Epidemiological factors associated with Candida albicans in patients using complete denture: A scoping review


Dentistry School, Federal University of Alfenas, Alfenas, Minas Gerais, Brazil
Dentistry School, State University of Campinas, Campinas, São Paulo, Brazil
Regional Board of Brasília, Oswaldo Cruz Fundation (Fiocruz Brasília), Brasilia, DF, Brazil

Abstract

Objective: This study undertakes a scoping review of research on epidemiological factors of Candida albicans in patients using complete denture (CD). Methods: PubMed, LILACS, Embase, SciELO, Web of Science, and Scopus databases were used. Searches were conducted in December 2020. Keywords used in this search were Candida albicans, Complete Denture, Mouth, and Microbiology. Results: Initially, 89 articles were identified; 19 of these comprised the final sample after applying the exclusion/inclusion criteria. There was a greater tendency for females to use DC. In addition, among all samples evaluating the incidence of the fungus (n = 2,724), approximately 44.7% (n = 1,218) had C. albicans-associated prosthetic stomatitis. Conclusion: Prosthetic stomatitis is a condition that mainly affects women aged 50–70 years and has a multifactorial predisposition. Also, Newton's classification proposed in 1962 is the most used for the clinical diagnosis of oral candidiasis. The CD's hygiene status is a crucial factor for the progression of candidosis, in the same way that the C. albicans fungus plays an important role in the progression of this pathogenesis in the host.

Keywords: Candida albicans, complete denture, mouth, microbiology

Keywords

Candida albicans, complete denture, mouth, microbiology

General information

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

*Corresponding author:

Faculdade de Odontologia, Universidade Federal de Alfenas

End.: Rua Gabriel Monteiro da Silva, 700. Centro. Alfenas, MG, Brasil | CEP 37.130-003

Fone: (35) 3299-1425

The study was carried out at the Federal University of Alfenas (UNIFAL)

https://doi.org/10.21876/rcshci.v11i1.1050

Introduction

According to data presented by the World Health Organization (WHO) in 2005, it is estimated that approximately 25% of the world population over sixty years of age have total edentulism1. In this context, the rehabilitation treatment that presents a satisfactory performance, a pleasant aesthetic, low cost, and acceptable durability for the total edentulous patients is the complete denture (CD)2, 3. The use of CDs without the correct instructions on their use or hygiene can cause opportunistic diseases such as prosthetic stomatitis, which may significantly drop in the quality of life of patients when speaking or chewing4, 5.

In this regard, several epidemiological investigations have shown that approximately two-thirds of patients using CDs may present prosthetic stomatitis2, 6, 7. This type of lesion can be characterized by an intense inflammatory process in the supporting soft tissues, but it is clinically asymptomatic. However, some patients may present with symptomatic clinical conditions related to this condition, such as burning, itching, or pain8, 9, 10.

Clinical research has correlated the association between the colonization of Candida spp. in CD, since these microorganisms have high adherence abilities, which establishes a favorable environment for their growth, strict relationships with dimorphism between species, and secretion/production of enzymes such as phospholipase and proteinases. Those enzymes are important mediators of virulence to the host, thus contributing to the formation of a pathogenic biofilm that is firmly adhered between the acrylic resin surface and oral mucosa7, 9, 11, 12, 13. Despite that, several researchers have linked its incidence to multifactorial conditions; therefore, it is necessary to understand its characteristics and ways to contribute to the onset of this comorbidity6, 7, 10.

Thus, a scoping review was conducted to map the research done in this area and identify any existing gaps in knowledge about Candida albicans in patients using complete dentures. The following research question was formulated: What is known from the literature about epidemiological factors associated with C. albicans in patients using complete dentures? What are the literature articles in a twenty-year retrospective? Who evaluated the epidemiological profiles of C. albicans in patients using complete denture in several countries?

Methods

This scoping review was conducted following the Preferred Reporting Items for Systematic reviews and Meta-Analyses extension for Scoping Reviews (PRISMA-ScR).

Focused question

The focused question was proposed by following the PECO principles. The key established question was "What are the literature articles in a twenty-year retrospective who evaluated the epidemiological profiles of C. albicans in patients using complete denture in several countries?".

Search strategy

This research is a critical review of the literature, in which the following descriptors from the Medical Subject Headings (MeSH) and Descriptors in Health Sciences (DeCS) were used: "Candida albicans"[All Fields] AND "complete denture"[All Fields] AND "Mouth"[All Fields] AND "Microbiology"[All Fields]. The search was performed in PubMed, LILACS, SciELO, Web of Science, Embase, and Scopus databases until December 202014.

Study selection and data extraction 

Duplicates were removed using EndNote™ X7 software (Thomson Reuters, New York, NY, USA). This study included research conducted between 2000 and 2020, published in the English language, performed in humans, that assessed the incidence of C. albicans in total edentulous. Exclusion criteria were themes that addressed other types of rehabilitation; studies that associated only the treatment of oral candidosis without analyzing the epidemiological profile; literature reviews; and posters. The selection of articles was ordered in three important methodological steps:

  • Article exclusion by title.

  • Critical reading of the articles to perform a systematic investigation of the information.

  • Selection and extraction of data by independent and calibrated researchers (FIDC and JAM). A third evaluator (MFH) was asked to perform the article's inclusion or exclusion in case of conflicting information. 

After careful selection, the data obtained were ordered according to Table 1. Data obtained were analyzed using SPSS (SPSS Statistics for Windows, Version 17.0. Chicago: SPSS Inc.). Information obtained was evaluated by absolute (n) and relative (%) frequencies.

Table 1: Characteristics of the studies and sample included in the scoping review.

Author, year Country

Full sample

Sample distribution

Clinical features and prevalence of patients with C. albicans using CD

Characteristics of published studies

Male

Female

Clinical criteria used for the diagnosis

Prevalence n (%)

Follow-up

Objectives of the study

Original title

Journal of publication

Abaci et al., 20107 Turkey

110

47

63

Clinical examination was performed by the clinicians, who classified according to the criteria proposed by Newton. *

14 (12.72)

12 months

The aim of this study was to determine Candida spp. incidence in the oral cavity of denture wearers and characterize predisposing factors in denture-related stomatitis.

Determining Candida spp. Incidence in denture wearers.

Mycopathologia.

Aleva et al., 20074 Brazil

51

DNI

DNI

DNI

30 (58.82)

DNI

This investigation was designed to evaluate the frequency of erythematous candidosis and Candida species, proteinase and phospholipase exoenzyme production, and to compare clinical features in patients with complete dentures and HIV+/Acquired Immunodeficiency Disease Syndrome.

Erythematous candidosis in patients with complete dentures and HIV+/AIDS.

Mycoses

Bilhan et al., 20096 Turkey

91

DNI

DNI

Clinical examination was performed by the clinicians, who classified according to the criteria proposed by Newton. *

58 (54.94)

24 months

The aim of this study was to investigate the relationship of DRS with the presence of Candida albicans hyphae and Lactobacillus.

The role of Candida albicans hyphae and Lactobacillus in denture-related stomatitis.

Clinical Oral Investigation

Cross et al., 200411 United Kingdom

22

5

12

Clinical examination was performed by the clinicians, who classified according to the criteria proposed by Newton. *

11 (50)

36 months

The aim of the study was to determine the recurrence rate of denture stomatitis and persistence of Candida in 22 patients over a 3-year period.

Evaluation of the recurrence of denture stomatitis and Candida colonization in a small group of patients who received itraconazole.

Oral Surgery Oral Medicine Oral Pathology

Daniluk et al., 200634 Poland

95

42

53

Clinical examination was performed by the clinicians, who classified according to the criteria proposed by Newton. *

38 (40)

DNI

The aim was to determine the fungi occurrence rate in the oral cavity of denture wearer patients in comparison to those without dentures.

Occurrence rate of oral Candida albicans in denture wearer patients.

Advances in Medical Sciences

Gumru et al., 200626 Turkey

75

24

51

Clinical examination was performed by the clinicians, who classified according to the criteria proposed by Newton. *

31 (33.33)

DNI

The aim of this study was to evaluate the correlation between frequency and phospholipase activity of Candida species and denture stomatitis according to Newton’s classification.

Distribution and phospholipase activity of Candida species in different denture stomatitis types.

Mycopathologia

Iinuma et al., 20155 Japan

524

228

296

Denture plaque was assessed using a modification of the Ambjornsen Denture Plaque Index. †

108 (20.61)

36 months

“To identify modifiable oral health–related risk factors, we prospectively investigated associations between a constellation of oral health behaviors and incident pneumonia in the community-living very elderly (i.e., 85 years of age or older).”

Denture wearing during sleep doubles the risk of pneumonia in the very elderly.

Clinical Research Supplement

Jafari et al., 201336 Iran

28

18

10

DNI

16 (52)

3 months

Determine the distribution profile of Candida species isolated from cheek angles of patients with old denture before and after replacing with new ones.

Distribution profile of Candida species involved in angular cheilitis lesions before and after denture replacement.

Jundishapur Journal of Microbiology

Kanli et al., 20052 Turkey

42

29

13

DNI

21 (50)

6 months

The purpose of this study was to determine oral hygiene habits, denture cleanliness and presence of yeasts in elderly complete denture wearers.

Oral candidosis, denture cleanliness and hygiene habits in an elderly population.

Aging Clinical and Experimental Research

Kulak-Ozkan et al., 2002 8 Turkey

70

DNI

DNI

The degree of palatal erythema was scored by using the following clinical index: ‡ 0: No inflammation 1: Slight inflammation 2: Moderate inflammation 3: Severe inflammation.

15 (21.42)

DNI

The purpose of this study was to determine oral hygiene habits, denture cleanliness, presence of yeasts and denture stomatitis in elderly people.

Oral hygiene habits, denture cleanliness, presence of yeasts and stomatitis in elderly people.

Journal of Oral Rehabilitation

Loster et al., 201610 Poland

930

307

613

DNI

552 (59.35)

60 months

The purpose of this study was to evaluate the intensity, genera, and frequency of yeasts in the oral cavity of complete denture wearers in terms of subject gender and age.

Correlation between age and gender in Candida species infections of complete denture wearers: a retrospective analysis.

Clinical Interventions in Aging

Lund et al., 20103 Brazil

143

35

108

Detection of diffuse or focal erythematous micropapular lesions, confined to palatal denture-bearing mucosa and clinically compatible with CAC; and lesions in dorsal tongue, central papillary atrophy, associated or not to a white surface change, besides the presence of the lesions at palate previously described.

44 (62.92)

12 months

The purpose of this study was to survey the frequency of Candida spp. in patients with chronic atrophic candidiasis (CAC), to differentiate Candida species and to assess the prevalence of certain infection-associated variables to this disease. Patients with CAC and wearing partial or complete dentures were recruited.

Occurrence, isolation and differentiation of Candida spp. And prevalence of variables associated to chronic atrophic candidiasis

Mycoses

Lyon et al., 200612 Brazil

99

DNI

DNI

Clinical examination was performed by the clinicians, who classified according to the criteria proposed by Newton.*

28 (27.72)

12 months

The aim of this study was to assess the contribution and the correlation between the virulence factors of Candida albicans in denture stomatitis.

Correlation between adhesion, enzyme production, and susceptibility to fluconazole in Candida albicans obtained from denture wearers

Oral Surgery, Oral Medicine, Oral Pathology, Oral Radiology Endodontic

Nagaral et al., 201435 Saudi Arabia

25

25

0

Clinical examination was performed by the clinicians, who classified according to the criteria proposed by Newton.*

10 (40)

12 months

This study investigated the association between oral and fingertip candidal isolation in a group of denture wearers.

Isolation of Candida species from the oral cavity and fingertips of complete denture wearers.

The Journal of Prosthetic Dentistry

Nayak et al., 201233 India

100

50

50

DNI

57 (57)

DNI

1) To assess the prevalence of Candida in non-denture wearers and in denture wearers by oral rinse technique, with isolation on SDA; 2) to speciate and quantify Candida in non-denture wearers and denture wearers by using conventional methods (germ tube test, carbohydrate fermentation test, urease test) and the CHROMagar method; 3) to assess the influence of smoking and diabetes on candidal species among the denture wearers; and 4) to assess the sensitivity and specificity of SDA and CHRO Magar.

Comparative study of Candida by conventional and CHROMagar method in non-denture and denture wearers by oral rinse technique.

Indian Journal of Dental Research

Pires et al., 200215 Brazil

77

28

49

Clinical examination was performed by the clinicians, who classified according to the criteria proposed by Newton.*

51 (66.23)

6 months

Denture stomatitis is frequently associated with high levels of Candida in saliva and deficient denture hygiene.

Denture stomatitis and salivary Candida in Brazilian edentulous patients.

Journal of Oral Rehabilitation

Song et al., 200932 Norway

41

22

19

DNI

20 (48.78)

DNI

To study the species and phenotypic characteristics of yeasts, i.e., colony morphology, biotypes, and biotype relatedness, and the oral distribution of yeasts, in thrush and denture stomatitis.

Colony morpholo-gies, species, and biotypes of yeasts from thrush and denture stomatitis

Acta Odontologica Scandinavica

Vanden Abbeele et al., 200813 Belgium

87

26

61

Inclusion criterion was wearing a maxillary removable acrylic prosthesis and exclusion criteria were the presence of stomatitis, acute illness, chronic infection and the use of oral hygiene care products with antimicrobials or antifungals

53 (60.91)

6 months

The aim of this study was to investigate yeast carriage in healthy denture wearers by swabbing and to evaluate the effect of denture hygiene habits.

Denture contamination by yeasts in the elderly

Gerodontology

Zomorodian et al., 201116 Iran

114

35

79

DNI

61 (53.50)

DNI

“In this study, we investigated risk factors associated with progression to Candida-related denture stomatitis in patients using complete dentures, and we genetically identified Candida isolates associated with disease and colonization.”

Assessment of Candida species colonization and denture-related stomatitis in complete denture wearers

Medical Mycology

Results

Initially, 89 original studies were selected. After removing all duplicates, 84 remained. Subsequently, the exclusion criteria were established, which allowed 19 unique studies to assess C. albicans incidence in patients using CD (Figure 1).

https://typeset-prod-media-server.s3.amazonaws.com/article_uploads/f2ea3a54-6757-4734-bdea-775d3417954f/image/227f6d5c-232d-435d-855e-b9dc964d6b7b-ucaptura-de-tela-2021-03-22-xe0s-00-u49-u35.png
Figure 1: Flow diagram of the identification, inclusion and exclusion process.

Concerning the countries where most of the studies were conducted, 26.3% (n = 5) were in Turkey and 21% (n = 4) in Brazil. Almost half of the studies were done in these two countries (Table 2).

Table 2: Countries where studies were developed.

Countries

n (%)

Turkey

5 (26.3)

Brazil

4 (21.0)

Iran

2 (10.5)

Poland

2 (10.5)

Belgium

1 (5.3)

India

1 (5.3)

Japan

1 (5.3)

Norway

1 (5.3)

Saudi Arabia

1 (5.3)

United Kingdom

1 (5.3)

Table 3 shows the results regarding demographic evaluation and frequency of C. albicans contamination in patients using CD. Poland (37.6%; n = 1,025), Japan (19.2%; n = 524), and Turkey (14.3%; n = 388) showed the highest patient samples while Saudi Arabia (0.9%; n = 25) and United Kingdom (0.8%; n = 22), the lowest. There was also a greater trend in the use of CD in females compared to males. Poland (48.4%; n = 590), Brazil (12.5%; n = 153) and Turkey (11.4%; n = 139) presented the highest frequency of patients that correlated the contamination by C. albicans in CD. Countries such as Saudi Arabia (0.8%; n = 10) and United Kingdom (1.1%; n = 14) had the lowest recurrence rates. CD users presented prosthetic stomatitis associated with C. albicans microorganisms in approximately 1.218 (44.7%) of 2.724 cases studied.

Table 3: Demographic evaluation and frequency of Candida albicans contamination in patients using Complete Denture.

Study location

Full sample investigated by the study n (%)

Males (n)

Females (n)

Sample prevalence of C. albicans n (%)

Poland

1025 (37.6)

349

666

590 (48.4)

Brazil

370 (13.6)

63*

157*

153 (12.5)

Turkey

388 (14.3)

100*

127*

139 (11.4)

Japan

524 (19.2)

228

296

108 (8.9)

Iran

142 (5.2)

54

89

77 (6.3)

India

100 (3.7)

50

50

57 (4.7)

Belgium

87 (3.2)

26

61

53 (4.3)

Norway

41 (1.5)

22

19

20 (1.6)

United Kingdom

22 (0.8)

5

12

14 (1.1)

Saudi Arabia

25 (0.9)

25

0

10 (0.8)

Discussion

This review allowed us to trace the epidemiology of C. albicans in CD wearers, outlining its causes, the population most affected, thus giving some contribution in developing public health policies. With that in mind, the profile of patients who use CD, the most used classifications for diagnosing prosthetic stomatitis, hygiene factors of CD, systemic diseases associated with candidiasis, and C. albicans incidence in patients using CD will be discussed.

Profile of patients using Complete Dentures

Clinical studies analyzing the use of CD and prosthetic stomatitis association showed a higher prevalence of females in Turkey7, 8, Brazil, Japan, Iran, and Poland3, 5, 10, 15, 16. Mesas et al.17 evaluated an incidence of chronic infection in patients with CD in Brazil, showing that 59.9% of their sample was also composed of women. Other authors have confirmed these findings in different Brazilian cities3, 18.

Also, in Poland, it was observed an association between age and gender with the incidence of oral candidiasis in a sample of 920 CD users10. A total of 613 female patients aged 50–70 years were studied, and 58% had their prosthesis contaminated by C. albicans. In the same direction, Azevedo et al. assessed the use and need for dental prostheses in elderly patients in Brazil, observing that 62.2% were composed of women aged 65–74 years old19.

It can be recognized that women are predominant, aged 50–70 years, when the profiles of patients using CD are tracked. This is justified because women have a higher perception of the impact of rehabilitation on the quality-of-life indexes, are more concerned with oral health and are more often looking for dental care for function rehabilitation and aesthetics20, 21, 22. Age should be highlighted as a crucial factor for edentulism since progressive and cumulative diseases, such as caries and periodontal disease, play an essential role in the gradual loss of dentition in this population19, 22.

Diagnosis of prosthetic stomatitis

Several classifications were developed to diagnose prosthetic stomatitis, such as the proposed by Newton and Ambjornsen23. It was observed in this scoping review that the most used classification divided prosthetic stomatitis into three types: Type I (presence of small points of inflammation), Type II (presence of erythematous areas covered by a white exudate), and Type III (characterized by a hyperplastic or nodular reaction)24, 25.

In this context, a study conducted in Turkey demonstrated a correlation between inflammation points in the oral mucosa and a slight formation of yeasts of C. albicans in CDs, classified as prosthetic stomatitis type II (n = 18; 83.3%)26. However, another study in Turkey stated that Type III clinical intensity was the one with the highest colony forming units per milliliter (mean = 3.6 x 106 ± 3.8 x 106 cfu/mL) due to the clinical characteristics of an intense inflammatory process and the presence of hyperplasia6. Another study conducted in Brazil reported Type I as the most recurrent clinical condition (n = 21; 27.2%), and it was considered a positive factor related to the other classifications15. Thus, the definitive diagnosis of prosthetic stomatitis should be based on the clinical characteristics, such as tissue color, tissue weight, and symptom assessment. Also, the importance of the differential diagnosis and complementary exams for this condition must be emphasized (Figure 2)27, 28.

https://typeset-prod-media-server.s3.amazonaws.com/article_uploads/f2ea3a54-6757-4734-bdea-775d3417954f/image/02027ba5-4482-4765-aac4-585ae41b639e-ucaptura-de-tela-2021-03-22-xe0s-00-u54-u40.png
Figure 2: Differential diagnostic flowchart, types of candidiasis, clinical conduct and complementary diagnostic tests. Information taken from Dorko et al., 200127 and Neville et al., 201628.

Hygiene of the Complete Denture

There are several reports associating hygiene and CD contamination by C. albicans, considering it critical for developing prosthetic stomatitis in the host2, 8, 29. Factors such as brushing, motor debility, poor hygiene and usage instructions given by the dental surgeon, products with low antimicrobial efficiency, and inadequate anatomical morphologies of the prosthesis may result in poor hygiene of CDs9, 16. Other factors such as old age, systemic debility, poor hygiene, and wear of the CD end up contributing to the proliferation of a pathogenic biofilm that is firmly adhered between the acrylic resin and the patient's oral mucosa, which would suddenly cause a decline in the state of oral health and the quality of life due to the interference in talking and chewing2, 8.

A study conducted in Singapore confirmed that 69.3% (n = 52) of patients removed organic matter by daily brushing, and 38.6% (n = 29) had poor hygiene status (n = 29; 38.6%)29. Furthermore, these values can be observed in a Turkish study that associated oral candidiasis and the hygiene status and cleanliness state of the CD in an elderly population. Their results showed that 78.6% of patients (n = 33) only brushed the CD to remove the biofilm, and 28.5% (n = 12) showed poor hygiene status2.

Systemic diseases and association with oral candidiasis

It has been shown that oral candidiasis may be associated with the progression of some systemic diseases such as HIV, pneumonia, progressive malignancies, and severe malnutrition4, 5, 28, 30, 31. The correlation between erythematous candidiasis in HIV-positive patients and CD users has been reported. Results showed that 15 patients in the examined sample (71.4%) had their prostheses contaminated by C. albicans. Furthermore, these results were observed in other systemic diseases, such as pneumonia, in which 19.9% of the elders in Japan (n = 108) presented their prostheses contaminated by C. albicans with a mild association in the patient's oral and systemic health status.

Sample of C. Albicans in patients using Complete Dentures

Oral candidiasis is a condition predominantly found in patients using CD, and it is considered a critical public health problem worldwide24, 25, 26. This disease can be characterized by the growth of the C. albicans fungus and the supporting action of other species such as C. tropicalis, C. parapsilosis, C. krusei, and C. glabrata 3, 6, 16, 26, 32, 33, 34, 35, 36.

The growth of C. albicans (n = 31; 41.3%) and the secondary participation of other yeasts such as C. krusei (n = 6; 8%), C. glabrata (n = 3; 4%), C. tropicalis (n = 3; 4%), C. kefyr (n = 1; 1.3%) and C. guilliermondii (n = 1; 1.3%) has been reported previously in Turkey26. These results were similar to Norwegian findings in which C. albicans (n = 20; 90.9%) was highlighted as the main microorganism in the prosthetic stomatitis pathogenesis32. Similar results were found in an elderly Iranian population, in which the same growth pattern of these fungi was observed: C. albicans (41.5%), C.glabrata (18.4%), C. Tropicalis (12.9%), C. dubliniensis (10.9%), and C. parapsilosis (6.1%)16. In this study, approximately 44.7% of CD users presented prosthetic stomatitis associated with C. albicans (total n = 2,724).

Limitations of the review process and the extent of information uncovered

This review has some limitations. To make this review more feasible, we opted to conduct an integrative, not a systematic review. So, the quality of the included studies was not an analyzed criterion. Also, there was a limitation in the database selection, and the gray literature was not searched. It is also possible to mention as a limitation the period of analysis of the literature since studies published more than 20 years ago were excluded.

Conclusion

Prosthetic stomatitis is a condition that mostly affects women aged 50–70 years and has a multifactorial predisposition. Furthermore, the classification proposed by Newton in 1962 is the most used for the clinical diagnosis of oral candidiasis. Still, the state of hygiene of CD is a crucial factor for the progression of candidosis, in the same way that C. albicans plays an essential role in the progression of this pathogenesis in the host.

Acknowledgments

We thank the Brazilian Ministry of Education and Culture for sponsoring Tutorial Education Program - PET of the Federal University of Alfenas.

Additional information

Conflicts of interest: No conflicts of interest declared concerning the publication of this article.

Indications about the contributions of each author:

Conception and design of the study: FIDC, MFH

Analysis and interpretation of data: Not applicable

Data collection: JAM, FIDC

Writing of the manuscript: FIDC, KCSG, MFH

Critical revision of the article: KCSG, MFH

Final approval of the manuscript*: FIDC, JAM, KCSG, MFH

Statistical analysis: Not applicable

Overall responsibility: FIDC

*All authors have read and approved of the final version of the article submitted to Rev Cienc Saude.

Funding information: We thank the Brazilian Ministry of Education and Culture for sponsoring the Tutorial Education Program - PET at the Federal University of Alfenas, providing scholarships for the student approved by the edict 063/2017.