Oral yeast colonization in patients with eating disorders: commensal acquisition or due to purgative habits?

Camilla Esteves

Roseli de Freitas

Wladimir de Campos

Natali Shimabukuro

^{Universidade de São Paulo, Faculdade de Odontologia, Departamento de Estomatologia, São Paulo, São Paulo, Brazil}

^{Universidade de São Paulo, Instituto de Medicina Tropical de São Paulo, Laboratório de Micologia Médica (LIM 53), São Paulo, São Paulo, Brazil}

^{Universidade de São Paulo, Faculdade de Medicina, Departamento e Instituto de Psiquiatria, São Paulo, São Paulo, Brazil}

Correspondence to: Wladimir Gushiken de Campos Universidade de São Paulo, Faculdade de Odontologia, Departamento de Estomatologia, Av. Professor Lineu Prestes, 2227, CEP 05508-001, São Paulo, SP, Brazil Tel: +55 11 3091-7883 E-mail: rb.psu@sopmac.rimidalw

CONFLICT OF INTERESTS

We have no conflict of interests or disclosures to declare.

CONFLICT OF INTERESTS

We have no conflict of interests or disclosures to declare.

Received 2019 Nov 28; Accepted 2020 Apr 27.

This is an Open Access article distributed under the terms of the Creative Commons Attribution Non-Commercial License, which permits unrestricted non-commercial use, distribution, and reproduction in any medium, provided the original work is properly cited.

ABSTRACT

Oral problems are common in patients diagnosed with Eating Disorders (ED) and still require better elucidation. We aimed to analyze the prevalence of oral Candida spp in individuals with ED. The sample of the study was comprised of 30 women with purgative habits and 15 without purgative habits. Samples of the oral cavity were collected by sterile cotton swab rubbed on soft tissues and teeth. Yeasts were isolated on Sabouraud dextrose agar. Yeasts were isolated from the oral cavity of 53% of the patients yielding 75 yeast isolates; of these, 43 were identified by conventional mycological methods: C. parapsilosis (n=19), C. glabrata (n=16), Rhodotorula sp (n= 6), C. famata (n=2). The remaining 32 isolates were presumptively identified as C. albicans or C. dubliniensis and required mass spectrometry for the final differentiation: 28 isolates were confirmed as C. albicans and four as C. dubliniensis. Among the control group, only four subjects (26.7%) were found to harbor C. albicans. The four C. dubliniensis isolates were from two patients, one that was only colonized and the other, with severe ED, was diagnosed with an oral candidiasis as demonstrated by the presence of pseudohyphae on the direct mycological exam from different sites. The increased rate of isolation of non-albicans species, such as C. glabrata, C. parapsilosis, and C. dubliniensis in the oral cavity from ED patients with nutritional deficiency may suggest that purgative habits of these patients can lead to changes in normal flora and predispose to oral candidiasis.

Keywords: Eating disorders, Oral candidiasis, Candida, Infection

ABSTRACT

ACKNOWLEDGMENTS

DYT conducted this work supported by a Fapesp postdoctoral fellowship (2018/15491); GB conducted this work with finacial support from Fapesp, grant Nº 2016/08730-6, and Conselho Nacional de Desenvolvimento Científico e Tecnológico. We are grateful to the anonymous reviewers for their many suggestions, which helped improving the manuscript.

ACKNOWLEDGMENTS

REFERENCES

References

1. Klump KL, Bulik CM, Kaye WH, Treasure J, Tyson EAcademy for eating disorders position paper: eating disorders are serious mental illnesses. Int J Eat Disord. 2009;42:97–103.[PubMed][Google Scholar]
2. Uhlen MM, Tveit AB, Stenhagen KR, Mulic A. Self-induced vomiting and dental erosion: a clinical study. 92BMC Oral Health. 2014;14
3. Dynesen AW, Bardow A, Petersson B, Nielsen LR, Nauntofte BSalivary changes and dental erosion in bulimia nervosa. Oral Surg Oral Med Oral Pathol Oral Radiol Endod. 2008;106:696–707.[PubMed][Google Scholar]
4. Lo Russo L, Campisi G, Di Fede O, Di Liberto C, Panzarella V, Lo Muzio LOral manifestations of eating disorders: a critical review. Oral Dis. 2008;14:479–484.[PubMed][Google Scholar]
5. Chanda W, Joseph TP, Wang W, Padhiar AA, Zhong MThe potential management of oral candidiasis using anti-biofilm therapies. Med Hypotheses. 2017;106:15–18.[PubMed][Google Scholar]
6. Akgül Ö, Çerikçioǧlu NHypertonic sabouraud dextrose agar as a substrate for differentiation of Candida dubliniensis. Mycopathologia. 2009;167:357–359.[PubMed][Google Scholar]
7. Coleman DC, Rinaldi MG, Haynes KA, Rex JH, Summerbell RC, Anaissie EJ, et al Importance of Candida species other than Candida albicans as opportunistic pathogens. Med Mycol. 1998;36(Suppl 1):156–165.[PubMed][Google Scholar]
8. Matic Petrovic S, Radunovic M, Barac M, Kuzmanovic Pficer J, Pavlica D, Arsic Arsenijevic V, et al Subgingival areas as potential reservoirs of different Candida spp in type 2 diabetes patients and healthy subjects. PLoS One. 2019;14:e0210527. [Google Scholar]
9. Vieira Esteves C, Gushiken de Campos W, Gallo RT, Ebling Artes G, Shimabukuro N, Witzel AL, et al Oral profile of eating disorders patients: case series. Spec Care Dentist. 2019;39:572–577.[PubMed][Google Scholar]
10. Hoog GS, Guarro J, Gené J, Figueras MJ Atlas of clinical fungi. 2nd. Utrecht: Centraalbureau voor Schimmelcultures; 2000. [PubMed][Google Scholar]
11. Gales AC, Pfaller MA, Houston AK, Joly S, Sullivan DJ, Coleman DC, et al Identification of Candida dubliniensis based on temperature and utilization of xylose and α-methyl-D-glucoside as determined with the API 20C AUX and Vitek YBC systems. J Clin Microbiol. 1999;37:3804–3808.[Google Scholar]
12. Pinjon E, Sullivan D, Salkin I, Shanley D, Coleman DSimple, inexpensive, reliable method for differentiation of Candida dubliniensis from Candida albicans. J Clin Microbiol. 1998;36:2093–2095.[Google Scholar]
13. Chowdhary A, Randhawa HS, Kowshik T, Kathuria S, Roy P, Brandt MEApplication of hypertonic Sabouraud glucose agar for differentiation of Candida dubliniensis from Candida albicans. Diagn Microbiol Infect Dis. 2011;69:440–442.[PubMed][Google Scholar]
14. Morgan XC, Segata N, Huttenhower CBiodiversity and functional genomics in the human microbiome. Trends Genet. 2013;29:51–58.[Google Scholar]
15. Rossoni RD, Barbosa JO, Vilela SF, Jorge AO, Junqueira JC. Comparison of the hemolytic activity between C. albicans and non-albicans Candida species. Braz Oral Res. 2013;27:484–489.[PubMed]
16. Trofa D, Gácser A, Nosanchuk JDCandida parapsilosis: an emerging fungal pathogen. Clin Microbiol Rev. 2008;21:606–625.[Google Scholar]
17. Rodrigues CF, Rodrigues ME, Silva S, Henriques M J Fungi. Vol. 3. Basel: 2017. Candida glabrata biofilms: how far have we come?E11 [Google Scholar]
18. Livério HO, Ruiz LS, Freitas RS, Nishikaku A, Souza AC, Paula CR, et al. Phenotypic and genotypic detection of candida albicans and candida dubliniensis strains isolated from oral mucosa of AIDS pediatric patients. e14Rev Inst Med Trop Sao Paulo. 2017;59
19. Back-Brito GN, Mota AJ, Souza Bernardes LÂ, Takamune SS, Prado EF, Cordás TA, et al Effects of eating disorders on oral fungal diversity. Oral Surg Oral Med Oral Pathol Oral Radiol. 2012;113:512–517.[PubMed][Google Scholar]
20. Li L, Redding S, Dongari-Bagtzoglou ACandida glabrata: an emerging oral opportunistic pathogen. J Dental Res. 2007;86:204–215.[PubMed][Google Scholar]
21. Tati S, Davidow P, McCall A, Hwang-Wong E, Rojas IG, Cormack B, et al Candida glabrata binding to Candida albicans hiphae enables its development in oropharyngeal candidiasis. PLoS Pathog. 2016;12:e1005522. [Google Scholar]
22. Seabra CL, Botelho CM, Henriques M, Oliveira RDifferential adherence and expression of virulence traits by Candida albicans and Candida parapsilosis in mono- and dual-species cultures in artificial saliva. Mycopathologia. 2013;176:33–40.[PubMed][Google Scholar]
23. Fotedar R, Al Hedaithy SSPrevalence of Candida dubliniensis among germ tube-positive yeasts recovered from the respiratory specimens in HIV-negative patients. Mycoses. 2004;47:150–155.[PubMed][Google Scholar]
24. Loreto ES, Pozzatti P, Alves Scheid L, Santurio D, Santurio JM, Alves SHDifferentiation of Candida dubliniensis from Candida albicans on rosemary extract agar and oregano extract agar. J Clin Lab Anal. 2008;22:172–177.[Google Scholar]
25. Chalupová J, Raus M, Sedlářová M, Šebela MIdentification of fungal microorganisms by MALDI-TOF mass spectrometry. Biotechnol Adv. 2014;32:230–241.[PubMed][Google Scholar]