans in dental biofilm of Chinese children associated with severe early childhood caries. Arch Oral Biol 57:1048–1053. doi:10.1016/j.archoralbio.2012.05.012 PubMed

30.

Kumar K, Prakash A, Tasleem M, Islam A, Ahmad F, Hassan MI (2014) Functional annotation of putative hypothetical proteins from Candida dubliniensis. Gene 543:93–100. doi:10.1016/j.gene.2014.03.060 PubMed

31.

Priest SJ, Lorenz MC (2015) Characterization of virulence-related phenotypes in Candida species of the CUG clade. Eukaryotic Cell 14:931–940. doi:10.1128/ec.00062-15 PubMedPubMedCentral

32.

Alnuaimi AD, O'Brien-Simpson NM, Reynolds EC, McCullough MJ (2013) Clinical isolates and laboratory reference Candida species and strains have varying abilities to form biofilms. FEMS Yeast Res 13:689–699. doi:10.1111/1567-1364.12068 PubMed

33.

Syed SA, Loesche WJ (1972) Survival of human dental plaque flora in various transport media. Appl Microbiol 24:638–644PubMedPubMedCentral

34.

Al-Ahmad A, Pelz K, Schirrmeister JF, Hellwig E, Pukall R (2008) Characterization of the first oral vagococcus isolate from a root-filled tooth with periradicular lesions. Curr Microbiol 57:235–238. doi:10.1007/s00284-008-9182-0 PubMed

35.

Anderson AC, Hellwig E, Vespermann R, Wittmer A, Schmid M, Karygianni L, Al-Ahmad A (2012) Comprehensive analysis of secondary dental root canal infections: a combination of culture and culture-independent approaches reveals new insights. PLoS One 7:e49576. doi:10.1371/journal.pone.0049576 PubMedPubMedCentral

36.

Schirrmeister JF, Liebenow AL, Pelz K, Wittmer A, Serr A, Hellwig E, Al-Ahmad A (2009) New bacterial compositions in root-filled teeth with periradicular lesions. J Endod 35:169–174. doi:10.1016/j.joen.2008.10.024 PubMed

37.

Sullivan DJ, Westerneng TJ, Haynes KA, Bennett DE, Coleman DC (1995) Candida dubliniensis sp. nov.: phenotypic and molecular characterization of a novel species associated with oral candidosis in HIV-infected individuals. Microbiology 141(Pt 7):1507–1521PubMed

38.

Schoofs A, Odds FC, Colebunders R, Ieven M, Goossens H (1997) Use of specialised isolation media for recognition and identification of Candida dubliniensis isolates from HIV-infected patients. Eur J Clin Microbiol Infect Dis 16:296–300PubMed

39.

Sullivan D, Haynes K, Bille J, Boerlin P, Rodero L, Lloyd S, Henman M, Coleman D (1997) Widespread geographic distribution of oral Candida dubliniensis strains in human immunodeficiency virus-infected individuals. J Clin Microbiol 35:960–964PubMedPubMedCentral

40.

Klinke T, Kneist S, de Soet JJ, Kuhlisch E, Mauersberger S, Forster A, Klimm W (2009) Acid production by oral strains of Candida albicans and lactobacilli. Caries Res 43:83–91. doi:10.1159/000204911 PubMed

41.

Kneist S, Borutta A, Sigusch BW, Nietzsche S, Kupper H, Kostrzewa M, Callaway A (2015) First-time isolation of Candida dubliniensis from plaque and carious dentine of primary teeth. Eur Arch Paediatr Dent. doi:10.1007/s40368-015-0180-1 PubMed

42.

Starr JR, White TC, Leroux BG, Luis HS, Bernardo M, Leitao J, Roberts MC (2002) Persistence of oral Candida albicans carriage in healthy Portuguese schoolchildren followed for 3 years. Oral Microbiol Immunol 17:304–310PubMed

43.

Owotade FJ, Patel M, Ralephenya TR, Vergotine G (2013) Oral Candida colonization in HIV-positive women: associated factors and changes following antiretroviral therapy. J Med Microbiol 62:126–132. doi:10.1099/jmm.0.047522-0 PubMed

44.

Shen S, Samaranayake LP, Yip HK, Dyson JE (2002) Bacterial and yeast flora of root surface caries in elderly, ethnic Chinese. Oral Dis 8:207–217PubMed

45.

Linossier A, Vargas A, Villegas R, Chimenos E (2002) Quantitative relationship between salivary level of Streptococcus mutans and Candida albicans in children with Down's syndrome. Med Oral 7:284–292PubMed

46.

Holmes AR, Gopal PK, Jenkinson HF (1995) Adherence of Candida albicans to a cell surface polysaccharide receptor on Streptococcus gordonii. Infect Immun 63:1827–1834PubMedPubMedCentral

47.

Gross EL, Leys EJ, Gasparovich SR, Firestone ND, Schwartzbaum JA, Janies DA, Asnani K, Griffen AL (2010) Bacterial 16S sequence analysis of severe caries in young permanent teeth. J Clin Microbiol 48:4121–4128. doi:10.1128/jcm.01232-10 PubMedPubMedCentral

48.

Klinke T, Urban M, Luck C, Hannig C, Kuhn M, Kramer N (2014) Changes in Candida spp., mutans streptococci and lactobacilli following treatment of early childhood caries: a 1-year follow-up. Caries Res 48:24–31. doi:10.1159/000351673 PubMed

Title: Prevalence of Candida albicans and Candida dubliniensis in caries-free and caries-active children in relation to the oral microbiota—a clinical study
Authors: A. Al-Ahmad
T. M. Auschill
R. Dakhel
A. Wittmer
K. Pelz
C. Heumann
E. Hellwig
N. B. Arweiler
Publication date: 01-11-2016
Publisher: Springer Berlin Heidelberg
Published in: Clinical Oral Investigations / Issue 8/2016
Print ISSN: 1432-6981
Electronic ISSN: 1436-3771
DOI: https://doi.org/10.1007/s00784-015-1696-9

Keynote webinar | Spotlight on sleep in brain health

Springer Medicine

Prevalence of Candida albicans and Candida dubliniensis in caries-free and caries-active children in relation to the oral microbiota—a clinical study

Abstract

Objectives

Material and methods

Results

Conclusions

Clinical relevance

Keynote webinar | Spotlight on sleep in brain health

Springer Medicine

Abstract

Objectives

Material and methods

Results

Conclusions

Clinical relevance

Please log in to get access to this content

Other articles of this Issue 8/2016

Erratum to: Classification of periodontal biotypes with the use of CBCT. A cross-sectional study

Cone beam CT evaluation of mandibular molar root canal morphology in a Turkish Cypriot population

Evaluation of an interdisciplinary preventive programme for early childhood caries: findings of a regional German birth cohort study

Vascularization after treatment of gingival recession defects with platelet-rich fibrin or connective tissue graft

An ex vivo comparison of working length determination by three electronic root canal length measurement devices integrated into endodontic rotary motors

Significance of endothelial progenitor cells (EPC) for tumorigenesis of head and neck squamous cell carcinoma (HNSCC): possible marker of tumor progression and neovascularization?