Skip to main content
NCBI home page
Current Medical Mycology logoLink to Current Medical Mycology
. 2020 Jun;6(2):63–68. doi: 10.18502/CMM.6.2.3420

Association between Candida species and periodontal disease: A systematic review

Anjana Suresh Unniachan 1*, Nisha Krishnavilasom Jayakumari 1, Shruthi Sethuraman 1
PMCID: PMC7888513  PMID: 33628985

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: Dental plaque, Periodontal pockets, Yeasts

Introduction

he human oral cavity remains to be the most important microbial gateway that harbors a wide variety of environmental microorganisms, mostly bacteria, in addition to fungi, protozoa, and viruses [ 1 ]. This complex microbiome is comprised of an estimated 600 bacterial species [ 1 ] and 100 fungal species [ 2 ]. Among the human fungi species, the members of Candida are the most frequently recovered ones. Candidosis or candidiasis caused by Candida albicans is considered the most common fungal infection of the human oral cavity. Nonetheless, candidiasis caused by non-albicans Candida species, such as C. tropicalis, C. parapsilosis, C. krusei, C. glabrata, and C. dubliniensis, are also becoming common among certain groups of patients [ 3 ]. Candida has the ability to form multispecies biofilms; therefore, it is considered a well-known human and animal pathogen that causes polymicrobial diseases [ 4 ].

Periodontitis is one of the earliest human diseases recognized to be associated with mixed-species biofilms. Periodontal disease, or periodontitis, is a chronic inflammatory disease of the periodontium, which comprises of the tissues that surround and support the teeth [ 5 ]. It is caused by a synergistic and dysbiotic dental plaque microbial community, with such keystone pathogens as Porphyromonas gingivalis, initiating the disruption of tissue homeostasis [ 6 ]. This dental “plaque biofilm” consists of a multitude of microorganisms, including bacteria, fungi, and possibly viruses [ 7 ]. Several studies have reported increased subgingival colonization by yeasts, particularly C. albicans, in chronic periodontitis patients, compared to that in periodontally healthy subjects [ 8 ].

The colonization and proliferation of Candida species in the oral mucosa and periodontal pockets are facilitated by the virulence factors they possess. With bacterial species, such as Porphyromonas gingivalis, Tannerella forsythia, and Aggregatibacter actinomycetemcomitans being the most frequently associated periodontal pathogens, the evidence for yeast involvement in periodontal disease remains to be scarce [ 9 ]. The fungi may act directly, in conjunction with subgingival bacterial pathogens, or as a cofactor by inducing the production of pro-inflammatory cytokines, which increase the occurrence of periodontal attachment loss and as a result lead to the occurrence of periodontal disease [ 10 ].

Systematic reviews are designed to assemble, appraise, and make sense of the totality of the evidence available as far as possible [ 11 ]. To the best of our knowledge, no previous systematic review has investigated the role of Candida in periodontal disease. Therefore, the aim of this systematic review was to critically and comprehensively evaluate the presence of Candida species in periodontal disease.

Materials and Methods

Search strategies

The studies evaluating the presence of Candida species in periodontal diseases from September 2003 to January 2019 were searched in several databases, including the PubMed, Web of Science, Google Scholar, Medline, Embase, Cochrane Library, and Scopus. The search was restricted to original articles that were published in English language and addressed the presence of Candida species in periodontal disease. The search process was performed considering the following keywords in the medical subject headings, titles, or abstracts of the articles: "Candida species", "Chronic periodontitis", and "Gingivitis".

The bibliographies of the retrieved articles were also searched for additional references. The titles of the identified articles were examined closely in order to determine the eligibility of the paper to be included in this review. In addition, the references from the selected articles were examined as a further search tool. All papers the keywords of which were present in their titles or abstracts were used in the initial list, and other unrelated articles were eliminated.

Inclusion criteria

There was no time restriction for the selection of the articles for the review process. All sources which could give us the relevant data for our systematic review were included in the study. In this regard, all original articles addressing the prevalence or presence of Candida species in periodontal diseases were considered. The selection of the articles for review was completed based on three stages, involving the examination of: a) titles, b) abstracts, and c) full texts.

The articles which fulfilled the STROBE checklist was finally considered for the review. The quality of the studies was assessed according to the variables related to study objectives, study population characteristics, inclusion and exclusion criteria, and data collection method. The validity, explicit findings, and appropriate data analysis methods of the studies were also assessed (low quality<10.5, moderate quality=10.6-16.5, and high quality=16.6-22) [ 12 ].

Exclusion criteria

The exclusion criteria included: 1) data insufficiency, 2) non-epidemiological type, 3) investigation of the presence of Candida species in diseases other than periodontal diseases, 4) publication in languages other than English, and 5) duplication.

Data extraction

The data extracted from the reviewed articles included the name of the first author, year of publication, study location, and sample size, sample age, screening method, specimens, presence of Candida species, and virulence factors. The abstract and full-text version of the articles were reviewed independently by two authors. In cases of facing any discordance, the papers were reviewed jointly until the differences were resolved.

Results

The search process in the Google Scholar, PubMed, and Scopus databases resulted in the identification of a total of 105 studies. After the removal of duplicate papers, 85 studies remained. In the next stage, 39 cases were excluded following the initial evaluation given the irrelevancy of the titles or topics. Consequently, 46 studies were found to be eligible for the evaluation of the abstract out of which 6 cases were again excluded as the full-text version was not accessible. Then, after the full-text evaluation of the remaining 40 studies, only 23 cases, satisfying the inclusion criteria, were included in the systematic review (Figure 1). The mean score of the STROBE scale obtained for the included studies was 13.8, indicating a moderate quality. The characteristics of the 23 included studies are summarized in Table 1.

Figure 1.

Figure 1

Open in a new tab

Flow diagram describing the different phases of this systematic review

Table 1.

List of studies included in this systematic review

Serial No. First author Year Country Sample size Number of groups Age Type of disease Specimen Methods of identification Species identified
1 Ja¨rvensivu et al. [24] 2004 Finland 25 1 NS CP Subgingival plaque, epithelial, connective tissue sample PCR C. albicans (16%) C. albicans (16%)
2 Urzua et al. [24] 2008 Chile 74 3 20-40 years CP, AP, PH* Subgingival plaque, saliva Biochemical and CHROMagar Candida C. albicans (87.5%), C. dubliniensis (8.4%), C. glabrata (2.6%)
3 Javed et al. [25] 2009 Pakistan 58 1 45-60 years CP with diabetes Tongue surface scraping PCR C. albicans (50%)
4 Alicia et al. [26] 2010 Argentina 82 2 18-70 years Gingivitis, CP Subgingival plaque CHROMagar Candida Gingivitis-Candida spp. (57.7%), CP- Candida spp. (53.6%)
5 Melton et al. [27] 2010 Mexico 30 2 NS CP with controlled and uncontrolled diabetes Saliva, subgingival plaque CHROMagar Candida CP with controlled diabetes-C. albicans(33%),C. glabrata (13%),C. parapsilosis(0%), C. tropicalis (0%)
CP with uncontrolled diabetes - C.albicans(53%),C. glabrata (20%), C. parapsilosis(6%), C. tropicalis (6%)
6 Sardi et al. [28] 2012 Brazil 11 1 31-68 years CP with diabetes Subgingival plaque PCR C. albicans- 63.3%
7 Mcmanus et al. [29] 2012 Ireland 71 2 21-67 years CP, PH Subgingival plaque CHROMagar Candida CP-C. albicans (47.6%), C. dubliniensis(23.8%),C. parapsilosis (1%), C. keyfr (1%), PH-C.albicans (32%), C. glabrata(1%)
8 Almubarak et al. [30] 2013 Saudi Arabia 42 1 21-70 years CP with diabetes Subgingival plaque CHROMagar Candida C. albicans-38%, C. dubliniensis(9.5), C.tropicalis (4.7%), C. glabrata(4.7%)
9 Canabarro et al. [8] 2013 Brazil 60 2 31-67 years CP, PH Subgingival plaque Biochemical CP-30% Candida-positive(C.albicans-12, C. parapsilosis-2, C. dubliniensis-1, C.tropicalis-1) PH-15% Candida-positive(C.albicans-3)
10 Joshi PS et al. [17] 2013 India 80 2 40-60 years CP, PH Subgingival plaque Biochemical C. albicans-7.5%
11 Joshi PS et al. [31] 2014 India 80 2 40-60 years CP,CP with diabetes Subgingival plaque Biochemical CP-C. albicans(90%), CP with Diabetes-C. albicans(7.5%)
12 Popova et al. [19] 2014 Bulgaria 20 1 NS CP Subgingival plaque PCR No-Candida spp. was isolated
13 Chezian N et al. [32] 2015 India 30 1 35-70 years CP with diabetes Subgingival plaque Sabouraud agar C. albicans-40%
14 Venkatesan et al. [33] 2015 India 30 2 40-60 years CP , CP with diabetes Whole saliva Biochemical tests CP- Candida spp.(13%) CP with diabetes-Candida spp.(60%)
15 Arumugam et al. [36] 2015 India 40 2 30.12, 36.71 CP, peri-implatitis Subgingival plaque CHROMagar Candida CP-C. albicans (14.6%), C. tropicalis(2.4%), C. dubliniensis (4.9%), C. krusei(4.9%), C.glabrata (0%), C. parapsilosis(0%)
Periimplantitis- C. albicans (19.5%), C. tropicalis (4.9%), C. glabrata (2.4%), C. parapsilosis(2.4%), C. dubliniensis (0%), C. krusei (0%),
16 Arumugam et al. [36] 2015 India 82 2 19-45 years CP,CP with patient’s using hormonal contraceptives (HC) Subgingival plaque CHROMagar Candida CP with HC-C. albicans-54.5%,C.tropicalis-9.1%, C. krusei-18.2%, C. parapsilosis-0%,C.dubliniensis-18.2%, C. glabrata-0%
CP-C. albicans-66.7%,C.tropicalis-16.7%,C.krusei-0%, C. parapsilosis-8.3%,C.dubliniensis-0%, C. glabrata-8.3%
17 Babitha et al. [36] 2017 India 30 3 25-50 years CP,AP,PH Subgingival plaque PCR All the groups in all samples C. albicans was isolated
18 Lourenco et al. [22] 2017 Brazil 73 2 NS Non-HIV infected periodontally healthy, non-HIV infected periodontally affected, HIV-infected periodontally healthy, HIV-infected periodontally affected Saliva CHROMagar Candida Non HIV periodontally healthy- C.albicans-58%,C. tropicalis-16.7%, C. krusei-0%,C. parapsilosis-25%, C. dubliniensis-0%,C. glabrata-0%
Non HIV periodontally affected- C.albicans-61%,C. tropicalis-16.7%, C. krusei-0%,C. parapsilosis-15%, C. dubliniensis-0%, C. glabrata-0%
HIV periodontally healthy- C.albicans-58%,C. tropicalis-5%, C. krusei-0%, C. parapsilosis-5%, C. dubliniensis-0%, C. glabrata-0%
HIV periodontally affected- C.albicans-79%,C. tropicalis-7%, C. krusei-7%, C.parapsilosis-7%,C. dubliniensis-3%, C. glabrata-10%
19 Blignaut et al. [23] 2017 Pretoria 87 1 NS Necrotizing periodontal disease Tongue swab CHROMagar Candida C. albicans-54%
20 Bhalla et al. [38] 2018 India 45 3 24-65 years CP, PH, CP with diabetes Subgingival plaque Biochemical PH-0%, CP-Non-C. albicans(40%), CPwith DM- Non-C. albicans(25%)
21 Lingaiah et al. [39] 2018 India 100 2 NS CP with type I and CP with type II diabetes Whole saliva Sabouraud agar CP with type 1-Candida spp. (48.1%)
CP with type 2- Candida spp. (51.9%)
22 De la Torre et al. [19] 2018 Spain 155 3 30-80 years CP, PH Oral rinse, subgingival plaque CHROMagar Candida CP-OR-C. albicans (42%), Non C.albicans(16.1%)
Plaque- C. albicans (28.5%), Non C.albicans (12.5%)
23 Petrovic et al. [40] 2019 Serbia 146 4 NS PH, CP, CP with controlled and uncontrolled diabetes Tongue swab, subgingival plaque CHROMagar Candida and biochemical PH-tongue swab (22.2%), Plaque sample(41.6%)
CP-tongue swab (16.7%), Plaque sample(26.2%)
CP with controlled diabetes-tongue swab (21.5%), Plaque sample (53.5%)
CP with uncontrolled diabetes - tongue swab (47.5%), Plaque sample(72.5%)
Open in a new tab

*CP: chronic periodontitis, AP: aggressive periodontitis, PH: physically Healthy

Out of 23 studies, 10 and 3 cases had been performed on diabetic and human immunodeficiency virus (HIV)-infected patients, respectively. The remaining 10 studies had been conducted on systemically healthy periodontitis patients. However, out of these studies, on and two manuscripts had also addressed aggressive periodontitis and peri-implantitis, respectively. The age groups of the investigated patients were ≤ 50 and > 50 years in 4 and 12 papers, respectively. However, the age group of the study population was not mentioned in the remaining 7 studies. Regarding sampling, in the majority of the studies (n=18), subgingival plaque was used as the specimen for analysis. However, whole saliva (n=4), oral rinse (n=1), and tongue swab (n=3) were also applied in other studies. Furthermore, with regard to the applied method for organism identification, the majority of the studies used agar or biochemical tests rather than polymerase chain reaction (PCR), which is expensive. Accordingly, PCR was used in only five studies. The results of 22 studies (out of 23 cases) revealed an increased number of Candida species in patients with chronic periodontitis, compared to that in healthy subjects, thereby establishing the possibility of the role of this species in periodontal disease.

Discussion

Periodontal disease has a polymicrobial etiology. The development of periodontal disease requires the presence of a susceptible host, along with the presence of bacterial plaque. Accordingly, some individuals consider periodontopathogenic bacteria as “required but not sufficient” to cause periodontal disease. However, no disease process results from a single isolated cause or event (i.e., no cause is necessary and sufficient by itself to result in a disease) [ 13 ].

The opportunistic fungus C. albicans has a preponderant role among other species of its genus in periodontal disease. The presence of its hyphae has been demonstrated in the connective tissue of periodontal patients in association with highly invasive anaerobic bacteria, such as Porphyromonas gingivalis, Prevotella intermedia, and Aggregatibacter actinomycetemcomitans [ 14 ].

The exact pathogenic mechanism by which Candida species contribute to the progression of periodontal disease is not still known. However, this has been attributed to the known virulent properties of these species, like adhesion, dimorphism, invasion, and biofilm formation. The ability of these species to coaggregate with the periodontal pathogen is also one of the main proposed pathogenic mechanisms. Candida albicans colonizes the oral cavity, presenting the commensal or pathogenic properties that can be modified by direct or indirect interactions with different types of bacteria, depending on the localization of the microbial communities (e.g., supragingival plaque, subgingival plaque, and tongue coating).

Candida albicans coaggregates with an obligatory anaerobe F. nucleatum [ 15 ] with the engagement of a mannose receptor on the C. albicans surface [ 16 ]. Recent studies have also shown that C. albicans is able to interact with the keystone pathogen of subgingival plaque, P. gingivalis, and obligatory anaerobe. However, it is difficult to judge whether the pathogens apply a synergistic or concurrence style of interactions [ 17 ]. The aim of this systematic review was to evaluate the association between the presence of Candida species and periodontal diseases. The obtained results revealed a significantly strong positive correlation between the presence of Candida species and periodontal diseases.

Joshi et al. stated that C. albicans would have a role in the infrastructure of periodontal microbial plaque, as well as in the adherence of this species to the periodontal tissues [ 18 ]. In a study conducted by De la Toree et al., chronic periodontitis patients were reported to have a higher Candida colonization rate than those without chronic periodontitis. However, they were unable to confirm a statistically significant relationship between the colonization of Candida and the severity of chronic periodontitis [ 19 ].

In a study carried out by Popova et al. (2014), no Candida species was observed in patients with chronic periodontitis. Therefore, among the studies reviewed in the present study, the mentioned study was the only case showing a negative correlation [ 20 ]. Out of the 23 included studies, 10 papers involved the evaluation of the presence of Candida species in subgingival microbiota in the patients diagnosed with type I, type II, well-controlled, and poorly controlled diabetes. The results of these studies showed a positive correlation. Diabetic patients have a higher prevalence of C. albicans in the form of subgingival biofilm in the oral cavity, specifically in the periodontal pockets. This could indicate the co-participation of this species in the progression of periodontal disease [ 21 ]. Two of the included studies had been performed on HIV-positive individuals and introduced periodontal disease as a possible factor responsible for the increase in commensal Candida species count in HIV-infected patients [ 22 ].

Furthermore, another study included in this review had been performed on HIV-positive individuals with necrotizing periodontal disease. In the mentioned study, tongue swabs were used to investigate the presence of Candida species. The results were suggestive of no association between C. albicans and necrotizing periodontal disease. This may be due to the dynamics of the acute inflammatory environment, with an abundance of necrotic, desquamating tissue, associated bleeding, and mediators of acute inflammation, which is not conducive to the undisturbed colonization, replication, and biofilm formation by C. albicans [ 23 ].

During our search for the articles for systematic review, no study was found to assess the effect of periodontal treatment on this opportunistic fungus. The results of all the reviewed studies were suggestive of a positive correlation between the presence of Candida species and periodontal diseases; however, the exact pathogenic mechanism is still unknown.

Conclusion

Based on the results of the reviewed papers, it can be concluded that there is a strong association between the presence of Candida species and periodontal diseases. However, further research should be undertaken in this field/area to establish the exact pathogenic mechanism of this opportunistic fungus in periodontal diseases and also confirm the results using a long-term follow-up by evaluating the effect of periodontal treatment on this opportunistic fungus.

Acknowledgement

We would like to acknowledge the Department of Periodontics and Public Health Dentistry for all their support and guidance.

Author’s contribution

All authors were involved in data collection, manuscript drafting, and manuscript revision. Furthermore, they uniformly approved the submission of the manuscript.

Conflict of Interest: There is no conflict of interest.

Financial disclosure:No external funding was received for this study.

References

  • 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. doi: 10.1128/JB.00542-10. [DOI] [PMC free article] [PubMed] [Google Scholar]
  • 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. doi: 10.1371/journal.ppat.1000713. [DOI] [PMC free article] [PubMed] [Google Scholar]
  • 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. doi: 10.1128/jcm.33.5.1104-1107.1995. [DOI] [PMC free article] [PubMed] [Google Scholar]
  • 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. doi: 10.1128/jcm.25.1.162-164.1987. [DOI] [PMC free article] [PubMed] [Google Scholar]
  • 5.Darveau RP. Periodontitis: a polymicrobial disruption of host homeostasis. Nat Rev Microbiol. 2010; 8(7):481–90. doi: 10.1038/nrmicro2337. [DOI] [PubMed] [Google Scholar]
  • 6.Hajishengallis G, Darveau RP, Curtis MA. The keystone-pathogen hypothesis. Nat Rev Microbiol. 2012; 10(10):717–25. doi: 10.1038/nrmicro2873. [DOI] [PMC free article] [PubMed] [Google Scholar]
  • 7.Offenbacher S. Periodontal diseases: pathogenesis. Ann Periodontol. 1996; 1(1):821–78. doi: 10.1902/annals.1996.1.1.821. [DOI] [PubMed] [Google Scholar]
  • 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. doi: 10.1111/jre.12022. [DOI] [PubMed] [Google Scholar]
  • 9.Kornman KS. Diagnostic and prognostic tests for oral diseases: practical applications. J Dent Educ. 2005; 69(5):498–508. [PubMed] [Google Scholar]
  • 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. doi: 10.1902/annals.1998.3.1.62. [DOI] [PubMed] [Google Scholar]
  • 11.Needleman IG. A guide to systematic reviews. J Clin Periodontol. 2002; 29(Suppl 3):6–9. doi: 10.1034/j.1600-051x.29.s3.15.x. [DOI] [PubMed] [Google Scholar]
  • 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. doi: 10.7326/0003-4819-147-8-200710160-00010. [DOI] [PubMed] [Google Scholar]
  • 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. doi: 10.1111/prd.12010. [DOI] [PMC free article] [PubMed] [Google Scholar]
  • 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. doi: 10.1034/j.1600-051x.2001.028009860.x. [DOI] [PubMed] [Google Scholar]
  • 15.Grimaudo NJ, Nesbitt WE. Coaggregation of Candida albicans with oral Fusobacterium spp. Oral Microbiol Immunol. 1997; 2(3):168–73. doi: 10.1111/j.1399-302x.1997.tb00374.x. [DOI] [PubMed] [Google Scholar]
  • 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. doi: 10.1128/jcm.37.5.1464-1468.1999. [DOI] [PMC free article] [PubMed] [Google Scholar]
  • 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. [Google Scholar]
  • 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. [Google Scholar]
  • 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. doi: 10.1016/j.riam.2018.03.005. [DOI] [PubMed] [Google Scholar]
  • 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. [Google Scholar]
  • 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. [Google Scholar]
  • 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. doi: 10.1590/S1678-9946201759029. [DOI] [PMC free article] [PubMed] [Google Scholar]
  • 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. [Google Scholar]
  • 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. doi: 10.1046/j.1354-523x.2003.00978.x. [DOI] [PubMed] [Google Scholar]
  • 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. doi: 10.1080/13693780802060899. [DOI] [PubMed] [Google Scholar]
  • 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. doi: 10.1186/1472-6831-9-12. [DOI] [PMC free article] [PubMed] [Google Scholar]
  • 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. [PubMed] [Google Scholar]
  • 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. doi: 10.1111/j.1754-4505.2010.00159.x. [DOI] [PubMed] [Google Scholar]
  • 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. doi: 10.3109/13693786.2011.633233. [DOI] [PubMed] [Google Scholar]
  • 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. doi: 10.1128/JCM.01532-12. [DOI] [PMC free article] [PubMed] [Google Scholar]
  • 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. doi: 10.1016/j.jiph.2012.12.007. [DOI] [PubMed] [Google Scholar]
  • 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. [Google Scholar]
  • 33.Chezhian N, Geetha RV. Prevalence of oral candidiasis in periodontal patients with diabetes. J Pharm Sci Res. 2015; 7(9):767–8. [Google Scholar]
  • 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. doi: 10.3390/dj3040123. [DOI] [PMC free article] [PubMed] [Google Scholar]
  • 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. [Google Scholar]
  • 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. [Google Scholar]
  • 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. [Google Scholar]
  • 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. [Google Scholar]
  • 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. [Google Scholar]
  • 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. doi: 10.1371/journal.pone.0210527. [DOI] [PMC free article] [PubMed] [Google Scholar]

Articles from Current Medical Mycology are provided here courtesy of Mazandaran University of Medical Sciences

RESOURCES