Skip to main content

Prevalence of Candida albicans in primary endodontic infections associated with a higher frequency of apical periodontitis in type two diabetes mellitus patients


To identify the prevalence of C. albicans in primary endodontic infections of type two diabetes mellitus (T2DM) patients and compare their clinical and radiographical characteristics with a non-diabetic control group, establishing the possible relationship between primary endodontic infection, T2DM, and C. albicans, since diabetes mellitus (DM), influences the development, course, and response to the treatment of apical periodontitis, but the presence of Candida albicans (C. albicans) has not been considered before. A total of 120 patients were selected and divided into two groups: 60 T2DM diagnosed patients and 60 non-diabetic controls. A clinical examination and radiographic analysis were performed to establish a periapical index score (PAI). Root canal samples were taken. Deoxyribonucleic acid (DNA) was extracted, and specific primers were used to identify C. albicans by polymerase chain reaction (PCR). A twofold increase in the prevalence of C. albicans in T2DM patients was observed in contrast to control patients (p = 0.0251). Sixty-five percent of T2DM patients with positive C. albicans scored a ≥ 3 PAI, while only 27% of the patients without C. albicans had a ≥ 3 PAI score (p = 0.0065). Long-term DM patients presented C. albicans more frequently (p < 0.0001). In this study, long-term T2DM patients carried C. albicans in their root canals more frequently when having a primary endodontic infection. Furthermore, this C. albicans presence seems to be related to a higher frequency of apical periodontitis.

This is a preview of subscription content, access via your institution.


  1. 1.

    Humphrey LL, Fu R, Buckley DI, Freeman M, Helfand M (2008) Periodontal disease and coronary heart disease incidence: a systematic review and meta-analysis. J Gen Intern Med 23:2079

    PubMed  PubMed Central  Google Scholar 

  2. 2.

    Rutger Persson G, Ohlsson O, Pettersson T, Renvert S (2003) Chronic periodontitis, a significant relationship with acute myocardial infarction. Eur Heart J 24:2108–2115

    CAS  PubMed  Google Scholar 

  3. 3.

    Khader YS, Ta’ani Q (2005) Periodontal diseases and the risk of preterm birth and low birth weight: a meta-analysis. J Periodontol 76:161–165

    PubMed  Google Scholar 

  4. 4.

    Scannapieco FA, Ho AW (2001) Potential associations between chronic respiratory disease and periodontal disease: analysis of National Health and Nutrition Examination Survey III. J Periodontol 72:50–56

    CAS  PubMed  Google Scholar 

  5. 5.

    Pepelassi E, Nicopoulou-Karayianni K, Archontopoulou AD, Mitsea A, Kavadella A, Tsiklakis K et al (2012) The relationship between osteoporosis and periodontitis in women aged 45–70 years. Oral Dis 18:353–359

    CAS  PubMed  Google Scholar 

  6. 6.

    Nibali L, Tatarakis N, Needleman I, Tu Y-K, D’Aiuto F, Rizzo M et al (2013) Association between metabolic syndrome and periodontitis: a systematic review and meta-analysis. J Clin Endocrinol Metab 98:913–920

    CAS  PubMed  Google Scholar 

  7. 7.

    Segura-Egea JJ, Martín-González J, Castellanos-Cosano L (2015) Endodontic medicine: connections between apical periodontitis and systemic diseases. Int Endod J 48:933–951

    CAS  PubMed  Google Scholar 

  8. 8.

    Pussinen PJ, Salomaa V (2018) Oral health: a neglected aspect of diabetes care. Lancet Diabetes Endocrinol 6:917–919

    PubMed  Google Scholar 

  9. 9.

    Manfredi M, McCullough MJ, Vescovi P, Al-Kaarawi ZM, Porter SR (2004) Update on diabetes mellitus and related oral diseases. Oral Dis 10:187–200

    CAS  PubMed  Google Scholar 

  10. 10.

    Correa FOB, Gonçalves D, Figueredo CMS, Bastos AS, Gustafsson A, Orrico SRP (2010) Effect of periodontal treatment on metabolic control, systemic inflammation and cytokines in patients with type 2 diabetes. J Clin Periodontol 37:53–58

    CAS  PubMed  Google Scholar 

  11. 11.

    Delamaire M, Maugendre D, Moreno M, Le Goff M, Allannic H, Genetet B (1997) Impaired leucocyte functions in diabetic patients. Diabet Med 14:29–34

    CAS  PubMed  Google Scholar 

  12. 12.

    Iacopino AM (2001) Periodontitis and diabetes interrelationships: role of inflammation. Ann Periodontol 6:125–137

    CAS  PubMed  Google Scholar 

  13. 13.

    Murrah VA (1985) Diabetes mellitus and associated oral manifestations: a review. J Oral Pathol Med 14:271–281

    CAS  Google Scholar 

  14. 14.

    Fotos PG, Hellstein JW (1992) Candida and candidosis. Epidemiology, diagnosis and therapeutic management. Dent Clin N Am 36:857–878

    CAS  PubMed  Google Scholar 

  15. 15.

    Lucas VS (1993) Association of psychotropic drugs, prevalence of denture-related stomatitis and oral candidosis. Community Dent Oral Epidemiol 21:313–316

    CAS  PubMed  Google Scholar 

  16. 16.

    Arendorf TM, Walker DM (1980) The prevalence and intra-oral distribution of Candida albicans in man. Arch Oral Biol 25:1–10

    CAS  PubMed  Google Scholar 

  17. 17.

    Willis AM, Coulter WA, Sullivan DJ, Coleman DC, Hayes JR, Bell PM et al (2000) Isolation of C. dubliniensis from insulin-using diabetes mellitus patients. J oral Pathol Med 29:86–90

    CAS  PubMed  Google Scholar 

  18. 18.

    Jacob LS, Flaitz CM, Nichols CM, Hicks MJ (1998) Role of dentinal carious lesions in the pathogenesis of oral candidiasis in HIV infection. J Am Dent Assoc 129:187–194

    CAS  PubMed  Google Scholar 

  19. 19.

    Pizzo G, Barchiesi F, Di Francesco LF, Giuliana G, Arzeni D, Milici ME et al (2002) Genotyping and antifungal susceptibility of human subgingival Candida albicans isolates. Arch Oral Biol 47:189–196

    CAS  PubMed  Google Scholar 

  20. 20.

    Sundqvist G (1994) Taxonomy, ecology, and pathogenicity of the root canal flora. Oral Surgery Oral Med Oral Pathol 78:522–530

    CAS  Google Scholar 

  21. 21.

    Siqueira JF, Sen BH (2004) Fungi in endodontic infections. Oral Surg Oral Med Oral Pathol Oral Radiol Endod 97:632–641.

    Article  PubMed  Google Scholar 

  22. 22.

    Baumgartner JC, Watts CM, Xia T (2000) Occurrence of Candida albicans in infections of endodontic origin. J Endod 26:695–698.

    CAS  Article  PubMed  Google Scholar 

  23. 23.

    Armada-Dias L, Breda J, Provenzano JC, Breitenbach M, Rôças I d N, Gahyva SMM et al (2006) Development of periradicular lesions in normal and diabetic rats. J Appl Oral Sci 14:371–375

    PubMed  PubMed Central  Google Scholar 

  24. 24.

    Fouad AF (2003) Diabetes mellitus as a modulating factor of endodontic infections. J Dent Educ 67:459–467

    PubMed  Google Scholar 

  25. 25.

    Fouad AF, Burleson J (2003) The effect of diabetes mellitus on endodontic treatment outcome: data from an electronic patient record. J Am Dent Assoc 134:43–51

    PubMed  Google Scholar 

  26. 26.

    Segura-Egea JJ, Castellanos-Cosano L, Machuca G, López-López J, Martín-González J, Velasco-Ortega E et al (2012) Diabetes mellitus, periapical inflammation and endodontic treatment outcome. Med Oral Patol Oral Cir Bucal 17:356–361.

    Article  Google Scholar 

  27. 27.

    Segura-Egea JJ, Jiménez-Pinzón A, Ríos-Santos JV, Velasco-Ortega E, Cisneros-Cabello R, Poyato-Ferrera M (2005) High prevalence of apical periodontitis amongst type 2 diabetic patients. Int Endod J 38:564–569

    CAS  PubMed  Google Scholar 

  28. 28.

    Ørstavik D, Kerekes K, Eriksen HM (1986) The periapical index: a scoring system for radiographic assessment of apical periodontitis. Dent Traumatol 2:20–34

    Google Scholar 

  29. 29.

    Dumani A, Yoldas O, Yilmaz S, Koksal F, Kayar B, Akcimen B et al (2012) Polymerase chain reaction of Enterococcus faecalis and Candida albicans in apical periodontitis from Turkish patients. J Clin Exp Dent 4:e34

    PubMed  PubMed Central  Google Scholar 

  30. 30.

    Belazi M, Velegraki A, Fleva A, Gidarakou I, Papanaum L, Baka D et al (2005) Candidal overgrowth in diabetic patients: potential predisposing factors. Mycoses 48:192–196

    PubMed  Google Scholar 

  31. 31.

    Möller AJ (1966) Microbiological examination of root canals and periapical tissues of human teeth. Methodological studies. Odontol Tidskr 74(Suppl-1)

  32. 32.

    Debelian GJ, Olsen I, Tronstad L (1997) Observation of Saccharomyces cerevisiae in blood of patient undergoing root canal treatment. Int Endod J 30:313–317

    CAS  PubMed  Google Scholar 

  33. 33.

    Hancock HH III, Sigurdsson A, Trope M, Moiseiwitsch J (2001) Bacteria isolated after unsuccessful endodontic treatment in a North American population. Oral Surgery Oral Med Oral Pathol Oral Radiol Endodontology 91:579–586

    Google Scholar 

  34. 34.

    Pinheiro ET, Gomes B, Ferraz CCR, Sousa ELR, Teixeira FB, Souza-Filho FJ (2003) Microorganisms from canals of root-filled teeth with periapical lesions. Int Endod J 36:1–11

    CAS  PubMed  Google Scholar 

  35. 35.

    Rôças IN, Jung I-Y, Lee C-Y, Siqueira JF (2004) Polymerase chain reaction identification of microorganisms in previously root-filled teeth in a South Korean population. J Endod:504–508

    PubMed  Google Scholar 

  36. 36.

    Cheung GSP, Ho MWM (2001) Microbial flora of root canal–treated teeth associated with asymptomatic periapical radiolucent lesions. Oral Microbiol Immunol 16:332–337

    CAS  PubMed  Google Scholar 

  37. 37.

    Peciuliene V, Reynaud AH, Balciuniene I, Haapasalo M (2001) Isolation of yeasts and enteric bacteria in root-filled teeth with chronic apical periodontitis. Int Endod J 34:429–434

    CAS  PubMed  Google Scholar 

  38. 38.

    Gomes CC, Guimarães LS, Pinto LCC, Camargo GA d CG, Valente MIB, Sarquis MI d M (2017) Investigations of the prevalence and virulence of Candida albicans in periodontal and endodontic lesions in diabetic and normoglycemic patients. J Appl Oral Sci 25:274–281

    CAS  PubMed  PubMed Central  Google Scholar 

  39. 39.

    Soysa NS, Samaranayake LP, Ellepola ANB (2006) Diabetes mellitus as a contributory factor in oral candidosis. Diabet Med 23:455–459

    CAS  PubMed  Google Scholar 

  40. 40.

    Tsang CSP, Chu FCS, Leung WK, Jin LJ, Samaranayake LP, Siu SC (2007) Phospholipase, proteinase and haemolytic activities of Candida albicans isolated from oral cavities of patients with type 2 diabetes mellitus. J Med Microbiol 56:1393–1398

    CAS  PubMed  Google Scholar 

  41. 41.

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

    CAS  PubMed  PubMed Central  Google Scholar 

  42. 42.

    Grimaudo NJ, Nesbitt WE, Clark WB (1996) Coaggregation of Candida albicans with oral Actinomyces species. Oral Microbiol Immunol 11:59

    CAS  PubMed  Google Scholar 

  43. 43.

    Grimaudo NJ, Nesbitt WE (1997) Coaggregation of Candida albicans with oral Fusobacterium species. Oral Microbiol Immunol 12:168–173

    CAS  PubMed  Google Scholar 

  44. 44.

    Bagg J, Silverwood RW (1986) Coagglutination reactions between Candida albicans and oral bacteria. J Med Microbiol 22:165–169

    CAS  PubMed  Google Scholar 

  45. 45.

    Jenkinson HF, Lala HC, Shepherd MG (1990) Coaggregation of Streptococcus sanguis and other streptococci with Candida albicans. Infect Immun 58:1429–1436

    CAS  PubMed  PubMed Central  Google Scholar 

  46. 46.

    Soll DR (2002) Candida commensalism and virulence: the evolution of phenotypic plasticity. Acta Trop 81:101–110

    PubMed  Google Scholar 

  47. 47.

    Darwazeh AMG, Lamey P-J, Samaranayake LP, MacFarlane TW, Fisher BM, Macrury SM et al (1990) The relationship between colonisation, secretor status and in-vitro adhesion of Candida albicans to buccal epithelial cells from diabetics. J Med Microbiol 33:43–49

    CAS  PubMed  Google Scholar 

  48. 48.

    Hill LV, Tan MH, Pereira LH, Embil JA (1989) Association of oral candidiasis with diabetic control. J Clin Pathol 42:502–505

    CAS  PubMed  PubMed Central  Google Scholar 

  49. 49.

    Mindiola MJ, Mickel AK, Sami C, Jones JJ, Lalumandier JA, Nelson SS (2006) Endodontic treatment in an American Indian population: a 10-year retrospective study. J Endod 32:828–832

    PubMed  Google Scholar 

  50. 50.

    Garner RE, Rubanowice K, Sawyer RT, Hudson JA (1994) Secretion of TNF-α by alveolar macrophages in response to Candida albicans mannan. J Leukoc Biol 55:161–168

    CAS  PubMed  Google Scholar 

  51. 51.

    Ashman RB, Papadimitriou JM (1995) Production and function of cytokines in natural and acquired immunity to Candida albicans infection. Microbiol Rev 59:646–672

    CAS  PubMed  PubMed Central  Google Scholar 

  52. 52.

    Dongari-Bagtzoglou A, Wen K, Lamster IB (1999) Candida albicans triggers interleukin-6 and interleukin-8 responses by oral fibroblasts in vitro. Oral Microbiol Immunol 14:364–370

    CAS  PubMed  Google Scholar 

  53. 53.

    Haynes K (2001) Virulence in Candida species. Trends Microbiol 9:591–596

    CAS  PubMed  Google Scholar 

  54. 54.

    Tajonar S-LY, Gustavo R, Sánchez-Mendieta KP, Martínez-Martínez RE, Domínguez-Pérez RA (2018) Periapical healing of endodontically treated teeth filled only in the apical third: a randomized controlled trial. Eur Endod J 3:24–30

    Google Scholar 

Download references


The authors wish to thank Dr. Adriana Lucia Arenas Pérez for her kind attention and to allow us to attend the clinic of Endodontics at the Centro Universitario de Estudios de Posgrado e Investigación, UMSNH to invite patients to participate in this study.

Statement of author contributions

R.D.T.L., R.A.D.P., A.L.G.N., M.E.R.A., R.M.P.S., and M.S.V.G. conceived and planned the idea; R.D.T.L., R.A.D.P., and M.E.R.A. collected the samples; R.A.D.P., A.L.G.N., J.L.A.H., and R.E.M.M. carried out the laboratory experiments; J.L.A.H., R.E.M.M., and M.E.R.A contributed to the interpretation of the results; R.A.D.P., A.L.G.N., R.M.P.S., and M.S.V.G analyzed the data; R.A.D.P. and M.S.V.G took the lead in writing the manuscript. All authors provided critical feedback and helped shape the research, analysis, and manuscript.

Author information



Corresponding author

Correspondence to Rubén Abraham Domínguez-Pérez.

Ethics declarations

An informed and voluntary written consent was obtained prior to clinical examination according to the ethical principles of the Declaration of Helsinki (version 2013). The protocol study was approved by the Ethical Committee of the dentistry department of the faculty.

Conflict of interest

The authors declare that they have no conflict of interest.

Additional information

Publisher’s note

Springer Nature remains neutral with regard to jurisdictional claims in published maps and institutional affiliations.

Rights and permissions

Reprints and Permissions

About this article

Verify currency and authenticity via CrossMark

Cite this article

De la Torre-Luna, R., Domínguez-Pérez, R.A., Guillén-Nepita, A.L. et al. Prevalence of Candida albicans in primary endodontic infections associated with a higher frequency of apical periodontitis in type two diabetes mellitus patients. Eur J Clin Microbiol Infect Dis 39, 131–138 (2020).

Download citation


  • Apical periodontitis
  • Candida albicans
  • Diabetes mellitus
  • Endodontics
  • Primary endodontic infection
  • Root canal treatment