Association between Candida species and periodontal disease: A systematic review

Document Type: Reviews

Authors

Department of Periodontics, Vydehi Institute of Dental Sciences and Research Center, Bangalore, India

Abstract

Periodontal diseases result in the inflammation of the supporting structures of the teeth, thereby leading to attachment loss and bone loss. One of the main etiological factors responsible for this condition is the presence of subgingival biofilms, comprising microorganisms, namely bacteria, viruses, and fungi. Candida species is one of the fungi reported to be found in periodontal disease which is suggestive of the presence of an association between these variables. The aim of this systematic review was to evaluate the association of Candida species with periodontal disease and determine the prevalence of these species in the patients affected with this disease.
The articles related to the subject of interest were searched in several databases, including the PubMed, Web of Science, Google Scholar Medline, Embase, Cochrane Library, and Scopus. The search process was accomplished using three keywords, namely ‘‘Candida species’’, ‘‘Chronic periodontitis’’, and ‘‘Gingivitis’’. All the identified studies were comprehensively evaluated for the association of Candida species with periodontal disease.
This systematic review included 23 articles, which assessed the prevalence of Candida species in periodontal diseases. The results of 21 studies were indicative of a positive association between Candida species and periodontal diseases. Accordingly, it was concluded that there is a strong association between the presence of Candida species and periodontal diseases.
 

Keywords


1. Dewhirst FE, Chen T, Izard J, Paster BJ, Tanner AC, Yu WH, et al. The human oral microbiome. J Bacteriol. 2010; 192(19):5002-17.
2. Ghannoum MA, Jurevic RJ, Mukherjee PK, Cui F, Sikaroodi M, Naqvi A, et al. Characterization of the oral fungal microbiome (mycobiome) in healthy individuals. PLoS Pathog. 2010; 6(1):e1000713.
3. Pfaller MA, Bale M, Buschelman B, Lancaster M, Espinel-Ingroff A, Rex JH, et al., Quality control guidelines for National Committee for Clinical Laboratory Standards recommended broth macrodilution testing of amphotericin B, fluconazole, and flucytosine. J Clin Microbiol. 1995; 33(5):1104-7.
4. Samaranayake LP, Mac-Farlane TW, Williamson MI. Comparison of Sabouraud dextrose and Pagano-Levin agar media for detection and isolation of yeasts from oral samples. J Clin Microbiol. 1987; 25(1):162-4.
5. Darveau RP. Periodontitis: a polymicrobial disruption of host homeostasis. Nat Rev Microbiol. 2010; 8(7):481-90.
6. Hajishengallis G, Darveau RP, Curtis MA. The keystone-pathogen hypothesis. Nat Rev Microbiol. 2012; 10(10):717-25.
7. Offenbacher S. Periodontal diseases: pathogenesis. Ann Periodontol. 1996; 1(1):821-78.
8. Canabarro A, Valle C, Farias MR, Santos FB, Lazera M, Wanke B. Association of subgingival colonization of Candida albicans and other yeasts with severity of chronic periodontitis. J Periodontal Res. 2013; 48(4):428-32.
9. Kornman KS. Diagnostic and prognostic tests for oral diseases: practical applications. J Dent Educ. 2005; 69(5):498-508.
10. Lamster IB, Grbic JT, Mitchell‐Lewis DA, Begg MD, Mitchell A. New concepts regarding the pathogenesis of periodontal disease in HIV infection. Ann Periodontol. 1998; 3(1);62-75.
11. Needleman IG. A guide to systematic reviews. J Clin Periodontol. 2002; 29(Suppl 3):6-9.
12. Von Elm E, Altman DG, Egger M, Pocock SJ, Gøtzsche PC, Vandenbroucke JP. The strengthening the reporting of observational studies in epidemiology (STROBE) statement: guidelines for reporting observational studies. Ann Intern Med. 2007; 147(8):573-7.
13. Teles R, Teles F, Frias-Lopez J, Paster B, Haffajee A. Lessons learned and unlearned in periodontal microbiology. Periodontol 2000. 2013; 62(1):95-162.
14. Reynaud AH, Nygaard-Østby B, Bøygard GK, Eribe ER, Olsen I, Gjermo P. Yeasts in periodontal pockets. J Clin Periodontol. 2001; 28(9):860-4.
15. Grimaudo NJ, Nesbitt WE. Coaggregation of Candida albicans with oral Fusobacterium spp. Oral Microbiol Immunol. 1997; 2(3):168-73.
16. Jabra-Rizk MA, Falkler WA Jr, Merz WG, Kelley JI, Baqui AA, Meiller TF. Coaggregation of Candida dubliniensis with Fusobacterium nucleatum. J Clin Microbiol. 1999; 37(5):1464-8.
17. Takahashi N. Microbial ecosystem in the oral cavity: Metabolic diversity in an ecological niche and its relationship with oral diseases. Int Congr Ser. 2005; 1284:103-12.
18. Joshi PS, Joshi SG, Gedam R. Isolation of Candida albicans from subgingival plaque in patients with chronic periodontitis- a microbiological study. Int J Sci Res. 2013; 2(2):268-70.
19. De-La-Torre J, Quindós G, Marcos-Arias C, Marichalar-Mendia X, Gainza ML, Eraso E, et al. Oral Candida colonization in patients with chronic periodontitis. Is there any relationship? Rev Iberoam Micol. 2018; 35(3):134-9.
20. Popova C, Dosseva-Panova V, Kisselova-Yaneva A, Panov V. Subgingival microbiota in severe chronic periodontitis. J IMAB Ann Proc. 2014; 20(3):554-7.
21. Semprebom AM, Isidoro AC, Machado MA, Campelo PM, Hofling JF, Samaranayake LP, et al. Enhanced susceptibility of Candida albicans to chlorhexidine under anoxia. Braz J Oral Sci. 2009; 8:105-10.
22. Lourenço AG, Ribeiro AE, Nakao C, Motta AC, Antonio LG, Machado AA, et al. Oral Candida spp carriage and periodontal diseases in HIV-infected patients in Ribeirão Preto, Brazil. Rev Inst Med Trop São Paulo. 2017; 59:e29.
23. Blignaut E, Phiri R. Prevalence and genotypes of Candida Albicans from necrotising periodontal disease and the tongue. Int J Oral Dent Health. 2017; 3:38.
24. Järvensivu A, Hietanen J, Rautemaa R, Sorsa T, Richardson M. Candida yeasts in chronic periodontitis tissues and subgingival microbial biofilms in vivo. Oral Dis. 2004; 10(2):106-12.
25. Urzúa B, Hermosilla G, Gamonal J, Morales-Bozo I, Canals M, Barahona S, et al. Yeast diversity in the oral microbiota of subjects with periodontitis: Candida albicans and Candida dubliniensis colonize the periodontal pockets. Med Mycol. 2008; 46(8):783-93.
26. Javed F, Klingspor L, Sundin U, Altamash M, Klinge B, Engstrom PE. Periodontal conditions, oral Candida albicans and salivary proteins in type 2 diabetic subjects. BMC Oral Health. 2009; 9:12.
27. Cuesta AI, Jewtuchowicz V, Brusca MI, Nastri ML, Rosa AC. Prevalence of Staphylococcus spp. and Candida spp. in the oral cavity and periodontal pockets of periodontal disease patients. Acta Odontol Latinoam. 2010; 23(1):20-6.
28. Melton JJ, Redding SW, Kirkpatrick WR, Reasner CA, Ocampo GL, Venkatesh A, et al. Recovery of Candida dubliniensis and other Candida spp. from the oral cavity of subjects with periodontitis who had well-controlled and poorly controlled type 2 diabetes: a pilot study. Spec Care Dent. 2010; 30(6):230-4.
29. Sardi JC, Cruz GA, Höfling JF, Duque C, Gonçalves RB. Genetic and phenotypic evaluation of Candida albicans strains isolated from subgingival biofilm of diabetic patients with chronic periodontitis. Med Mycol. 2012; 50(5):467-75.
30. McManus BA, Maguire R, Cashin PJ, Claffey N, Flint S, Abdulrahim MH, et al. Enrichment of multilocus sequence typing clade 1 with oral Candida albicans isolates in patients with untreated periodontitis. J Clin Microbiol. 2012; 50(10):3335-44.
31. Al Mubarak S, Robert AA, Baskaradoss JK, Al-Zoman K, Al
Sohail A, Alsuwyed A, et al. The prevalence of oral Candida infections in periodontitis patients with type 2 diabetes mellitus. J Infect Public Health. 2013; 6(4):296-301.
32. Joshi PR, Gedam R, Joshi SG, Hongal BP. Study of oral manifestations & isolation of Candida Albicans from Subgingival plaque of patients with or without diabetes mellitus using staining and culture method. Int J Dent Med Res. 2014; 1(4):6-16.
33. Chezhian N, Geetha RV. Prevalence of oral candidiasis in periodontal patients with diabetes. J Pharm Sci Res. 2015; 7(9):767-8.
34. Venkatesan G, Uppoor A, Naik D, Kadkampally D, Maddi A. Oral Candida carriage and morphotype differentiation in chronic periodontitis patients with and without diabetes in the Indian Sub-Continent. Dent J. 2015; 3(4):123-31.
35. Arumugam M. A Comparative evaluation of subgingival occurrence of Candida species in chronic periodontitis and peri-implantitis. A clinical and microbiological study. Int J Clin Implant Dent. 2015; 1(3):95-100.
36. Arumugam M, Seshan H, Hemanth B. A comparative evaluation of subgingival occurrence of Candida species in periodontal pockets of female patients using hormonal contraceptives and non-users–A clinical and microbiological study. Oral Health Dent Manag. 2015; 14(4):206-11.
37. Babitha GA, Aditya V, Prakash S, Suresh K, Bhat KG. Candida albicans: can it be a periodontal pathogen? Int J Adv Res. 2018; 6:1216-25.
38. Bhalla DN, Veena HR, Patil SR, Chaitra KR. The consortium of Candida spp. in the subgingival microbiota of type 2 diabetics with chronic periodontitis - a case control study. Int J Sci Res. 2018; 7(2):63-6.
39. Lingaiah U, Latha S, Shankaregowda AM, Lakshminara-simahaiah V, Krishna SA, Virupaksha VL. Association of oral candidal carriage, candidiasis and periodontal disease with the degree of glycemic control in Type I and Type II diabetes mellitus. Int J Prev Clin Dent Res. 2018; 5(1):55-8.
40. Matic Petrovic M, 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(1):e021