328

ORIGINAL
Assessing the oral health of in-patients with diabetes using aclinical version of the Diabetes Oral Health Assessment Tool©
and its association with dental examinations
Yumi Kuwamura1, Eijiro Sakamoto2, Masuko Sumikawa3, Munehide Matsuhisa4, Daisuke Hinode5, Hirokazu Uemura6,
and Sachi Kishida11Department of Nursing, Tokushima University Graduate School of Biomedical Sciences, Tokushima, Japan, 2Periodontology and Endodontology, Dental Clinic, Tokushima University Hospital, Tokushima, Japan, 3Department of Nursing, School of Health Sciences, Sapporo Medical
University, Hokkaido, Japan, 4Diabetes Therapeutics and Research Center, Institute of Advanced Medical Sciences, Tokushima University,
Tokushima, Japan, 5Department of Hygiene and Oral Health Science, Tokushima University Graduate School of Biomedical Sciences, Tokushima, Japan, 6Department of Preventive Medicine, Tokushima University Graduate School of Biomedical Sciences, Tokushima, Japan

Abstract : Aims : To compare assessment of the oral health conditions and behaviors of in-patients with diabetes
using a clinical version of the Diabetes Oral Health Assessment Tool (C-DiOHAT©) with dental examinations.
Methods : A cross-sectional design was used. A nurse assessed 60 in-patients using the C-DiOHAT© (a formatted
questionnaire to assess four factors of patients’ oral health conditions and behaviors : oral health conditions, oral
hygiene behaviors, sharing health information among patients and dental/medical professionals, and perception
and knowledge of oral health) while a dentist examined their oral health conditions. Results : “Use of supplementary tools (e.g., interdental brush, dental floss)” in the item of C-DiOHAT© was significantly associated withdental examination of “the number of present teeth” and “no recommendation of further dental visit”. “Symptoms of gingival swelling” in the item of C-DiOHAT© was also significantly associated with “recommendation ofdental visit”. “Knowledge of a relationship between periodontal disease and systemic disease including diabetes”
was significantly associated with Community Periodontal Index. Conclusions : These results suggest that nurses
should prioritize these assessment items to most quickly acquire useful information about patients’ oral health.
It is important to encourage nurses to be interested in patients’ oral health by such small pile of clue. J. Med.
Invest. 66 : 328-336 August, 2019
Keywords : Nurse, Diabetes, Oral Health Conditions and Behaviors, Assess, Dental Examination

INTRODUCTION
The increasing number of patients with diabetes is a global
burden. It is important to develop strategies to tackle suchdiabetes-related complications as neuropathy, retinopathy, nephropathy, and cardiovascular disease. Periodontal disease is
the “sixth complication of diabetes” (1). It is crucial for diabetes
patients to maintain good oral health to prevent oral diseases
such as periodontitis and dental caries. Indeed, some studies
have examined the frequency of tooth brushing (2) and the useof supplementary tools (e.g., interdental brush, dental floss (3))
among individuals with diabetes. However, to our knowledge,
few previous studies have examined oral self-management
behavior as a part of diabetes self-management behavior. The
Diabetes Oral Health Assessment Tool (DiOHAT©) for nurses(4)—which includes the following four factors : oral health conditions, oral hygiene behaviors, sharing health information among
patients and dental / medical professionals, and perception andknowledge of oral health behaviors—was developed for nurses toassess patients’ oral health conditions and behaviors. Althoughdiabetes nurse specialists recognized the value of DiOHAT©,
its implementation has been considered difficult in clinicalReceived for publication May 16, 2019 ; accepted August 2, 2019.
Address correspondence and reprint requests to Yumi Kuwamura,
RN, Ph.D., 3-18-15, Kuramoto-cho, Tokishima-city, Tokushima, 7708509, Japan.

application due to insufficient time, problems with interdisciplinary coordination between nurses and other specialists, etc.
(5). Therefore, an assessment sheet based on DiOHAT© served
as the clinical assessment sheet for nurses to assess patients’
oral health conditions and behaviors. This is the clinical versionof the DiOHAT© (C-DiOHAT©). It was an assessment sheet
formed as a questionnaire (answering “yes” or “no”) with minerchange from the items in DiOHAT©.
Hence, the present study aimed to assess the oral healthconditions and behaviors of in-patients using C-DiOHAT© andcompare them with dental examinations. The present findings
may reveal the usefulness of the assessment sheet in collecting
evidence on the oral health behaviors of patients with diabetes.

METHODS
DesignThis study used a cross-sectional design.

Participants
Inclusion criteria were the hospital in-patients with diabetes
who provided consent to participation in this study and who
were treated at the diabetes clinic of a university hospital (which
has both medical and dental clinics) and being aged ≥ 20 years.
Exclusion criteria were impediments to communication, and possibility of change in condition due to participation in this study.
This study was conducted from April 2016 to March 2017.

The Journal of Medical Investigation Vol. 66 2019

The Journal of Medical Investigation Vol. 66 August 2019
Survey Methods
Questionnaire Used by the Nurse
The nurse utilized a questionnaire on participants’ characteristics (age ; sex ; type of diabetes ; age at diabetes diagnosis ; complications of diabetes ; current treatment, i.e., oral hypoglycemic
agent alone, injection alone, combination therapy ; and hemoglobin A1c (HbA1c) level), and the questionnaire based on the
DiOHAT©. Although the DiOHAT© comprises 4 factors and
21 items, it was revised for clinical use in a limited time frameby both nurses and patients as an assessment sheet formed asa questionnaire (answering “yes” or “no”). The following changes were made to items of the DiOHAT© : [1] “tooth brushingaround the border between the teeth and marginal gingiva” and“brushing each tooth very carefully” were modified to “brushing each tooth carefully” ; [2] the item “perceptions of one’s oral
health condition” was deleted because patients with painful (6),stressful, or fearful memories of dental treatment require an intervention program, which was not part of this study ; and [3] theitems “presence of dentures (partial or full)”, “checking the insideof the patient’s mouth”, and “counting the patient’s total numberof teeth (exclusive of dentures, bridges, and implants)” were excluded from the questionnaire. These three items were evaluatedby nurses as objective items. They were left out because, in thisstudy, the dentist examined these three aspects during clinicalevaluation when checking patients’ oral health conditions.

Oral Examinations by the Dentist
A dentist carried out the oral examinations in a position convenient to the patient using a disposable dental instrument set(MORITA (Osaka, Japan), comprising a dental explorer, a mirror, and a pair of dental forceps) in the hospital ward under room
light and pen light (bright LED model BF-325BP, Panasonic).
The dentist examined the number of teeth, presence of dentures,
Community Periodontal Index (CPI) (7), and oral conditions.
The number of present teeth by age and sex were comparedwith data from the 2016 Survey of Dental Disease, conductedby the Japanese Ministry of Health, Labor and Welfare (2016Survey of Dental Diseases).
To assess the periodontal condition simply, the CPI (7) was
determined using a disposable probe approved by the World
Health Organization (YDM, Tokyo Japan) (after ethylene oxide
gas sterilization). The following 10 teeth were the targets of thisexamination : the upper and lower first and second molars, theright maxillary central incisor, and the left mandibular central
incisor (7). The dentist chose the highest applicable code fromthe following options (7) : 0 – no inflammatory findings in thegingiva ; 1 – bleeding at probing ; 2 – calculus deposition without
4 mm or greater pocket depth ; 3 – 4 to 5 mm pocket depth ; 4 – 6mm or greater pocket depth. The CPI code was determined as
the highest value at the six sites.
The oral conditions were examined and assessed on the following four items (yes, no) : 1 – “good condition ; please continue
your current oral care program” (no obvious dental problem wasfound in the present brief examination) ; 2 – “please brush each
tooth more carefully” (the patient was required to brush each
tooth more carefully because of his/her poor oral condition) ; 3 –“please get a dental checkup at least once a year” (it was not necessary for the patient to visit the dentist immediately following
the current brief examination, but it was recommended that he/she visit the dentist at least once a year) ; and 4 – “we recommend
dental visit and further dental examination because treatment isnecessary” (the patient had to visit a dentist as soon as possible
because the present brief examination was not sufficient to treat
their dental problems). During or after oral examinations, if thepatients asked questions about their oral conditions and behaviors

329

to the dentist, he answered them.

Statistical Analysis
Continuous variables with a normal distribution are expressed as mean ± standard deviation (SD) and those with askewed distribution as median (25th, 75th percentiles). Categorical variables are expressed as number and proportion (%). The
Mann-Whitney U test or Fisher’s exact test was used to compare
the demographic or clinical characteristics between each itemof the C-DiOHAT© (yes or no) where appropriate. The clinicalcharacteristics included periodontal condition (three categories : health (CPI 0), mild (CPI 1–2) or severe (CPI 3–4)), numberof present teeth (two categories : having more than the mean
number of present teeth by sex and age or not), and recommendation of dental visit (yes or no). The number of present teeth by sex
and age group were compared with the 2016 Survey of Dental
Diseases (8) (i.e., if the patient had more teeth than the mean
number of teeth in the 2016 Survey of Dental Diseases, “yes”
was chosen). Logistic regression analysis was used to assess thefactors associated with periodontal condition (CPI).
IBM SPSS Statistics versions 23.0 was used for all analyses.
The level of statistical significance was set at P < 0.05.

Ethical Approval and Consent
This study was conducted with the approval of the ClinicalResearch Ethics Committee of Tokushima University Hospital(approval no. 2113). Before acquiring consent to participate inthis study, first author explained the contents of the study using
documents approved by the ethics committee. Patients who
collaborated in this study fully understood its contents and they
provided voluntary verbal and written consent to participate inthis study.

RESULTSOut of 60 participants, two patients only participated in thequestionnaire survey (because they did not want their oralcavity examined). Regarding 58 patients, the CPI code wasdetermined for 55 patients, and oral conditions were examined
only for 54 patients.

Participants’ Characteristics
Participants’ characteristics are shown in Table 1. A total of
60 patients (male : 32, female : 28) were recruited. Their medianage was 58.5 (IQR 43.0 – 66.0) years ; their clinical diagnosis(diabetes type) included type 1 diabetes (n = 18), type 2 diabetes(n = 35), and others (n = 7) ; the median HbA1c was 8.8% (IQR
7.9 – 10.2) ; and the median duration of diabetes mellitus was
9.5 (IQR 1 – 18) years. With regard to their current treatment,
88.4% of patients use injections and with regard to additional
complications, 55% of patients have hypertension and 63.3% of
patients have dyslipidemia.
Regarding oral conditions, the CPI code for all participants
was over 2. No patients were CPI code 0. The patients’ data pertaining to the number of present teeth by sex and age group areshown in Table 2. The mean numbers of present teeth by sex andage group as per the 2016 Survey of Dental Diseases are also reported in this table for comparison. In the present study, for mostage groups, fewer than 60% of the patients had the mean numberof teeth reported in the 2016 Survey of Dental Diseases : 20s(50.0%), 30s (33.3%), 40s (37.5%), 50s (55.6%), 60s (42.1%), 70s(50.0%), and 80s (50.0%).

Nurse Assessment Using the C-DiOHAT©
The findings regarding oral health condition and oral healthY. Kuwamura, et al. Assessing the oral health330
Table 1. Patients’ Characteristics(n = 60)
Median

IQR

Min

Max
81

Age (yr)

58.5

43.0 - 66.0

21

Duration of diabetes mellitus1) (yr)9.5

1.0 - 18.0036

Age at diagnosis (yr)44.5

35.0 - 55.0

474

HbA1c level (%)

8.8

7.9 - 10.2

5.3

16.7

The number of present teeth2)

23.5

17.8 - 27.0032Community Periodontal Index : CPI3)

3.0

2.0 - 3.0

2

4

n

(%)

Male

32

53.3

Female28

46.7

Type 1 diabetes mellitus (T1DM)

18

30.0

Type 2 diabetes mellitus (T2DM)

35

58.3

Other

7

11.7

Oral hypoglycemic agent alone

7

11.7

Injections alone

28

46.7

Combination therapy

25

41.7

Diabetic neuropathy

29

48.3

Diabetic retinopathy

21

35.0

Angina pectoris, myocardial infarction

7

11.7
15.0

Sex
Clinical diagnosis

TherapyComplications

Denture2)

CPI code3)

Cerebral (brain) infarction

9

Diabetic foot ulcers

4

6.7

Periodontitis

6

10.0

Hypertention

33

55.0

Dyslipidemia

38

63.3

No denture

39

52.7

Only partial denture

14

18.9

Only full denture2

2.7

Both full and partial denture

3

4.1

0

0

0

1

0

0

2

19

34.5

3

23

41.8

4

13

23.6

1) There were 14 patients (23%) who were diagnosed for less than 1 year.
2) Only 58 patients agreed to have their total number of teeth and dentures checked.
3) Only 55 patients agreed to have their CPI code checked.

Table 2. Peresent teeth by age and sex, compared with data from the 2016 Survey of Dental Diseases, conducted by Japanese Ministry of
Health, Labor and Welfare

Age
Mean number of present teeth1)(Total number of the patientsin the age group)

Total

20-29 yr

30-39 yr

40-49 yr

50-59 yr

60-69 yr

70-79 yr

> 80 yr20.8 ± 8.2(n = 58)26.2(n = 6)22.3(n = 6)26.3(n = 8)22.3(n = 9)19.3(n = 19)13.3(n = 8)14.5(n = 2)

Number of the patients who have more teeth than
2016 Survey of Dental Disease2)(% of the total number in each aged group)3(50.0%)

2(33.3%)

3(37.5%)

5(55.6%)

8(42.1%)

4(50.0%)

1(50.0%)

Mean number of teeth by sex and age group in the2016 Survey of Dental Diseases

Age : 20-24
Men ; 29.2,
Women ; 28.3
Age : 25-29
Men ; 29.0,
Women ; 28.6

Age : 30-34
Men ; 28.8,
Women ; 28.5
Age : 35-39
Men ; 28.8,
Women ; 28.4

Age : 40-44
Men ; 28.0,
Women ; 28.0
Age : 45-49
Men ; 27.6,
Women ; 27.6

Age : 50-54
Men ; 25.8,
Women ; 26.8
Age : 55-59
Men ; 24.5,
Women ; 25.9

Age : 60-64
Men ; 23.7,
Women ; 24.0
Age : 65-69
Men ; 21.5,
Women ; 21.7

Age : 70-74
Men ; 18.6,
Women ; 20.7
Age : 75-79
Men ; 18.5,
Women ; 17.6

Age : 80-84
Men ; 15.1,
Women ; 15.5
Age : 85-89
Men ; 12.0,
Women ; 9.5

1) Only the patients who agreed to get the data of the total number of teeth were included.
2) The 2016 Survey of Dental Diseases shows the average number of present teeth by sex and age group in individuals. In this comparison, the values corresponding to
the number of present teeth were rounding to the nearest whole number, according to the first decimal place. (e.g.) If 27.6 was shown in it, it was compared as 27 teeth.

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The Journal of Medical Investigation Vol. 66 August 2019behavior using the C-DiOHAT© are shown in Table 3. Only 16
patients (26.7%) could bite firmly with the molars and dentures.
Less than approximately 40% of patients were found to engage
in oral hygiene behavior, e.g., the number of patients who usedsupplementary tools (e.g., interdental brush, dental floss) was 23(39.0%), although 65.0% of them had “experience of receiving instructions for brushing”, and 49 patients (81.7%) had “knowledgeof the relationship between periodontal disease and systemic
diseases, including diabetes”. Regarding “sharing health information among patients and dental/medical professionals”, thepercentage showing their personal health records for diabetes/
medications to their dentists was 13.3% and 10.0%, respectively.

Comparison between the C-DiOHAT© and HbA1c Levels
As is evident from Table 3, the HbA1c level was lower among
patients who responded “yes” to the items “experience of receiving instructions for brushing by a dentist” (P = 0.001), “dental
visits more than once a year” (P = 0.048), “checking one’s mouthwith a mirror” (P = 0.020), “toothbrushing carefully” (P = 0.015),

and “notification of dental condition to their primary doctor” (P =0.025) than those who responded “no”.

Oral Examination by a Dentist
The CPI code and the number of teeth have already shown in
Table 1 and Table 2, respectively. As shown in Table 4, the dentist evaluated 45 patients (83.3%) as needing to brush their teeth
more carefully and 36 patients (66.7%) as being recommended
dental visits. Some patients asked the dentist about problems
with the teeth or dentures, brushing technique, oral health tools(i.e. ; toothbrush, mouthwash, etc.), and so on. Some patients said
they would like to treat their teeth, but they could not because of
systemic disease.

Relationship between the Nurse’s Oral Assessment Using the CDiOHAT© and the Dentist’s Oral Examination
As shown in Table 5, the number of present teeth by sex andage was significantly associated with greater “use of supplementary tools” (P = 0.013). In addition, the dentist’s recommendation

Table 3. Relationships between nursing assessment with C-DiOHAT© and age / HbA1c / sexn (%)
60 (100%)

Items of assessment

Age
MediamIQR1)

59

43 - 66

HbA1c
P-value2)

MediamIQR1)

8.8

7.9 - 10.2

Sex
P-value2)

Men

Women

P-value3)

32 (53.3%) 28 (46.7%)

Factor 1 : Oral health conditions
Symptom of gingival swelling
Bleeding during toothbrushing
Awareness of halitosis
Biting firmly on molar or denturesNo

21 (35.0%)

59

41 - 66Yes

39 (65.0%)

58

43 - 71

No

35 (58.3%)

64

49 - 69Yes

25 (41.7%)

50

35 - 59

No

37 (61.7%)

63

43 - 67Yes

23 (38.3%)

53

43 - 64No

44 (73.3%)

59

43 - 66Yes

16 (26.7%)

59

48 - 710.467
0.002 *
0.233
0.865

8.80

7.80 - 10.55

8.95

7.85 - 9.98

8.80

7.70 - 10.10

8.95

7.95 - 10.28

8.70

7.90 - 10.55

9.10

7.63 - 9.98

8.75

7.70 - 10.05

9.80

8.40 - 10.30

0.872

11 (34.4%) 10 (35.7%)

1.000

21 (65.6%) 18 (64.3%)
0.745

20 (62.5%) 15 (53.6%)

0.331

12 (37.5%) 13 (46.4%)
0.997

23 (71.9%) 14 (50.0%)

0.112

9 (28.1%) 14 (50.0%)
0.065

24 (75.0%) 20 (71.4%)
8 (25.0%)

0.778

8 (28.6%)

Factor 2 : Oral hygiene behaviors
Experience of receiving instructions for brushing
Dental visits more than once a year
Checking one’s mouth with a mirror
Use of supplementary tools (e.g., interdental brush,dental floss)4)
Toothbrushing carefully5)No

21 (35.0%)

55

41 - 64Yes

39 (65.0%)

61

48 - 67No

34 (57.6%)

54

43 - 65Yes

25 (42.4%)

63

41 - 68

No

35 (58.3%)

54

43 - 67Yes

25 (41.7%)

61

42 - 66

No

36 (61.0%)

55

39 - 67Yes

23 (39.0%)

59

49 - 66

No

38 (63.3%)

63

47 - 67Yes

22 (36.7%)

54

32 - 65

0.204
0.354
0.757
0.490
0.185

10.15

8.80 - 10.90

8.30

7.50 - 9.80

9.60

8.25 - 10.70

8.30

7.60 - 9.75

9.70

8.00 - 10.80

8.40

7.75 - 9.10

9.50

8.10 - 10.60

8.40

7.33 - 9.63

9.60

8.20 - 10.70

8.20

7.00 - 9.38

0.001 **

9 (28.1%) 12 (42.9%)

0.284

23 (71.9%) 16 (57.1%)
0.048 *

16 (50.0%) 18 (66.7%)
16 (50.0%)

0.020 *

0.290

9 (33.3%)

22 (68.8%) 13 (46.4%)

0.116

10 (31.3%) 15 (53.6%)
0.096

17 (53.1%) 19 (70.4%)
15 (46.9%)

0.015 *

0.194

8 (29.6%)

19 (59.4%) 19 (67.9%)
13 (40.6%)

9 (32.1%)

5 (15.6%)

6 (21.4%)

0.595

Factor 3 : Perceptions and knowledge of oral health behaviors
Knowledge of a relationship between periodontal
disease and systemic disease including diabetes
Perceptions of oral care (e.g., brushing teeth,
washing denture, gargling) efficacy regardless oftiming of care initiationNo

11 (18.3%)

58

38 - 66Yes

49 (81.7%)

59

43 - 67

No

24 (40.0%)

61

37 - 73Yes

36 (60.0%)

57

44 - 65

0.825
0.526

10.10

8.00 - 10.90

8.80

7.75 - 9.90

8.70

7.90 - 9.80

9.40

7.78 - 10.63

0.410

0.740

27 (84.4%) 22 (78.6%)
0.179

14 (43.8%) 10 (35.7%)

0.603

18 (56.3%) 18 (64.3%)

Factor 4 : Sharing health information among patients and dental / medical professionals
Showing personal health record nootbook for diabetes
to the dentist
Showing personal health record nootbook for
medication to the dentist
Showing self-monitoring blood glucose notebook to
the dentist6)
Notification of dental condition to their primary
doctorNotification of dental condition to their primary
nurse

No

52 (86.7%)

58

43 - 66Yes

8 (13.3%)

61

50 - 73No

54 (90.0%)

59

45 - 66Yes

6 (10.0%)49

32 - 72No

49 (92.5%)

61

43 - 68

Yes

4 (7.5%)54

49 - 62No

52 (88.1%)

56

39 - 66Yes

7 (11.9%)

67

58 - 76No

56 (94.9%)

60

43 - 67

Yes

3 (5.1%)58

50 - 66

0.382
0.723
0.609
0.055
0.903

9.20

7.90 - 10.40

8.20

7.75 - 8.73

9.10

7.90 - 10.35

7.90

6.93 - 9.05

9.00

7.75 - 10.63

8.80

8.05 - 9.63

9.20

7.90 - 10.30

7.70

7.10 - 8.50

8.80

7.90 - 10.20

7.10

6.70 - 8.50

0.135

29 (90.6%) 23 (82.1%)
3 (9.4%)0.095

31 (96.9%) 23 (82.1%)
1 (3.1%)

0.697
0.025 *
0.081

0.692

4 (14.8%)

31 (96.9%) 25 (92.6%)
1 (3.1%)1.000

2 (7.1%)29 (90.6%) 23 (85.2%)
3 (9.4%)0.088

5 (17.9%)23 (92.0%) 26 (92.9%)
2 (8.0%)0.454

5 (17.9%)

0.588

2 (7.4%)1) IQR : interquartile range ; 2) Mann-Whitney test, **P < 0.01, *P < 0.05 ; 3) Fisherʼs exact test (two-tailed) ; 4) Participants with more than a tooth (dentulous ; n = 59),
as they can use supplementary tools if they have one or more teeth ; 5) Patients with edentulous jaw answered questions about brushing dentures ; 6) Only patients who
used injected medications.

332

Y. Kuwamura, et al. Assessing the oral health

Table 4. Diagnostics results of dental examinations(n = 54)

Evaluation items

Yes

No

Good condition ; please continue your current oral care program.

9 (16.7%)

45 (83.3%)

Please brush each tooth more carefully.

45 (83.3%)

9 (16.7%)

Please get a dental checkup at least once a year.

18 (33.3%)

36 (66.7%)

We recommend dental visit and further dental examination because treatment is necessary.
(Recommendation of dental visit)

36 (66.7%)

18 (33.3%)

Table 5. Relationships between nursing assessment with C-DiOHAT© and oral examinations conducted by a dentist (periodontal disease(CPI), number of present teeth by sex and age group, and recommendation of dental visit)
Periodontal disease (CPI)1)
Mild
Severe(CPI = 1,2) (CPI = 3,4) P-value3)(%)(%)
19 (34.5%)

Items of assessment

36 (65.5%)

Number of present teeth by sex
and age group2)NoYes

32 (55.2%)

26 (44.8%)

P-value3)

Recommendation of dental visit
NoYes

18 (33.3%)

36 (66.7%)

P-value3)

Factor 1 : Oral health conditions
Symptom of gingival swelling
Bleeding during toothbrushing
Awareness of halitosis
Biting firmly on molar or denturesNo

8 (42.1%)

12 (33.3%)Yes

11 (57.9%)

24 (66.7%)

No

12 (63.2%)

20 (55.6%)Yes

7 (36.8%)

16 (44.4%)No

12 (63.2%)

20 (55.6%)Yes

7 (36.8%)

16 (44.4%)

No

16 (84.2%)

25 (69.4%)Yes

3 (15.8%)

11 (30.6%)

0.566

9 (28.1%)

11 (42.3%)

23 (71.9%)

15 (57.7%)

19 (59.4%)

14 (53.8%)

13 (40.6%)

12 (46.2%)

0.775

21 (65.6%)

14 (53.8%)

11 (34.4%)

12 (46.2%)

0.334

21 (65.6%)

21 (80.8%)

11 (34.4%)

5 (19.2%)

0.775

0.282
0.791

10 (55.6%)

9 (25.0%) 0.037 *

8 (44.4%)

27 (75.0%)

13 (72.5%)

17 (47.2%) 0.145

5 (27.8%)

19 (52.8%)

0.425

10 (55.6%)

22 (61.1%) 0.773

8 (44.4%)

14 (38.9%)

0.246

15 (83.3%)

24 (66.7%) 0.334

3 (16.7%)

12 (33.3%)

Factor 2 : Oral hygiene behaviors
Experience of receiving instructions for brushing
Dental visits more than once a year
Checking one’s mouth with a mirror
Use of supplementary tools (e.g., interdental brush,dental floss)4)
Toothbrushing carefully5)No

6 (31.6%)

13 (36.1%)

Yes

13 (68.4%)

23 (63.9%)No

9 (47.4%)

22 (61.1%)

Yes

10 (52.6%)

14 (38.9%)No

12 (63.2%)

21 (58.3%)

Yes

7 (36.8%)

15 (41.7%)

No

11 (57.9%)

22 (61.1%)Yes

8 (42.1%)

14 (38.9%)No

9 (47.4%)

26 (72.2%)

Yes

10 (52.6%)

10 (27.8%)

0.775
0.397
0.779
1.000
0.084

13 (40.6%)

7 (26.9%)19 (59.4%)

19 (73.1%)

21 (67.7%)

12 (46.2%)

10 (32.3%)

14 (53.8%)

17 (53.1%)

17 (65.4%)

15 (46.9%)9 (34.6%)

24 (77.4%)

11 (42.3%)

7 (22.6%)

15 (57.7%)

22 (68.8%)

14 (53.8%)

10 (31.3%)

12 (46.2%)

0.405
0.115
0.426
0.013 *
0.285

3 (16.7%)

16 (44.4%) 0.069

15 (83.3%)

20 (55.6%)

8 (44.4%)

23 (63.9%) 0.245

10 (55.6%)

13 (36.1%)

10 (55.6%)

22 (61.1%) 0.773

8 (44.4%)

14 (38.9%)

7 (38.9%)

26 (72.2%) 0.036 *

11 (61.1%)

10 (27.8%)

9 (50.0%)

26 (72.2%) 0.136

9 (50.0%)

10 (27.8%)

Factor 3 : Perceptions and knowledge of oral health behaviors
Knowledge of a relationship between periodontal
disease and systemic disease including diabetes
Perceptions of oral care (e.g., brushing teeth,
washing denture, gargling) efficacy regardless oftiming of care initiationNo

6 (31.6%)

3 (8.3%)Yes

13 (68.4%)

33 (91.7%)No

9 (47.4%)

14 (38.9%)Yes

10 (52.6%)

22 (61.1%)

0.051
0.577

3 (9.4%)6 (23.1%)

29 (90.6%)

20 (76.9%)

15 (46.9%)

8 (30.8%)

17 (53.1%)

18 (69.2%)

26 (81.3%)

25 (96.2%)

6 (18.8%)

1 (3.8%)1.000

28 (87.5%)

24 (92.3%)

4 (12.5%)

2 (7.7%)1.000

25 (89.3%) 23 (100.0%)
3 (10.7%)

0 (0.0%)0.157

26 (83.9%)

25 (96.2%)

5 (16.1%)

1 (3.8%)0.547

31 (100.0%)

24 (92.3%)

0 (0.0%)2 (7.7%)

0.274
0.283

4 (22.2%)

5 (13.9%) 0.461

14 (77.8%)

31 (86.1%)

6 (33.3%)

15 (41.7%) 0.768

12 (66.7%)

21 (58.3%)

17 (94.4%)

31 (86.1%) 0.651

Factor 4 : Sharing health information among patients and dental / medical professionals
Showing personal health record nootbook for diabetes
to the dentist
Showing personal health record nootbook for
medication to the dentist
Showing self-monitoring blood glucose notebook to
the dentist6)
Notification of dental condition to their primary
doctorNotification of dental condition to their primary
nurse

No

19 (100.0%)31 (86.1%)

Yes

0 (0.0%)5 (13.9%)

No

17 (89.5%)

33 (91.7%)

Yes

2 (10.5%)

3 (8.3%)No

18 (94.7%)

29 (96.7%)

Yes

1 (5.3%)1 (3.3%)

No

18 (100.0%)31 (86.1%)

Yes

0 (0.0%)5 (13.9%)

No

18 (100.0%)34 (94.4%)

Yes

0 (0.0%)2 (5.6%)

0.152

0.116

1 (5.6%)0.681

16 (88.9%)

0.242

17 (100.0%)

0.205

15 (83.3%)

0.204

17 (94.4%)

2 (11.1%)
0 (0.0%)3 (16.7%)
1 (5.6%)5 (13.9%)32 (88.9%) 1.000
4 (11.1%)
28 (90.3%) 0.543
3 (9.7%)33 (94.3%) 0.323
2 (5.7%)34 (97.1%) 1.000
1 (2.9%)1) Only 55 patients agreed to offer the CPI code data. CPI code 1 or 2 meant mild periodontal disease, CPI code 3 or 4 meant severe periodontal disease ; 2) 58 patients
who agreed to offer the data of the number of present teeth. 3) Fisherʼs exact test (two-tailed), **P < 0.01, *P < 0.05 ; 4) Participants with more than a tooth, as they canuse supplementary tools if they have one or more teeth. (dentulous patients : Shapiro-Wilk test ; P = 0.014) ; 5) Patients with edentulous jaw answered questions about
dentures brushing ; 6) Only patients who used injected medications.

333

The Journal of Medical Investigation Vol. 66 August 2019of dental visit was significantly associated with “no use of supplementary tools” (P = 0.036) and “symptoms of gingival swelling”(P = 0.037). CPI code was significantly associated with “knowledge of a relationship between periodontal disease and systemic
disease including diabetes” (P = 0.021) in Table 6.

DISCUSSION
In the present study, the oral health of in-patients with diabetes was assessed by a nurse using the C-DiOHAT© and by a dentist conducting the oral examination. Patients’ awareness of thesymptoms of gingival swelling was also significantly associatedwith recommendation of dental visit. Use of supplementary tools(e.g., interdental brush, dental floss) was significantly associatedwith the number of present teeth and no recommendation offurther dental visit.
Periodontal diseases are classified as gingivitis and periodontitis. The major symptoms of gingivitis are redness, swelling,
and bleeding. The item of “patients’ awareness of the symptoms
of gingival swelling” in C-DiOHAT© may be a useful predictorof oral health condition.
To prevent periodontal disease (9), both oral self-care (daily

self-performed oral health (e.g., toothbrushing, flossing, using interdental brush)) and oral professional care (regular professionalremoval of the microbial biofilm) are important.
Regarding oral self-care, 39.2% of the respondents performedinterdental cleaning with supplementary tools (8). Flossing in
addition to brushing has also been reported to reduce interproximal gingivitis (10). Even when compared with the resultsof previous research (11–13), the implementation rate found in
this study (39%) does not seem low. It stands to reason that thepatients who use supplementary tools have more teeth and fewer
dental problems. Therefore, these results suggest that the itemof “use of supplementary tools” in C-DiOHAT© may be a usefulpredictor of oral health condition.
Regarding oral professional care, 52.9% of the participants
had undergone a dental examination in the past year (14). Targets is 65% by 2022 (15). The present result was 42%. It wassuggested that patients with diabetes have to visit physicians
to treat diabetes once every 1–3 months, as well as make special visits in cases of diabetes complications or other diseases.
Therefore, it might be difficult to visit dentists. To encourage
patients to visit medical and dental clinics regularly, the diabetes information-sharing notebook (16) has been published by

Table 6. Logistic regression analysis for periodontal condition (CPI)
Independent variable1)

OR2)

Symptom of gingival swelling0 : NoP value4)

95%CI3)

1.44

0.41

5.01

0.57

3.71

0.83

16.64

0.09

2.81

0.68

11.67

0.15

2.93

0.61

14.09

0.18

0.53

0.14

2.00

0.35

0.36

0.10

1.34

0.13

1.65

0.45

6.01

0.45

0.57

0.16

2.06

0.39

0.36

0.10

1.37

0.13

7.61

1.35

42.86

0.02 *

1.80

0.51

6.33

0.36

1.39

0.18

10.89

0.75

0.56

0.03

10.81

0.70

1 : Yes
Bleeding during toothbrushing0 : No1 : Yes

Awareness of halitosis

0 : No1 : Yes

Biting firmly on molar or dentures

0 : No1 : Yes

Experience of receiving instructions for brushing0 : No1 : Yes

Dental visits more than once a year

0 : No1 : Yes

Checking one’s mouth with a mirror

0 : No1 : YesUse of supplementary tools (e.g., interdental brush, dental floss)

5)

0 : No1 : Yes

Toothbrushing carefully6)

0 : No1 : Yes

Knowledge of a relationship between periodontal disease andsystemic disease including diabetes
Perceptions of oral care (e.g., brushing teeth, washing denture,
gargling) efficacy regardless of timing of care initiation
Showing personal health record nootbook for diabetes to the dentist7)

0 : I donʼt know.
1 : I know.
0 : I donʼt know.
1 : I know.
0 : No1 : YesShowing personal health record nootbook for medication to thedentist0 : NoShowing self-monitoring blood glucose notebook to the dentist8)

0 : No1 : Yes
1 : Yes

Notification of dental condition to their primary doctor7)

0 : No1 : Yes

Notification of dental condition to their primary nurse7)

0 : No1 : Yes

1) Independent variables are dummy ; 2) OR : odds ratio ; 3) 95%CI : 95% confidence interval. 4) Dependent variable : Community Periodontal Index (CPI) : 0 : CPI = 1
or 2, 1 : CPI = 3 or 4 ; Age and gender were adjusted ; *P < 0.05 ; 5) Participants with more than a tooth, as they can use supplementary tools if they have one or moreteeth. ; 6) Patients with edentulous jaw answered questions about dentures brushing ; 7) In this variable, it was not applicable to calculate OR ; 8) Only patients who
used injected medications.

334

Y. Kuwamura, et al. Assessing the oral health

the Japan Association for Diabetes Education and Care since2010. It is expected to help the diabetes cure/care team members develop interdisciplinary relationships. In a previous study(17), 35.1% of the patients provided their dentist with clinicaldata pertaining to their HbA1c level, and 43.9% reported their
ongoing medical treatment. It is suggested that patients may
not manage their physical information appropriately. There isa high risk of incomplete healing of wounds or infection during
dental treatment when the patient has hyperglycemia (18). After
dental treatment, the patient might be unable to eat meals at
the usual time (because of the use of anesthesia for dental treatment) and thereby become hypoglycemic. Furthermore, if patients cannot chew foods easily because of dental problems, they
will have to consume only soft meals (19) and soft drinks (20),which may lead to hyperglycemia through an increase in foodintake (19). These days, medical professionals share patients’
information with each other as part of their medical team (21,22). Person-centered care for the self-management of diabetes(23) is important. It is suggested that educational programs forpatients are recommended so that patients can manage theirown medical and dental information, understand their disease(including its stages and trajectory), and engage in self-management behavior.
Regarding knowledge of periodontal disease and systemic
diseases such as diabetes, it was reported that “people with diabetes have inadequate oral health knowledge, poor oral healthattitudes, and fewer dental visits (24)”. The patients’ knowledge
was higher in the present study (81.7%) than the other (30% (25),
32% (12)). Therefore, when patients with severe oral problems
visit dentists, the dentists might explain to them that theiroral condition could worsen owing to diabetes and encouragethem to develop their knowledge about their condition. Patients
will be prepared for disease complications if nurses educate
them early. As for oral care, nurses should discuss how they
can help patients avoid getting worse and what they can do toimprove patients’ oral self-management. In a previous study(4,5), several nurses reported that they wished to conduct quickoral assessments because in real clinical settings they have to
educate patients about several other aspects of the disease. Not
surprisingly, the present study found significant relationships
between the items of C-DiOHAT© (“use of supplementary tools”)
and the dentist’s examination (“number of present teeth by sex
and age” and “dentist’s recommendation of dental examination”).
The item “experience receiving instructions for brushing” had asignificant relationship with HbA1c levels. These results suggestthat nurses could utilize assessment items of the C-DiOHAT© toeffectively acquire useful information about patients’ oral healthconditions and behaviors. The authors think that the role of thenurse in oral care is to help the patients in their daily care andself-management.
On the other hand, the salivary multi-test system (26, 27) was
developed to assess oral health. One (28) such test requires thatpatients not eat or drink and not engage in oral cleaning for atleast 2 hours before the examination. These requirements may
be difficult for patients with diabetes, who tend to feel thirsty
and who need to keep drinking fluids to prevent cerebral complications. Therefore, assessment items of the C-DiOHAT© seem
useful in assessing patients’ oral health conditions in a shorttime frame in clinical settings.
CPI was significantly influenced by the duration of diabetes,
fasting blood glucose levels, and HbA1c levels (2). In the present
study, participants were in-patients receiving serious medicalcare. Naturally enough, all patients may have periodontal disease (the CPI codes of all patients exceeded 2.0), and the ratiosof mild to severe periodontal disease were one (34.5%) to two(65.5%). These things may be one of the reasons that there wasno association between the CPI code and each assessment item of
the C-DiOHAT© except for “knowledge of a relationship between
periodontal disease and systemic disease including diabetes”.
Furthermore, these things may be a reasons that the patients
who had more “knowledge of a relationship between periodontal
disease and systemic disease” had higher CPI code. However,further research should consider when the patients got the“knowledge of a relationship between periodontal disease andsystemic disease including diabetes”.
Regarding oral care by nurses (29–34), it has been pointed outthat nurses lack knowledge of oral health care (35). And nurses
need to know that many patients want to get knowledge about
oral health. They also acknowledge the importance of interprofessional and collaborative education between medicine/nursing
and dentistry (30). The need for dental hygiene registration
by nurses was also reported (36). It is important to encouragenurses to be interested in patients’ oral health conditions andbehaviors.

STUDY LIMITATIONS
Several limitations of this study should be acknowledged.
First, this survey was conducted with a small number of in-patients in one university hospital with medical and dental clinics.
Therefore, the study’s statistical power might be limited. Second,
the patients who consented to participate in the study may have
had high interest in oral care. Thus, the representativeness ofthe sample may be questioned, the findings cannot be generalized. Third, only the CPI code was used to examine the severityof periodontal disease, and X-rays were not used to diagnose thesame accurately. Fourth, the CPI code for all participants wasover 2. Further research should include participants of every
level of periodontal disease. Fifth, “checking the inside of thepatient’s mouth”, which is the items of DiOHAT©, was excluded
from the questionnaire. However, further research should consider which information regarding the oral cavity nurses need to
be able to observe. Finally, further research should also consider
when the patients got the “knowledge of a relationship between
periodontal disease and systemic disease including diabetes”.

CONCLUSION
According to the dentist’s oral examination, the CPI code forall the in-patients was over 2, indicating that all of them may
have had a periodontal disease. Further, the patients who had
the present number of teeth by sex and age use more supplementary tools (e.g., interdental brush, dental floss) for oral carethan those who did not. Thus, patients who used supplementary
tools were less likely to require further dental examination thanthose who did not. Similarly, patients who visited dentists once a
year had more teeth and a lower HbA1c level than patients who
did not. The dentist’s recommendation of further dental examination (need for dental treatment) was related to the patient’s
awareness of the symptoms of gingival swelling, and use of supplementary tools. However, the patients who had “knowledge ofa relationship between periodontal disease and systemic disease
including diabetes” were significantly higher CPI code. Regarding this, further research should also consider when the patients
got the knowledge.
The following assessment items of the C-DiOHAT© wereclosely related to the dentist’s oral examinations : “use of supplementary tools”, “symptom of gingival swelling”, and “knowledgeof a relationship between periodontal disease and systemic
disease including diabetes”. These results suggest that nurses

The Journal of Medical Investigation Vol. 66 August 2019should prioritize these assessment items to most quickly acquire
useful information about patients’ oral health conditions andbehaviors. It is important to encourage nurses to be interested
in patients’ oral health conditions and behaviors by such small
pile of clue.

ACKNOWLEDGMENT
This work was supported by Japan Society for the Promotion of
Science (JSPS), JSPS KAKENHI Grant Number JP26463305,
and a Grant-in-Aid for Scientific Research (C).
We would like to express our deepest gratitude to all the patients for participating in this study and for encouraging us. We
would like to offer our thanks to nurses and doctors in chargeof diabetes wards. We would also like to thank, Emeritus Professor, Toshihiko Nagata in the Department of Periodontology,
Tokushima University Graduate School of Biomedical Sciences.

AUTHOR CONTRIBUTIONSYK contributed to the study design, creation of the questionnaire, data collection, analysis, writing and approving the paper.
ES contributed to data collection, analysis, and final approvalof the paper. MS contributed to the study design, creation of thequestionnaire, analysis, and final approval of the paper. MM
contributed to the study design, analysis and final approval of
the paper. DH, HU, and SK contributed to the analysis and final
approval of the paper.

COMPLIANCE WITH ETHICAL STANDARDSCONFLICT OF INTEREST
The authors have no conflict of interest to declare.

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