Journal of Oral Rehabilitation 2006 33; 36–42

Association of candidal activity with denture use and salivary flow in symptom-free adults over 60 years1
K. IKEBE, K. MORII, K. MATSUDA, K. HATA & T. NOKUBI
Regeneration, Osaka University Graduate School of Dentistry, Yamadaoka Suita Osaka, Japan Division of Oromaxillofacial

SUMMARY

The purpose of this study was to examine the amount of palatal mucosa Candida species associated with denture use and stimulated salivary flow in symptom-free adults over 60 years. The subjects were 351 (189 men and 162 women) independently living elderly people with a mean age of 66Æ7 Æ 4Æ3 (SD) years. Candidal activity of palatal mucosa was evaluated by the pH change in the medium that was associated with the acid production of the yeast. Subjects whose stimulated salivary flow rate was less than 0.5ml/min were placed in the hyposalivation group. A multiple logistic regression analysis was used to determine if an independent variable was statistically significant after controlling for other variables. Candidal activity of the palatal mucosa was significantly associated with the dental status of the maxillae (Kruskal-Wallis test, P < 0Æ001), but was not significantly associated with age or drug intake. In

maxillary denture wearers, Candidal activity of palatal mucosa had a significantly positive correlation with candidal activity of tissue fitting surfaces of maxillary dentures (r ¼ 0Æ806, P < 0Æ001). A multiple logistic regression analysis showed that high candidal activity of the palate was significantly associated with being male and wearing maxillary removable dentures. Stimulated salivary flow rate was likely to be negatively related to high candidal activity (P ¼ 0Æ07). This study suggests that the activity of Candida species in the oral cavity is associated with the wearing of removable dentures and stimulated salivary flow, independent of age or gender even in the relatively healthy elderly. KEYWORDS: Candida, palatal mucosa, salivary flow, removable denture, independently living elderly, age, symptom-free, multiple logistic regression analysis, geriatric dentistry, epidemiology Accepted for publication 4 April 2005

Introduction
The most common infection involving oral mucosal tissues in the elderly patient is candidosis. Candida species are typically harmless and common fungi of the surface of the oral mucous membrane (1). Commensal existence of intraoral Candida species varies from 20 to 50% in a healthy dentulous population (2, 3) and up to 75% in a population wearing dentures (3, 4). Although most oral candidoses are symptomless, they can indicate the presence of an underlying
1

This paper was presented at the 80th International Association of Dental Research General Session in San Diego, USA in 2002. ª 2006 Blackwell Publishing Ltd

systemic disease (5, 6). Certain systemic conditions (e.g. diabetes), defects in the immune system, and/or some medications (e.g. antibiotics, corticosteroids) may predispose the transformation of a benign colonization, such as Candida species, into parasitic pathogens (7). Therefore, candidosis mainly has been discussed regarding a cohort of the frail elderly (8–11), not for physiologically aged, comparatively healthy adults. In Japan, most old people (95% between 75 and 79 years, 90% between 80 and 84 years, and 80% of those 85 years and older) are functionally independent and have no limitations in their daily activities (12). Denture use and hyposalivation are common not only in the frail elderly, but also in the comparatively

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ASSOCIATION OF CANDIDAL ACTIVITY WITH DENTURE AND SALIVA
healthy elderly who live independently. The 1999 Japanese national survey of dental diseases by the Ministry of Health and Welfare collected data from every member of all households in 300 municipalities that had been randomly sampled in every prefecture (13). The survey found that the number of residual teeth gradually declined after age 50. Consequently, 50% of people between 65 and 74 years and 70% of those between 75 and 84 used removable dentures. Another change in the oral cavity brought on by ageing is oral dryness. It is well known that saliva plays an important role in the preservation and maintenance of oral health and function (14). The prevalence of dry mouth varies from 13 to 39% in independent or community-living old people (15–20). In the similar subjects of this study, it was demonstrated that approximately one-fourth were classified as having hyposalivation (21). The purpose of this study was to examine the amount of palatal mucosa Candida associated with denture use and stimulated salivary flow in symptom-free adults over 60 years.

37

Dental status Subjects were classified into three categories according to the dental status of their maxilla: complete denture, removable partial denture, or natural dentition.

Candidal activity Samples of palatal mucosa were collected with sterile swabs because stomatitis is most prevalent on the maxillary hard palate (22). In the subjects whose palates were covered with removable dentures, samples of tissue fitting surfaces of a maxillary denture were also collected. Persons with a symptom or an obvious sign of stomatitis in the palatal mucosa were excluded from the analyses. Samples were incubated for 24h in a liquid selective medium for Candida species (StomastatTM)* (23). Candidal activity was evaluated by the pH change in the medium that was associated with the acid production of the yeasts. Lower pH of the medium indicates higher candidal activity.

Methods
Study population The subjects in this study were participants of the Senior Citizens’ College of Osaka prefecture. The study sample consisted of community-dwelling, independently living elderly people over the age of 60 years who attended lectures once a week. This college is one of the adult educational systems supported by the government of Osaka prefecture, which enrols volunteers for a period of 1 year. This course focused not only on health topics but also on other topics of interest to elderly people, such as finance or culture. The research protocol was approved by the Institutional Review Board of Osaka University Graduate School of Dentistry. After informed consent, subjects were given the opportunity to ask questions while completing the questionnaires; subjects could refuse to participate in the oral examination portion of the study. The final study population who voluntarily participated in the dental and oral examinations consisted of 351 persons (189 men and 162 women) with a mean age of 66Æ7 Æ 4Æ3 (s.d.) years. Information about the use of prescribed drugs was sought during the interview.
ª 2006 Blackwell Publishing Ltd, Journal of Oral Rehabilitation 33; 36–42

Saliva collection Stimulated whole saliva was collected by the mastication method (24). Subjects with complete or removable partial dentures wore their dentures during the saliva collection period (20). Subjects were asked to swallow all the saliva in the mouth, then to chew the wax for 2 min at their own pace and spit into a graduated tube. All saliva specimens were collected between 10:00 AM and 3:00 PM. Subjects were classified into two groups according to stimulated salivary flow rates. Persons whose stimulated flow rate was <0Æ5 mL min)1 were placed in the hyposalivation group, and the rest were designated as the normal stimulated salivary flow group (25, 26). Persons with a history of major salivary gland pathology or extirpation were excluded from the analyses.

Data analysis The data analyses were done by using SPSS 12Æ0** for Windows. Difference in candidal activity, which was the pH in the selective medium, was evaluated by the
*DENTSPLY – Senkin K. K., Tokyo. **SPSS Inc., Chicago, IL, USA.

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Mann–Whitney U-test or the Kruskal–Wallis test because the distributions did not have normality. P-values £0Æ05 were considered to be statistically significant. Pairwise comparisons after the Kruskal–Wallis tests were made by means of the Mann–Whitney U-tests with Bonferroni adjustments. Results were considered significant at a ¼ 0Æ01 for three categories (27). In addition, Spearman’s correlation coefficients were used to evaluate the relationship between candidal activity of tissue fitting surface of a maxillary denture and palatal mucosa in the same individuals. A multiple logistic regression analysis was used to determine if an independent variable was statistically significant after controlling for other variables. The dependent variable was the proportion of the subjects with high candidal activity of palatal mucosa (less than the 25th percentile in pH of the medium) (28). All independent variables evaluated were entered into the model. Age and stimulated salivary flow rate were continuous independent variables. Other independent variables, such as gender, drugs intake and dental status of maxilla, were transformed into dichotomous variables.
160 140

Number of persons

120 100 80 60 40 20 0
–4·25 –4·5 –4·75 –5 –5·25 –5·75 –6·25 –5·5 –6

pH of

StomastatTM

of palatal mucosa

Fig. 1. Distribution of candidal activity of palatal mucosa.

associated with being male and wearing maxillary removable dentures (Table 2). The odds ratio was the highest for dental status of maxilla (2Æ0 for RPD/natural dentition, 3Æ9 for CD/natural dentition). Stimulated salivary flow rate was likely to be negatively related to high candidal activity (odds ratio ¼ 0Æ74, P ¼ 0Æ07) (Table 3).

Results
Distribution of the pH in the selective medium after incubation was skewed (Fig. 1). The mean pH of the medium was 5Æ49 (s.d.: 0Æ37) and the median pH was 5Æ66. There was a significant difference in the candidal activity according to the dental status of the maxilla (P < 0Æ001) (Table 1). The complete denture group (n ¼ 38) showed significantly higher candidal activity than the other two groups, and the removable partial denture group (n ¼ 101) showed significantly higher candidal activity than the natural dentition group (n ¼ 212) in multiple comparisons (P < 0Æ01). Candidal activity was likely to be higher in the hyposalivation group (<0Æ5 mL min)1) than in the normal stimulated salivary flow group (P ¼ 0Æ059). Stimulated salivary flow rate was not significantly associated with dental status (P ¼ 0Æ40) (Table 2). In maxillary denture wearers, candidal activity of palatal mucosa had a significantly positive correlation with candidal activity of tissue fitting surfaces of a maxillary denture (r ¼ 0Æ806, P < 0Æ001) (Fig. 2). A multiple logistic regression analysis showed that high candidal activity of the palate was significantly

Discussion
Candidal parasitism to the palatal mucosa is usually symptomless and may not always lead to stomatitis or the need for treatment. However, decline in the body’s defenses or drug therapy may predispose an increase in numbers of Candida species or the transformation of Candida species into a pathological state (2). Most healthy elderly people inevitably become frail because of disease or from the natural process of ageing and they commonly wear removable dentures. Therefore, it is important both for individuals and for public health in general that information regarding risk factors of oral infection and disease prevention be made available. For this reason, we used persons who were symptom-free of stomatitis as study subjects. A number of epidemiological studies have yielded information about the prevalence of denture-related stomatitis (8, 9, 11, 29). However, there are remarkable differences in the findings. These might be explained by demographic variations, by the use of different diagnostic criteria, or by a lack of standardized definitions in clinical examinations (30). In examining colonized yeasts, the commonly used method of conventional vital counting has several
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ASSOCIATION OF CANDIDAL ACTIVITY WITH DENTURE AND SALIVA
Table 1. Association of gender, age, drug intake, dental status and salivary flow with candidal activity of palatal mucosa Variables Gender Male Female Age 60–64 years 65–69 years 70 years and more Medication No Yes Dental status of maxillae Complete denture Removable partial denture Natural dentition Stimulated salivary flow less than 0Æ5 mL min)1 0Æ5 mL min)1 and more Total

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% of subjects

pH of StomastatTM Interquartile range

n

%

Mean

s.d.

Median

P-value*

189 162 121 141 89 178 117 38 101 212 86 265 351

53Æ8 46Æ2 34Æ5 40Æ2 25Æ4 50Æ7 33Æ3 10Æ8 28Æ8 60Æ4 24Æ5 75Æ5

5Æ48 5Æ52 5Æ54 5Æ50 5Æ44 5Æ50 5Æ51 5Æ27 5Æ44 5Æ57 5Æ51 5Æ45 5Æ50

0Æ37 0Æ35 0Æ35 0Æ36 0Æ36 0Æ36 0Æ35 0Æ46 0Æ37 0Æ32 0Æ36 0Æ36 0Æ36

5Æ66 5Æ68 5Æ68 5Æ66 5Æ57 5Æ67 5Æ65 5Æ47 5Æ54 5Æ70 5Æ59 5Æ67 5Æ66

0Æ48 0Æ36 0Æ35 0Æ38 0Æ55 0Æ46 0Æ39 0Æ80 0Æ51 0Æ24 0Æ47 0Æ42 0Æ41

0Æ158

0Æ414

0Æ798

<0Æ001

0Æ059

*Mann–Whitney U-test or Kruskal–Wallis test.

6·5 pH of StomastatTM of palatal mucosa 6·0 5·5 5·0 4·5 y = 0·757x+1·39 4·0 3·5 3·5 r = 0·806, P < 0·001

Table 2. Salivary flow rate by status of maxillae n complete denture removable partial denture natural dentition Total *Kruskal–Wallis test. 38 101 212 351 Mean 0Æ97 1Æ13 1Æ16 1Æ13 s.d. 0Æ76 0Æ78 0Æ86 0Æ83 P-value* 0Æ403

4·0

4·5

5·0

5·5

6·0

6·5

pH of StomastatTM of denture surface

Fig. 2. Relationship between candidal activity of tissue fitting surface of denture and palatal mucosa.

shortcomings, particularly in respect to its precision. In order to objectively evaluate candidal activity, a simple method of measuring Candida biofilms activity using pH change in the liquid selective medium was used in this study (23). The logarithm of the initial
ª 2006 Blackwell Publishing Ltd, Journal of Oral Rehabilitation 33; 36–42

number of yeasts from the inoculated swab was linearly correlated with the pH value of StomastatTM after both 24-h incubation periods (r ¼ 0Æ992, P < 0Æ01), which confirmed the validity of this method (31). This simple quantitative method could be extended to the determination of the fungal levels in denture or oral carriage in vivo. Therefore, this method is quantitative, simple and suitable for large fieldwork populations. It has generally been assumed that old age may also represent a predisposing condition for increased candidal colonization. Lockhart et al. (32) demonstrated that the frequency and intensity of carriage of candidal colonization increased as a function of age, independent of denture use. However, our study demonstrated

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Table 3. Logistic regression analysis for the candidal activity of palate (n ¼ 351)

B Age )0Æ043 Gender 0Æ601 Medication )0Æ181 Dental status (P-value ¼ 0Æ002) CD 1Æ362 RPD 0Æ674 Salivary flow )0Æ311

s.e. 0Æ034 0Æ293 0Æ266 0Æ424 0Æ293 0Æ174

P-value 0Æ200 0Æ040 0Æ497 0Æ001 0Æ021 0Æ074

Odds ratio 0Æ96 1Æ82 0Æ83 3Æ90 1Æ96 0Æ73

95% CI 0Æ90–1Æ02 1Æ03–3Æ24 0Æ50–1Æ41 1Æ70–8Æ96 1Æ10–3Æ48 0Æ52–1Æ03

RPD, removable partial denture; CD, complete denture. Dependent variable: candidal activity of palate. Age (years): continuous variable. Gender: males ¼ 0, females ¼ 1. Medication: No ¼ 0, Yes ¼ 1. Dental Status: natural dentition was the reference category (¼0) for RPD or CD (¼1). Salivary flow (mL min)1): continuous variable.

that candidal activity was not significantly associated with age or gender in the relatively healthy old people. This discrepancy may be caused by the difference in mean age (77 versus 67 years) and chronic medical conditions between the study samples. The commonest form of oral candidosis is Candidaassociated denture stomatitis (9, 33). The maxillary denture was reported as the major source of candidal infection in long-term hospital care (9). High oral yeast counts and frequent prevalence of oral candidosis in elderly subjects living in institutions were associated with poor oral hygiene and neglect of denture care (11). Our results indicated that using a maxillary denture was the only significant independent variable associated with candidal activity, even in relatively healthy older adults, after controlling for age, gender and drug intake. This finding is not new: using imprint cultures, the frequency of isolation of Candida albicans in complete denture wearers was more than twice that of dentate patients (34). Dentures may be the direct cause of many oral mucosal lesions because of a change in the oral cavity and a loading of the oral mucosal (30). In addition, candidal activity of tissue fitting surfaces of a maxillary denture is strongly associated with candidal activity of the palatal mucosa, suggesting that wearing dentures, especially maxillary complete dentures, plays a role in creating a reservoir for disseminated infections (35). Therefore, in order to treat oral candidosis, we should disinfect or replace the dentures at the initial stage of treatment. Surface irregularities of the denture would increase the likelihood of microorganisms remaining on the surface after the prosthesis is cleaned, allowing continuous reinfection of the plate (36, 37), so

the denture surface must be polished as smooth as possible. Another possible reason for a change in the oral cavity is hyposalivation. Narhi et al. (38) demonstrated that subjects with low stimulated salivary flow rates had significantly higher yeast counts than did subjects with normal stimulated salivary flow rates in a group of 368 Finns aged 76, 81 and 86 years. Our results indicated that persons with low stimulated salivary flow tended to have high candidal activity in symptomfree older adults. Saliva mechanically cleans the oral cavity and reduces the adhesion of C. albicans to the acrylic resin of dentures (39, 40). Many salivary proteins protect the soft tissue of the oral cavity (41). Human saliva contains yeast inhibitors such as histatin, defensin or secretory immunoglobulin A (42–45). Our finding reconfirmed the importance of saliva in protecting the soft tissue of the oral cavity, even in the relatively healthy older adults. This study suggests that the activity of Candida species in the oral cavity is associated with the wearing of removable dentures and stimulated salivary flow, independent of age or gender even in the relatively healthy elderly. The results emphasize the critical need to measure candidal activity of denture wearers as candidosis is usually symptomless and hyposalivation is very common.

Acknowledgments
The authors greatly appreciated the grammatical correction of the manuscript by Joanne Madsen, M.A. We are especially grateful to Ronald L. Ettinger BDS,
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ASSOCIATION OF CANDIDAL ACTIVITY WITH DENTURE AND SALIVA
MDS, DDSc, Professor of University of Iowa, College of Dentistry and Robert P. Renner DDS, Professor of State University of New York at Stony Brook, School of Dental Medicine for commenting and advising on the manuscript. This investigation was partially supported by a Grant-in-Aid for Scientific Research (No. 16390555) from Japan Society for the Promotion of Science.
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Correspondence: Kazunori Ikebe, Division of Oromaxillofacial Regeneration, Osaka University Graduate School of Dentistry, University of Osaka Faculty of Dentistry, 1-8 Yamadaoka Suita Osaka 565-0871, Japan. E-mail: ikebe@dent.osaka-u.ac.jp

ª 2006 Blackwell Publishing Ltd, Journal of Oral Rehabilitation 33; 36–42