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Oral Health Conditions in Patients with Parkinson’s Disease

BACKGROUND: Oral health conditions and related factors of patients with Parkinson’s disease (PD) have not been well elucidated. The aim of the present study was to investigate oral health conditions and related factors which may influence oral health conditions among patients with PD. METHODS: We compared oral health conditions and related factors between 104 PD patients and 191 inhibitants (controls) who received dental health check-ups in Hokkiado, Japan. The unconditional logistic regression model was used for adjusting for sex and age. We also conducted stratified analysis by sex and age group using this model. The χ2 test and the Cochran-Mantel-Haenzel test were used for simple and stratified analyses of knowledge of oral health among PD patients, respectively. RESULTS: In the present survey, we found the following results. (1) PD patients had more complaints of chewing difficulties and denture discomfort than controls. (2) Fewer PD patients had their own teeth than controls regardless of sex. (3) Fewer PD patients cleaned their dentures every day than controls, regardless of sex or age. (4) More than half of the PD patients had problems with swallowing. CONCLUSION: We found that PD patients had more complaints about their oral health and more problems in oral health behavior than the general population. These findings may provide useful information for the caregivers of PD patients to conduct oral health care as well as for making oral health plans for PD patients and for medical and welfare services.

There is no established medical treatment to completely cure intractable diseases (i.e., Nanbyo in Japanese) because their etiologies remain unknown. Thus, patients with intractable diseases may suffer from disabilities even after treatment. As the clinical course is chronic, patients with intractable diseases need longlasting medical treatment and care, which causes a heavy burden for the patients themselves as well as their family members, not only mentally but also financially.
Patients with Parkinson's disease (PD), which is one of the most common intractable diseases, suffer from disabilities of walking, eating, biting, swallowing, using the toilet, communicating, or respiration through muscle weakness, or disability of movement, in addition to abnormal eye symptoms and autonomic nervous system disorders. 1,2 Patients with dysphagia, dental diseases and/or poor oral hygiene have been shown to have a high incidence of aspiration pneumonia, [3][4][5][6][7][8] which may sometimes lead to death, 5,[9][10][11] Therefore, it is important for patients with neuro-genic disorders to maintain good oral hygiene.
However, their oral health conditions and related factors, such as oral complains, tooth brushing, condition of swallowing, knowledge of oral health, frequency of having a checkup in a dental clinic, and so on, have not been clearly elucidated.
To the best of our knowledge, only a few surveys of oral health conditions in PD patients have been reported, and only the small numbers of PD patients were surveyed in these studies. [12][13][14] Persson et al. 12 compared only 30 PD patients with controls, while Nilsson et al. 13 compared 75 PD patients with controls. However, they did not investigate the oral health conditions, but only the swallowing situation.
Patients with dyskinesia of the hands and/or face often suffer from poor oral hygiene. Patients with PD may be a high-risk group for caries and periodontal disease, and may have more complains of poor oral health and more health problems in the oral cavity than the general population.
The aim of the present study was to investigate oral health conditions and related factors that may influence oral health among patients with PD.

Subjects
In Japan, patients with PD can receive public financial aid from the government if their disease stage according to Hoehn and Yahr is from III to V, 15 and the eligible study cases were all of 240 patients with PD who received public financial aid in the Okhotsk area, in 2000. Okhotsk is located in the eastern part of Hokkaido, and is one of tertiary medical-care zones in Hokkaido. Among them, 201 PD patients participated in a meeting held in the city of Abashiri or were certified in the cities of Kitami and Monbetsu. They were asked to take part in this survey, and 109 patients responded (response rate, 54.2%). We used 104 patients aged over 60 years as cases. In 2001, 422 persons got dental check-ups in basic health examinations of cities and towns in Okhotsk. We selected 191 persons aged over 60 years as controls. Sex and age distribution of the 104 cases with PD and 191 controls are shown in Table 1.

Method of Survey
During the period spanning January through March in 2000, we investigated the patients with PD mostly by mail (196 patients), and in part, by interview (5 patients). A structured questionnaire was employed for both patients and controls. As shown in Appendix, common questions in the survey for patients and controls were about oral complains, the presence of their own teeth, tooth brushing, denture condition, and the presence of a family dentist. Question items for all cases and controls were bad breath, swollen gums, chewing difficulties, the presence of their own teeth, and the presence of a family dentist. Those for people with dentures were denture discomfort and denture condition. People having own teeth were asked about toothache, gingival bleeding, food impaction, tooth movement, and tooth brushing. In addition, disability in brushing, the condition of swallowing, having a checkup in a dental clinic, and knowledge of oral health were surveyed among PD patients. A dentist in the Kitami Public Health Center of Hokkaido (the first author) examined the teeth of the       The present study revealed that more PD patients complained of denture discomfort, in particular female patients. This result was consistent with the report by Kieser et al. 21 suggesting that a third of PD patients have loose dentures or poor denture control. This may be explained by the following reasons. First, PD patients may be suffering from oral dyskinesia 7,19 or xerostomia 20 caused by the use of anticholinergics. Second, PD patients may be suffering from lack of muscle coordination and rigid facial muscles that jeopardize denture retention and control 20 . Many female, but not so many male, PD patients complained of denture discomfort. It is possible that, compared with male PD patients, female PD patients might suffer from denture discomfort caused by involuntary movements of some facial muscles, the tongue and lips, as oral dyskinesia is more commonly seen in elderly woman than in elderly men 4,7 .
The present study showed that many PD patients did not have their own teeth, regardless of sex. This result was the opposite of the results of studies reported in Europe showing that caries were generally less common in PD patients than in controls, and that teeth were retained longer in PD patients than in controls. 12,18 This may be explained by the following possibilities. Many PD patients in the present survey had lost their teeth due to many years of poor oral hygiene because fewer PD patients brushed their teeth every day or they had difficulty going to a dental clinic in the early stage of caries. The results of the present study may suggest that the support for oral health for PD patients in Japan remains less sufficient than in Europe.
Because PD patients often suffer from heartburn and nausea, causing a decrease in oral hygiene 6,21 as well as xerostomia, leading to an increased risk of caries due to the use of anticholinergics or monoamine oxidase inhibitors, 18-21 PD patients may have a high risk of losing their teeth.

Swallowing among PD patients
Fifty-six of the 104 (54%) PD patients had some subjective problems swallowing. In western countries 6,20,22 about half of PD patients are reported to have dysphagia. However, we may have underestimated the proportion of the PD patients with dysphagia in the present study because of the following reasons. First, several studies have revealed that PD patients have swallowing difficulties without any subjective symptoms. 5,11,13,23 Second, Nilsson et al. 13 found dysphagia in more than 90% of PD patients who were in the same stages as our study subjects (Hoehn and Yahr stages III and IV). Most of the PD patients in the present survey Fewer PD patients cleaned their dentures every day than in the control group after adjustment for sex and age (OR = 10.5, 95% CI:2.9-37.3). Fewer PD patients cleaned their own dentures every day than controls in both sexes. Fewer PD patients cleaned their dentures every day than controls in both the young and old elderly after adjusting for age and sex.
There were no differences between the PD patients and the control group about storing their own dentures correctly before sleeping. Forty-five PD patients (56%) removed their own dentures and put them in a cup of water before sleeping.
More PD patients complained of food impaction than controls after adjustment for sex and age. Among the young elderly, more PD patients complained of food impaction than controls after adjusting for age.
Fewer PD patients brushed their teeth every day than in the control group (p<0.01), in both sexes (p<0.01), and in both the young and old elderly (p<0.01).

Knowledge and condition of oral health among PD patients
Few PD patients had knowledge of dental floss (3%), brushes for cleaning dentures (19%) and coating of the tongue (14%). Table 3 shows oral-health conditions among 104 PD patients. Fifty-one PD patients (49%) had trouble brushing their teeth or cleaning their dentures, 38 patients (37%) had difficulty gargling. As for swallowing, 56 PD patients (54%) answered that they had some problems. Among the 60 patients who had their own teeth, 21 (35%) had trouble brushing by themselves. Among 80 PD patients who had dentures, 10 (13%) had some problems about either removing or putting them in by themselves. Concerning regular checkups of their dentures, 24 PD patients (30%) had never gone to a dental clinic after they had been made. Seven patients (7%) had been refused treatment in a dental clinic due to their disease. Fifty patients (48%) answered that they were able to go to a dental clinic if there was assistance by either family members or helpers, and transportation service by car, and 10 (10%) could not go to a dental clinic in any case. Of these 10 patients, 9 (90%) wanted to use home-visiting dental services. As for the content of home-visiting dental service, 62 patients (60%) wanted to have a dental check-up and tooth brushing instruction either at present or in the future.
As far as we know, this is the first study of oral health conditions in PD patients compared with controls in Japan. Although Fukayo 14 reported about oral health conditions of PD patients, they did not compare them with controls.

The oral health conditions of 104 PD patients
In the present study, those who complained of chewing difficulties were more common among PD patients than controls after adjustment for sex and age. This indicated that chewing difficulties might be common in PD patients. This may be explained by may have had poor oral hygiene, because only a few of them brushed their teeth every day. Therefore, they might be susceptible to aspiration pneumonia via aspiration of saburra and indigenous oral bacterial flora. 5,6,11,23 In addition, most elderly PD patients may have a high risk of severe aspiration pneumonia because elderly people are more likely to contract oral candidiasis 7,8 and fatal moniliasis pneumonia 8 when they have poor oral hygiene and denture discomfort. Bucbboz 24 reported that the most common cause of death among progressive PD patients was aspiration pneumonia.

Oral health behavior of PD patients
We found that very few PD patients brushed their teeth every day or cleaned their dentures every day. They probably had difficulties because of their PD symptoms such as resting tremors, akinesia and bradykinesia. [20][21][22]25,26 Even though most PD patients complained of food impaction, few PD patients had knowledge about the interdental brush. Therefore, it is very important for PD patients to get appropriate dental health advice from a dentist or dental hygienist, especially from their own family dentists. This is consistent with the report by Kieser et al. 21 who recommended that patients with neurodegenerative disorders should be followed by the same dentist.
However, most PD patients wanted to have dental treatment and dental health services by home visits because it was very difficult for them to receive those services at dental clinics unless their families took them there. Fiske et al. 20 reported that domiciliary dental care was important for PD patients because one of the major barriers to receive dental care was access to dental premises.
The results of the present study may show that many kinds of support (e.g., environmental considerations and advice on oral care for families of PD patients and their caregivers, usual support of oral care at the home by a welfare agency such as a home nursing station, special transport service to go to the dental clinic, and an increase of dental clinics doing dental treatment by home visits) are necessary for PD patients to maintain good oral health conditions, to prevent aspiration pneumonia and to have good quality of life.
There are some limitations to our study. First, information on most PD patients was obtained by mail; only 5 PD patients were interviewed. Because information of mailed self-administered questionnaire may be inferior to one by personal interview in quality, there is a possibility of information bias to some extent in our study. Second, we did not check the duration of the disorder. There is a possibility of survival bias, because we used not only incident cases but also prevalent cases. Third, the controls were not randomly selected from the general population, but were recruited from persons at health checkups. The tooth characteristics of 191 controls compared with participants of a survey on dental diseases in 1999 16 are shown in Table 4. Averages of tooth characteristics in the control group were calculated by adjusting : Averages of tooth characteristics in the control group were calculated by adjusting age via a direct method using the data of the survey on dental diseases in 1999 16 as a standard population.
age with a direct method using the data of the survey on dental diseases in 1999 16 as a standard population. As shown in Table 4, more controls had their own teeth than in the general population among males. We must consider the effect of using healthy participants as controls.
In conclusion, we found that PD patients had more complaints about their oral health (e.g., chewing difficulties, denture discomfort) and more problems in the oral health behavior than the general population. In addition, more than half of PD patients had problems with swallowing. These findings may be useful for the caregivers of PD patients to conduct oral care as well as for making health plans for dental care for PD patients and for medical and welfare services. Furthermore, dental staff members in public health centers should strengthen training for caregivers to enhance knowledge and skills about oral care, as well as dental checkups and dental health services by home visits for PD patients.