Oral frailty and carriage of oral Candida in community-dwelling older adults (Check-up to discover Health with Energy for senior Residents in Iwamizawa; CHEER Iwamizawa)

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Oral frailty and carriage of oral Candida in community-dwelling older adults (Check-up to discover Health with Energy
for senior Residents in Iwamizawa; CHEER Iwamizawa)

馬場, 陽久

北海道大学. 博士(歯学) 甲第15493号

2023-03-23

10.14943/doctoral.k15493

http://hdl.handle.net/2115/89889

theses (doctoral)

Haruhisa_Baba.pdf

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Hokkaido University Collection of Scholarly and Academic Papers : HUSCAP

博 士 論 文

Oral frailty and carriage of oral Candida in
community-dwelling older adults (Check-up to
discover Health with Energy for senior Residents in
Iwamizawa; CHEER Iwamizawa)
（地域在住高齢者におけるオーラルフレイルと
口腔カンジダの保菌状態との関連）

令和５年３月申請

北海道大学
大学院歯学院口腔医学専攻

馬

場 陽 久

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Received: 11 May 2021    Revised: 14 December 2021    Accepted: 16 January 2022
DOI: 10.1111/ger.12621

SPECIAL ISSUE

Oral frailty and carriage of oral Candida in community-­dwelling
older adults (Check-­up to discover Health with Energy for
senior Residents in Iwamizawa; CHEER Iwamizawa)
Haruhisa Baba1 | Yutaka Watanabe1  | Kazuhito Miura1 | Kimiya Ozaki1 |
Takae Matsushita1 | Miyako Kondoh1 | Kazutaka Okada1 | Akira Hasebe2 |
Tokiyoshi Ayabe3 | Kiminori Nakamura3 | Shinji Nakaoka4 | Katsuhiko Ogasawara5 |
Teppei Suzuki6 | Hiroshi Saito7 | Takashi Kimura7 | Akiko Tamakoshi7 |
Yutaka Yamazaki1
1

Gerodontology, Department of Oral Health Science, Faculty of Dental Medicine, Hokkaido University, Sapporo City, Japan

2

Oral Molecular Microbiology, Department of Oral Pathobiological Science, Faculty of Dental Medicine, Hokkaido University, Sapporo City, Japan

3

Department of Cell Biological Science, Faculty of Advanced Life Science, Hokkaido University, Sapporo City, Japan

4

Laboratory of Mathematical Biology, Department of Advanced Transdisciplinary Sciences, Faculty of Advanced Life Science, Hokkaido University, Sapporo
City, Japan
5

Health Innovation and Technology Center, Faculty of Health Sciences, Hokkaido University, Sapporo City, Japan

6

Hokkaido University of Education Iwamizawa Campus, Iwamizawa City, Japan

7

Department of Public Health, Division of Preventive Medicine, Hokkaido University, Sapporo City, Japan

Correspondence
Yutaka Watanabe, Gerodontology,
Department of Oral Health Science,
Faculty of Dental Medicine, Hokkaido
University, Kita 13 Nishi 7, Kita-­ku,
Sapporo City, Hokkaido 060-­8586, Japan.
Email: ywata@den.hokudai.ac.jp
Funding information
This work was supported by Japan Science
and Technology (JST) Agency Center of
Innovation (COI) Program (grant numbers:
JPMJCE1301), JSPS KAKENHI [grant
numbers: 20H03873 and 20H03899]
and the Japan Ministry of Health, Labor
and Welfare Administrative Promotion
Policy Science Comprehensive Research
(20AA2006). The funding source had no
involvement in study design; collection,
analysis and interpretation of data; writing
of the report or in the decision to submit
the article for publication.

Objective: To examine the association between oral frailty and oral Candida carriage
as a general indicator of deteriorating oral function in older adults.
Background: Older adults exhibit an elevated risk of oral candidiasis caused by
Candida. Although many studies have identified factors associated with oral Candida
carriage, none have evaluated its relationship with oral function.
Materials and Methods: This study included 210 community-­dwelling older adults
aged ≥60 years who participated in wellness checks. Fungal flora expression in saliva
samples was evaluated to identify oral C. albicans and C. glabrata. Participants were
categorised by detection of neither strain (group 1), either one of the strains (group
2), or both strains (group 3). The relationship between oral Candida carriage and oral
frailty was evaluated by multinomial logistic regression analysis.
Results: The participants included 58 men and 152 women with a mean age of
74.2 ± 6.1 years. A total of 88 (41.9%), 94 (44.8%) and 28 (13.3%) participants were
assigned to groups 1, 2 and 3 respectively. In the multinomial logistic regression analysis, significant associations were observed between group 1 and group 2 for “Have
you choked on your tea or soup recently?” and the number of applicable oral frailty
items. Between group 1 and group 3, significant associations were observed for the
number of remaining teeth, masticatory performance and the number of applicable
oral frailty items.

© 2022 Gerodontology Association and John Wiley & Sons Ltd
Gerodontology. 2022;00:1–10. 

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wileyonlinelibrary.com/journal/ger     1

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BABA et al.

Conclusion: We obtained basic data useful for intervention studies aimed at verifying
whether oral function management prevents deterioration of the oral bacterial flora.
KEYWORDS

Candida albicans, Candida glabrata, community-­dwelling older adults, cross-­sectional study,
internal transcribed spacer 2, oral frailty

1  |  I NTRO D U C TI O N

2  |  M E TH O D S

Oral Candida are normal fungi present in the oral cavity in 3%-­

2.1  |  Study design

75%1-­3 of healthy individuals. Systemic deterioration in the host’s
condition, however, can cause oral Candida to propagate, leading

This was a cross-­sectional study of community-­dwelling older adults.

to an opportunistic infection called oral candidiasis. Oral candidiasis, triggered primarily by Candida albicans (C. albicans), presents
with symptoms such as redness and pain of the oral mucosa and

2.2  |  Participants

dysgeusia. C.  albicans has little pathogenic potential on its own,
even in comparison with normal oral bacteria, and oral candidiasis

Citizens of Iwamizawa City in Hokkaido in northern Japan, aged

is rare in healthy individuals. However, older adults have an ele-

≥60 years, were recruited to participate in a wellness check. Local gov-

vated risk for developing candidiasis due to factors such as oral

ernment employees visited the social clubs of senior citizens in the city

hygiene deterioration, denture use, reduced salivary secretion, un-

to describe the nature of the study and recruit potential participants.

dernutrition and deteriorated immunity. Oral Candida strains are

In addition, the city newsletter ran an article to recruit participants,

also a cause of aspiration pneumonia in older adults. In addition,

and recruitment flyers were posted on the walls of major facilities in

some studies have reported that the pathology of oral candidia-

the city. The recruited participants were evaluated in October 2020,

4,5

In addition to C.  albicans, an increase

and those who had undergone previous wellness checks were se-

in another strain of Candida, C. glabrata, has been reported in pa-

lected for inclusion. The principal investigator explained the nature of

tients with oral candidiasis. 5-­7 Infection by C.  glabrata is believed

the study to the participants in advance, both orally and in writing, and

to occur as a mixed infection with C. albicans rather than a single

obtained written consent. The study was conducted in accordance

sis has recently changed.

infection.

7-­9

According to some studies, an increase in resistance

with the Declaration of Helsinki and was approved by the Hokkaido

to the azole class of antifungals in cases of mixed infections leads

University Faculty of Dental Medicine Clinical/Epidemiological

to treatment failure and repeated relapse.9-­11 Although clinical

Research Institutional Review Board (2020 no. 9).

studies on oral Candida have been conducted in patients with oral
candidiasis, few have investigated its expression in healthy, asymptomatic, older adults.
In contrast, there has been an increased focus on the evaluation

2.3  |  Assessment of outcomes (oral candida
carriage)

of oral frailty, which is assessed comprehensively based on the number of missing teeth, diminished tongue movement and strength,

The participants chewed a special gum used for salivary tests

reduced masticatory performance and impaired swallowing. Older

(Saliva Gum α; Tokyo Shizaisha) for 1  minute, and the saliva that

adults with oral frailty were found to have significantly higher rates

flowed during that time was collected in sterilised plastic tubes and

of physical frailty and sarcopenia over a 2-­year period, as well as sig-

weighed. The collected saliva was subsequently centrifuged at the

nificantly higher numbers of deaths and increased long-­term care re-

Oral Microbiome Center (Kagawa, Japan) to yield pellets, which

quirements over approximately 4 years.12 However, the mechanism

were cryopreserved until DNA extraction. Next, the salivary pellets

by which oral frailty is related to the onset of these events is not well

were homogenised with MORA-­E XTRACT (Cosmo Bio Co., Ltd.) and

understood. Compared with other oral microflora, such as periodon-

a genomic DNA purification kit (Genfind V2; Nippon Genetics Co.,

topathic bacteria, Candida strains are associated with greater deteri-

Ltd.) was used to extract and purify the DNA. An internal transcribed

oration of the oral environment and the patient's systemic condition,

spacer 2 (ITS2) analysis was conducted using MiSeq (Illumina, Inc)

including a heightened risk of undernutrition, deteriorated immunity

based on Meta-­16S analytical techniques. Polymerase chain reaction

and aspiration pneumonia.

(PCR) amplification of the ITS2 in each sample was performed using

The aim of this cross-­sectional study was to determine the as-

the following ITS2 amplification primers13: F gITS7 5′-­TCGTCGGCAG

sociation between the carriage of oral Candida and oral frailty in

CGTCAGATGTGTATAAGAGACAGN GTGARTCATCGARTCTTTG-­3′

Japanese community-­dwelling older adults.

and R ITS4 5′-­GTCTCGTGGGCTCGGAGATGTGTATAAGAGACA

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BABA et al.

GNTCCTCCGCTTATTGATATGC-­3′. ...

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