Abstract
Background/objectives
Parkinson’s disease (PD) patients appear to have an increased risk of developing dental disease. This study aimed to evaluate the status of the dental caries, oral hygiene and periodontal health among a group of Chinese PD patients with different disease severity.
Methods
A total of 424 PD patients were enrolled in the study. The Movement Disorder Society Unified Parkinson’s Disease Rating Scale (MDS-UPDRS) and Modified Hoehn and Yahr scale (HY) were used to assess PD symptoms and severity. The Decayed, Missing, and Filled Teeth index (DMFT), Community Periodontal Index for Treatment Needs (CPITN) and Simplified Oral Hygiene Index (OHI-S) were used to assess dental status. Multiple linear, binary logistic and ordinal logistic regression estimated the association between PD parameters and dental parameters.
Results
More advanced PD stage was associated with worse periodontal health (β = 0.771, p < 0.001). More advanced PD motor impairment was associated with increased number of untreated caries (β = 0.066, p < 0.001), poorer oral hygiene (β = 0.030, p < 0.001) and periodontal status (β = 0.040, p < 0.001). Increased difficulties in chewing and swallowing were experienced in PD patients with more decayed teeth (rho = 0.218, p < 0.00019).
Conclusions
After considering the influence of age, gender, civil status, years of education and place of residence, the findings from the present study suggested that poorer oral health was observed in more advanced staged PD patients. The findings underscore the importance of integrating oral care into the overall management of PD.
Clinical trial number
Not applicable.
Supplementary Information
The online version contains supplementary material available at 10.1186/s12903-025-06448-7.
Keywords: Parkinson’s disease, Dental health, Oral health
Introduction
Parkinson’s disease (PD) is a progressive neurodegenerative condition, affecting individuals globally with an incidence rate of between 47 and 77 cases per 100,000 individuals aged 45 and above [1]. PD has a wide range of motor and non-motor symptoms including bradykinesia, rigidity, tremor, and cognitive impairment [2]. In the advanced stages, the impairment and inconvenience caused by the disease may not only impact everyday-life activities, but also significantly influence patients’ overall quality of life. Oral health is no exception. Several published literatures reported that due to motor impairments and cognitive decline, PD patients appear to have higher risk of getting dental disease, including periodontal disease, dental caries and orofacial pain [3, 4, 5]. These oral health issues can further complicate PD management by increasing functional, psychological and economic burdens as the disease progresses.
Oral cavity, the focal point for the interaction of the body with the external environment, has been regarded as the “window to general health” [6]. Poor oral health may serve as a marker for frailty onset, as oral disease may interfere with mastication, reduce ability to eat and swallow, and ultimately bring negative impact on patient’s nutritional intake and psychosocial well-being [7]. A further connection between oral health and frailty may be attributed to the inflammatory pathway. Oral disease, particularly periodontitis, may trigger adverse systemic outcomes through blood-borne dissemination of oral pathogenic bacteria and systemic leakage of local inflammatory mediators [8]. Additionally, periodontitis-induced peripheral and systemic inflammation could trigger an immune response in the brain, potentially resulting in neuroinflammation [9].
Thus, attention of oral health should be concerning among PD patients and their health care providers, considering its direct (pain, orofunctional problems, nutritional imbalance, psychosocial wellbeing) and indirect (impaired drug absorption, increased risk of infections, inflammation and systemic diseases) impact [10, 11]. Nevertheless, oral health care has always been unprioritized and unvalued in the management of PD. While several observational studies reported worse oral health status in PD patients, they are limited by small sample size and lack of precise and reliable clinical measurements. Furthermore, in reviewing literature, studies focused on the comparison of dental status among different severity of PD patients were very scarce and no data was found in China population.
Therefore, the aim of the present study was to evaluate the oral health status of PD patient with different disease severity. The study also aimed to investigate the correlation between dental clinical measurements and motor and non-motor characteristics of PD.
Materials and methods
Design and setting
This cross-sectional study was conducted at the outpatient clinic of the Department of Neurology at the Second Affiliated Hospital Zhejiang University School of Medicine Binjiang campus and Jiefang campus in China from September 2020 to September 2021. The protocol was approved by the Research Ethics Committee of the hospital (Approval number: IR2020001108) and all patients signed informed consent prior to inclusion. The study was performed following the guidelines of the Declaration of the World Medical Association 1975 in Helsinki, revised in 2000. The study was reviewed and checked following the STROBE (Strengthening The Reporting Of Observational Studies In Epidemiology) guidelines.
Study population and ethical guidelines
The diagnosis of idiopathic PD was made by a highly experienced neurologist (L.W.) based on the Clinical Diagnostic Criteria for PD in China (2016) and all included patients were in their ‘on’ state. The general exclusion criteria were as follows: (1)being younger than 18 years of age; (2)edentulous; (3)patients with other neurodegenerative disease; (4)receipt of nonsurgical periodontal treatment (previous 6 months) and surgical periodontal treatment (previous 12 months); (5)status of pregnancy or lactation; (6)intake of drugs throughout the last 3 months prior to the study that may potentially cause gingival hyperplasia such as hydantoin, nifedipine, cyclosporin A or similar drugs. After the interview and assessment, each participant was informed with his/her oral status and was recommended for further dental treatment if necessary.
Two examiners (G.Z., C.J.) conducted the interviews and assessments. Prior to the study, a calibration process was carried out on 20 subjects who were not included in the study. Cohen’s.
kappa statistics were calculated to assess inter- and intra-examiner reliability for Decayed, Missing, and Filled Teeth index (DMFT), Community Periodontal Index for Treatment Needs (CPITN), Simplified Oral Hygiene Index (OHI-S), the Movement Disorder Society Unified Parkinson’s Disease Rating Scale (MDS-UPDRS) and Modified Hoehn and Yahr scale (HY).The results demonstrated strong agreement, with kappa values exceeding 0.8 for inter- and intra-examiner reliability.
PD assessment
A structured interview was conducted to acquire the following information: (1)age; (2)body mass index (BMI); (3)gender; (4)civil status; (5)years of education; (6)place of residence; (7)length of time since the last oral consultation; (8)frequency of tooth brushing; (9)the PD disease duration (Supplementary File 1).
Selected questions related to oral health were selected from MDS-UPDRS Part I and II to assess the motor and non-motor experiences of patient’s daily living [12]. MDS-UPDRS Part III was used to evaluate the motor symptoms of PD patients. HY was used to assess the stage and motor impairment severity of PD [12].
Dental examination
Clinical oral examination was performed with the patient sitting on a chair (or, when necessary, on a wheelchair) under a good light source. For dental examination, the present study focused on assessing patient’s dental caries status, level of periodontal disease and oral hygiene status, and was correspondingly evaluated by DMFT, CPITN and OHI-S.
DMFT was used to measure the dental caries status and is completed with Community Periodontal Index Probe following the World Health Organization (WHO) criteria [13]. The status of each status was recorded as a score from 0 to 9. The D component includes all teeth with codes 1 or 2. The M component includes teeth coded 4 in subjects under 30 years of age, and 4 or 5 in subjects 30 years and older. The F component includes only teeth with code 3.
CPITN was used to assess the level of periodontal disease and treatment need, and is completed by a 0.5 mm ball tip WHO CPITN-probe following WHO criteria [14]. Each sextant was assigned with a code number according to the worst affected site in that quadrant based on the following criteria: Code 0: no signs of disease; Code 1: gingival bleeding after gentle probing; Code 2: presence of supra- or subgingival calculus; Code 3: presence of pathological pocket of 4–5 mm; Code 4: presence of pathological pocket of 6 mm or more. The presence and absence of periodontitis was dichotomized and categorized into 2 groups: Absence of periodontitis: Code 0- Code 2; Presence of periodontitis: Code 3- Code 4.
OHI-S, performed by a No. 5 explorer (Shepard’s Crook), was used to measure the level of oral hygiene and has two components: Debris Index (DI-S) and Calculus Index (CI-S) [15]. DI-S determined the presence of soft debris on of the buccal and lingual surfaces on 6 representative teeth on a scale of 0–3. CI-S determined the presences of calculus on 6 representative teeth on a scale of 0–3. After recording, the index values (DI-S and CI-S scores) were separately calculated by dividing the corresponding total scores by the number of surfaces scored. OHI-S score was obtained by adding DI-S and CI-S scores.
Statistical analysis
The data were analyzed with the aid of IBM SPSS Statistics, version 29.0.0.0 (241) for Mac (Armonk, New York, NY, USA). The Kolmogorov-Smirnov test was used to check whether the distribution of variables was normal, and all variables did not present normal distribution. Consequently, the non-parametric approach was used for all tests. Demographic and clinical characteristics were presented in a descriptive way, numerical data were express as median (q1 = first quartile; q3 = third quartile) and categorical variables as number (percentage). For the comparisons among sample subsets stratified by HY, Kruskal-Wallis test was conducted for continuous variables and chi-square test was conducted for categorical variables. Spearman’s rank-order correlation coefficient (rho) applying Bonferroni correction was used to assess the existence of significant interdependence between MDS-UPDRS individual domains and the dental clinical measurements (DMFT, DI-S, CI-S, CPITN). After adjusting age, gender, civil status, years of education and place of residence, multiple linear regression (stepwise) was conducted to investigate the potential association between PD parameters (independent variable; HY, MDS-UPDRS part III total score, and PD disease duration) and dental status indicators (dependent variable; number of decayed, missing, filled teeth and OHI-S). For periodontal parameter (CPITN), ordinal logistic regression model was estimated to assess its dependence to the same PD parameters. Additionally, a binary logistic regression model was performed for periodontitis presence, with results expressed as odds ratios (ORs) and 95% confidence intervals (CI). Results from other regression analyses were expressed as beta coefficient (β) with 95% CI. A level of significance of 5% was considered.
Results
Participants characteristics
A total of 424 participants were enrolled in the study and their demographic features were shown in Table 1. The median age of the total sample was 63.0 (56.0; 68.0) years, including 248 women (59%) and 176 men(41%), and the median PD disease duration was 5.0(2.0;8.0) years. The median length of time since the last oral health consultation was 2.3(1.0;12.0) years and frequency of tooth brushing was 2.0(1.0;2.0) times/day, both showed no significant difference among different HY stages.
Table 1.
Descriptive statistics of study participants stratified by HY and comparison among them
| Variable | Total (n = 424) |
HY 1 (n = 36) |
HY 1.5 (n = 40) |
HY 2 (n = 202) |
HY 2.5 (n = 107) |
HY 3 (n = 30) |
HY 4 (n = 8) |
HY 5 (n = 1) |
p | ||
|---|---|---|---|---|---|---|---|---|---|---|---|
| Age, median (q1;q3) (years) | 63.0(56.0;68.0) | 61.0(50.0;66.0) | 60.5(53.5;67.0) | 62.0(55.0;67.0) | 65.0(58.0;72.0) | 66.0(57.8;70.3) | 70.5(62.0;75.0) | 77 | 0.001 | ||
| Age range, min-max (years) | 25–87 | 25–81 | 37–82 | 35–83 | 35–87 | 40–84 | 43–79 | 77 | |||
| Body mass index, median (q1;q3) | 23.0(21.4;24.3) | 22.9(20.6;24.2) | 22.9(21.0;24.5) | 22.9(22.0;24.8) | 22.9(21.0;23.3) | 22.9(21.5;25.0) | 22.7(20.6;23.6) | 23.3 | 0.063 | ||
| Gender, (Male/Female) | 176/248 | 15/21 | 10/30 | 98/104 | 37/70 | 14/16 | 2/6 | 0/1 | 0.050 | ||
| Civil status | Single, n(%) | 19(4.5%) | 1(2.8%) | - | 11(5.4%) | 4(3.7%) | 3(10%) | - | - | 0.809 | |
| Married, n(%) | 395(93.2%) | 34(94.4%) | 39(97.5%) | 188(93.1%) | 98(91.6%) | 27(90%) | 8(100%) | 1(100.0%) | |||
| Divorced, n(%) | 3(0.7%) | - | 1(2.5%) | 1(0.5%) | 1(0.9%) | - | - | - | |||
| Widow, n(%) | 7(1.7%) | 1(2.8%) | - | 2(1.0%) | 4(3.7%) | - | - | - | |||
| Years of education | ≤ 6, n(%) | 168(39.6%) | 12(33.3%) | 11(27.5%) | 78(38.6%) | 54(50.5%) | 12(40.0%) | 1(12.5%) | 0 | 0.217 | |
| > 6,≤9, n(%) | 84(19.8%) | 7(19.4%) | 9(22.5%) | 43(21.3%) | 18(16.8%) | 6(20.0%) | - | 1(100.0%) | |||
| > 9,≤12,n(%) | 127(30.0%) | 14(38.9%) | 14(35.0%) | 58(28.7%) | 28(26.2%) | 8(26.7%) | 5(62.5%) | 0 | |||
| > 12, n(%) | 45(10.6%) | 3(8.3%) | 6(15.0%) | 23(11.4%) | 7(6.5%) | 4(13.3%) | 2(25.0%) | 0 | |||
| Place of residence | Capital, n(%) | 202(47.6%) | 21(58.3%) | 19(47.5%) | 100(49.5%) | 42(39.3%) | 13(43.3%) | 6(75.0%) | 1(100.0%) | 0.385 | |
| Periurban area, n(%) | 107(25.2%) | 9(25.0%) | 11(27.5%) | 52(25.7%) | 29(27.1%) | 5(16.7%) | 1(12.5%) | 0 | |||
| Rural, n(%) | 115(27.1%) | 8(16.7%) | 10(25.0%) | 50(24.8%) | 36(33.6%) | 12(40.0%) | 1(12.5%) | 0 | |||
| Length of time since the last oral consultation, median (q1;q3) (years) | 2.3(1.0;12.0) | 2.8(1.0;5.0) | 2.0(0.5;27.5) | 2.3(0.9;20.0) | 3.0(1.0;15.0) | 2.0(1.0;21.3) | 18.0(0.5;3.3) | 0.5 | 0.059 | ||
| Frequency of tooth brushing, median (q1;q3) (times/day) | 2.0(1.0;2.0) | 2.0(1.1;2.0) | 2.0(1.1;2.0) | 2.0(1.0;2.0) | 2.0(1.0;2.0) | 1.0(1.0;2.0) | 2.0(1.3;3.0) | 3.0 | 0.171 | ||
| The PD disease duration, median (q1;q3) (years) | 5.0(2.0;8.0) | 2.5(1.0;3.9) | 2.5(1.0;4.0) | 4.0(2.0;7.1) | 6.0(4.0;10.0) | 9.0(5.0;14.0) | 5.0(5.0;6.8) | 5 | < 0.001 | ||
| DMFT | Filled, median (q1;q3) | 0.0(0.0;0.0) | 0.0(0.0;0.0) | 0.0(0.0;0.0) | 0.0(0.0;0.0) | 0.0(0.0;0.0) | 0.0(0.0;0.3) | 0.0(0.0;0.0) | 1 | 0.066 | |
| Missing, median (q1;q3) | 1.0(0.0;4.0) | 0.0(0.0;1.8) | 0.0(0.0;2.0) | 1.0(0.0;3.0) | 2.0(0.0;7.0) | 1.0(0.0;6.2) | 5.5(0.8;10.8) | 0 | 0.002 | ||
| Decayed, median (q1;q3) | 2.0(0.0;4.0) | 1.0(0.0;3.0) | 1.0(0.0;2.0) | 1.0(0.0;4.0) | 2.0(1.0;5.0) | 2.5(0.8;8.0) | 5.0(1.3;8.5) | 12 | < 0.001 | ||
| OHI-S | DI-S, median (q1;q3) | 2.0(1.7;2.3) | 1.8(1.3;2.0) | 2.0(1.5;2.0) | 2.0(1.7;2.3) | 2.0(1.8;2.5) | 2.3(2.0;3.0) | 2.1(2.0;2.7) | 3 | < 0.001 | |
| CI-S, median (q1;q3) | 1.9(1.2;2.3) | 1.5(1.0;2.0) | 1.3(1.0;2.0) | 1.8(1.2;2.2) | 2.0(1.7;2.4) | 2.3(2.0;3.0) | 2.0(1.9;2.3) | 3 | < 0.001 | ||
| CPITN | Code 0, n(%) | 0(0%) | - | - | - | - | - | - | - | < 0.001 | |
| Code 1, n(%) | 1(0.2%) | 1(2.8%) | - | - | - | - | - | - | |||
| Code 2, n(%) | 105(24.8%) | 17(47.2%) | 24(60%) | 44(21.9%) | 14(13.1%) | 5(16.7%) | 1(12.5%) | - | |||
| Code 3, n(%) | 274(64.7%) | 15(41.7%) | 15(37.5%) | 139(68.8%) | 77(72.0%) | 21(70%) | 6(75.0%) | 1(100.0%) | |||
| Code 4, n(%) | 44(10.4%) | 3(8.3%) | 1(2.5%) | 19(9.4%) | 16(15.0%) | 4(13.3%) | 1(12.5%) | - | |||
Abbreviations: HY, Modified Hoehn and Yahr scale; PD, Parkinson disease; DMFT, the Decayed, Missing, and Filled Teeth index; DI-S, Simplified Debris Index; CI-S, Simplified Calculus Index; CPITN, Community Periodontal Index for Treatment Need
p < 0.05 is considered statistically significant
PD severity and dental health
The median values of number of decayed teeth, missing teeth, filled teeth, DI-S and CI-S were presented in Table 1. Significant differences in number of missing teeth and decayed teeth, oral hygiene level and periodontal disease severity were found among patients in different HY stages. All patients had some level of periodontal pathology (CPITN ≥ 1), with 75.1% meeting the threshold indicative of periodontitis (CPITN 3–4). CPITN 3(64.7%) which implied periodontitis with 4–5 mm PPD was the most common grading for PD patients.
Regression analyses (Table 2) revealed how increased severity in PD staging was significantly associated with worse periodontal status (β = 0.771, 95% CI: 0.403;1.139, p < 0.001). Furthermore, a statistically significant positive association was observed between the PD disease duration and the number of missing teeth (β = 0.202, 95% CI: 0.093; 0.312, p < 0.001).
Table 2.
Regression models for dental status in PD patients
| Number of decayed teeth | Number of missing teeth | ||||||||
|---|---|---|---|---|---|---|---|---|---|
| Variables | Adjusted βa | 95% CI | SE | p | Adjusted βa | 95% CI | SE | p | |
| HY | - | - | - | n.s. | - | - | - | n.s. | |
| MDS-UPDRS part III | 0.066 | 0.046; 0.086 | 0.010 | < 0.001 | - | - | - | n.s. | |
| The PD disease duration | - | - | - | n.s. | 0.202 | 0.093; 0.312 | 0.056 | < 0.001 | |
| Number of filled teeth | OHI-S | ||||||||
| Variables | Adjusted βa | 95% CI | SE | p | Adjusted βa | 95% CI | SE | p | |
| HY | - | - | - | n.s. | - | - | - | n.s. | |
| MDS-UPDRS part III | - | - | - | n.s. | 0.030 | 0.024; 0.036 | 0.003 | < 0.001 | |
| The PD disease duration | - | - | - | n.s. | - | - | - | n.s. | |
| CPITN | Presence of periodontitis | ||||||||
| Variables | Adjusted βa | 95% CI | SE | p | Adjusted ORsa | 95% CI | SE | p | |
| HY | 0.771 |
0.403; 1.139 |
0.188 | < 0.001 | n.s. | ||||
| MDS-UPDRS part III | 0.040 | 0.026; 0.054 | 0.007 | < 0.001 | 1.034 |
1.010; 1.059 |
0.012 | 0.005 | |
| The PD disease duration | - | - | - | n.s. | n.s. | ||||
Abbreviations: β, β coefficient; CI, Confidence Interval; SE, Standard Error; ORs, Odds Ratios; HY, Modified Hoehn and Yahr scale; MDS-UPDRS, the Movement Disorder Society Unified Parkinson’s Disease Rating Scale; OHI-S, Simplified Oral Hygiene Index; CPITN, Community Periodontal Index for Treatment Need; n.s., not significant
aAdjusted for age, gender, civil status, years of education and place of residence
p < 0.05 is considered statistically significant
PD motor and non-motor symptoms and dental health
As showed in Table 2, regression analysis showed that an increase in MDS-UPDRS part III total score was associated with significantly higher estimated number of dental caries (β = 0.066, 95% CI: 0.046; 0.086, p < 0.001), poorer oral hygiene (β = 0.030, 95% CI: 0.024; 0.036, p < 0.001) and periodontal status (β = 0.040, 95% CI: 0.026; 0.054, p < 0.001). Although these associations were statistically significant, the effect sizes were small; for instance, each 10-point increase in MDS-UPDRS part III predicted 0.3 unit rise in OHI-S, suggesting a modest change within the ‘fair’ hygiene range. Furthermore, higher MDS-UPDRS part III scores were also significantly associated with increased odds of having periodontitis (OR = 1.034, 95% CI: 1.010–1.059, p = 0.005).
Table 3 showed the correlation between the PD motor and non-motor symptoms and dental status. Based on the interpretation of Spearman correlation proposed by Schober et al., all significant rho values in our study fall within the range of 0.10–0.39 and are therefore described as “weak correlations” [16]. Specifically, for motor symptoms, Spearman’s rank correlation coefficient indicated weak but statistically significant correlations between deterioration in both left- and right-hand functions—including finger tapping, hand opening-closing movements, and hand pronation-supination—and worsening oral hygiene (DI-S and CI-S) and periodontal status (CPITN). Similar weak positive correlation was observed between poor periodontal parameters (DI-S, CI-S, CPITN) and impaired leg motions including leg rigidity, toe tapping and leg agility. Deterioration in gait, posture and body bradykinesia were also correlated with increased number of missing and decayed teeth, poorer CPITN, DI-S and CI-S.
Table 3.
Correlation between MDS-UPDRS individual items and dental clinical measures
| MDS - UPDRS | Filled | Missing | Decayed | CPITN | DI-S | CI-S | |
|---|---|---|---|---|---|---|---|
| Non-motor symptoms | |||||||
| 1.1 Cognitive Impairment | rho | n.s. | n.s. | n.s. | n.s. | n.s. | 0.192* |
| 95% CI | 0.096, 0.285 | ||||||
| 1.3 Depressed Mood | rho | n.s. | n.s. | n.s. | n.s. | n.s. | 0.210* |
| 95% CI | 0.114, 0.302 | ||||||
| 1.4 Anxious Mood | rho | n.s. | n.s. | n.s. | n.s. | n.s. | 0.238* |
| 95% CI | 0.143, 0.328 | ||||||
| 1.5 Apathy | rho | n.s. | n.s. | n.s. | n.s. | n.s. | n.s. |
| 95% CI | |||||||
| 1.7 Sleep Problems | rho | n.s. | n.s. | n.s. | n.s. | n.s. | n.s. |
| 95% CI | |||||||
| 1.9 Pain and Other Sensations | rho | n.s. | n.s. | n.s. | n.s. | n.s. | n.s. |
| 95% CI | |||||||
| 1.13 Fatigue | rho | n.s. | n.s. | n.s. | n.s. | n.s. | 0.194* |
| 95% CI | 0.097, 0.286 | ||||||
| 2.2 Saliva and Drooling | rho | n.s. | n.s. | n.s. | n.s. | n.s. | n.s. |
| 95% CI | |||||||
| 2.3 Chewing and Swallowing | rho | n.s. | n.s. | 0.218* | n.s. | n.s. | n.s. |
| 95% CI | 0.123, 0.310 | ||||||
| 2.4 Eating Tasks | rho | n.s. | n.s. | n.s. | n.s. | 0.227* | 0.188* |
| 95% CI | 0.132, 0.318 | 0.092, 0.281 | |||||
| 2.6 Hygiene | rho | n.s. | n.s. | n.s. | n.s. | 0.185* | 0.225* |
| 95% CI | 0.089, 0.278 | 0.130, 0.316 | |||||
| Motor symptoms | |||||||
| 3.1 Speech | rho | n.s. | n.s. | n.s. | 0.260* | 0.257* | 0.289* |
| 95% CI | 0.166, 0.349 | 0.163, 0.346 | 0.196, 0.376 | ||||
| 3.2 Facial Expression | rho | n.s. | n.s. | n.s. | 0.264* | 0.312* | 0.309* |
| 95% CI | 0.170, 0.353 | 0.220, 0.397 | 0.217, 0.395 | ||||
| 3.3a Rigidity Neck | rho | n.s. | n.s. | n.s. | n.s. | 0.200* | 0.231* |
| 95% CI | 0.104, 0.292 | 0.136, 0.322 | |||||
| 3.3b Rigidity (LUE) | rho | n.s. | n.s. | n.s. | n.s. | 0.260* | 0.266* |
| 95% CI | 0.166, 0.349 | 0.173, 0.355 | |||||
| 3.3c Rigidity (RUE) | rho | n.s. | n.s. | n.s. | 0.183* | 0.164 | 0.219* |
| 95% CI | 0.086, 0.276 | 0.067, 0.258 | 0.123, 0.310 | ||||
| 3.3d Rigidity (LLE) | rho | n.s. | n.s. | n.s. | 0.242* | 0.251* | 0.312* |
| 95% CI | 0.147, 0.332 | 0.157, 0.341 | 0.221, 0.398 | ||||
| 3.3e Rigidity (RLE) | rho | n.s. | n.s. | n.s. | 0.199* | 0.192* | 0.266* |
| 95% CI | 0.103. 0.291 | 0.096, 0.285 | 0.173, 0.355 | ||||
| 3.4a Finger Tapping (L) | rho | n.s. | n.s. | 0.212* | 0.242* | 0.274* | 0.280* |
| 95% CI | 0.116, 0.304 | 0.147, 0.332 | 0.181, 0.363 | 0.187, 0.368 | |||
| 3.4b Finger Tapping (R) | rho | n.s. | n.s. | n.s. | 0.248* | 0.252* | 0.263* |
| 95% CI | 0.153, 0.337 | 0.158, 0.342 | 0.170, 0.352 | ||||
| 3.5a Hand Movements (L) | rho | n.s. | n.s. | 0.191* | 0.263* | 0.288* | 0.306* |
| 95% CI | 0.095, 0.284 | 0.169, 0.352 | 0.196, 0.376 | 0.214, 0.392 | |||
| 3.5b Hand Movements (R) | rho | n.s. | n.s. | n.s. | 0.278* | 0.246* | 0.300* |
| 95% CI | 0.185, 0.366 | 0.151, 0.336 | 0.209. 0.387 | ||||
| 3.6a Pronation-Supination Movements of Hands (L) | rho | n.s. | n.s. | n.s. | 0.255* | 0.306* | 0.326* |
| 95% CI | 0.161, 0.344 | 0.214, 0.392 | 0.236, 0.411 | ||||
| 3.6b Pronation-Supination Movements of Hands (R) | rho | n.s. | n.s. | n.s. | 0.229* | 0.212* | 0.280* |
| 95% CI | 0.134, 0.320 | 0.116, 0.303 | 0.187, 0.368 | ||||
| 3.7a Toe Tapping (L) | rho | n.s. | n.s. | 0.265* | 0.234* | 0.283* | 0.294* |
| 95% CI | 0.171, 0.354 | 0.139, 0.325 | 0.190, 0.371 | 0.202, 0.381 | |||
| 3.7b Toe Tapping (R) | rho | n.s. | n.s. | 0.193* | 0.230* | 0.266* | 0.320* |
| 95% CI | 0.097, 0.286 | 0.135, 0.321 | 0.173, 0.355 | 0.229, 0.405 | |||
| 3.8a Leg Agility (L) | rho | n.s. | n.s. | 0.254* | 0.268* | 0.370* | 0.353* |
| 95% CI | 0.160, 0.344 | 0.175, 0.357 | 0.282, 0.452 | 0.264, 0.436 | |||
| 3.8b Leg Agility (R) | rho | n.s. | n.s. | 0.219* | 0.233* | 0.337* | 0.357* |
| 95% CI | 0.123, 0.310 | 0.138, 0.323 | 0.247, 0.421 | 0.269, 0.440 | |||
| 3.9 Rising From Chair | rho | n.s. | n.s. | n.s. | n.s. | n.s. | n.s. |
| 95% CI | |||||||
| 3.10 Gait | rho | n.s. | 0.212* | 0.187* | 0.295* | 0.382* | 0.392* |
| 95% CI | 0.116, 0.304 | 0.090, 0.280 | 0.203, 0.382 | 0.295, 0.462 | 0.306, 0.472 | ||
| 3.11 Freezing Of Gait | rho | n.s. | 0.177* | 0.274* | 0.253* | 0.264* | 0.262* |
| 95% CI | 0.081, 0.271 | 0.181, 0.362 | 0.159, 0.343 | 0.170, 0.353 | 0.169, 0.351 | ||
| 3.12 Postural Stability | rho | n.s. | 0.168* | 0.253* | 0.196* | 0.188* | 0.286* |
| 95% CI | 0.071, 0.261 | 0.159, 0.343 | 0.100, 0.288 | 0.092, 0.281 | 0.193, 0.373 | ||
| 3.13 Posture | rho | n.s. | 0.266* | 0.230* | 0.332* | 0.368* | 0.374* |
| 95% CI | 0.172, 0.355 | 0.135, 0.321 | 0.242, 0.417 | 0.280, 0.450 | 0.286, 0.455 | ||
| 3.14 Body Bradykinesia | rho | n.s. | 0.265* | 0.276* | 0.333* | 0.339* | 0.348* |
| 95% CI | 0.172, 0.354 | 0.183, 0.365 | 0.243, 0.418 | 0.249, 0.423 | 0.259, 0.432 | ||
| 3.15a Postural Tremor of The Hands (L) | rho | n.s. | n.s. | n.s. | 0.117* | 0.253* | 0.283* |
| 95% CI | 0.020, 0.213 | 0.159, 0.342 | 0.190, 0.370 | ||||
| 3.15b Postural Tremor of The Hands (R) | rho | n.s. | n.s. | n.s. | 0.142* | 0.202* | 0.239* |
| 95% CI | 0.044, 0.237 | 0.106, 0.294 | 0.144, 0.329 | ||||
| 3.16a Kinetic Tremor of The Hands (L) | rho | n.s. | n.s. | n.s. | 0.143* | 0.216* | 0.203* |
| 95% CI | 0.046, 0.238 | 0.120, 0.307 | 0.107, 0.295 | ||||
| 3.16b Kinetic Tremor of The Hands (R) | rho | n.s. | n.s. | n.s. | n.s. | 0.112* | 0.143* |
| 95% CI | 0.014, 0.208 | 0.046, 0.238 | |||||
| 3.17a Rest Tremor Amplitude (LUE) | rho | n.s. | n.s. | n.s. | n.s. | n.s. | 0.151* |
| 95% CI | 0.053. 0.245 | ||||||
| 3.17b Rest Tremor Amplitude (RUE) | rho | n.s. | n.s. | n.s. | n.s. | n.s. | n.s. |
| 95% CI | |||||||
| 3.17c Rest Tremor Amplitude (LLE) | rho | n.s. | n.s. | n.s. | n.s. | n.s. | n.s. |
| 95% CI | |||||||
| 3.17d Rest Tremor Amplitude (RLE) | rho | -0.112* | n.s. | n.s. | n.s. | n.s. | n.s. |
| 95% CI | -0.207, -0.014 | ||||||
| 3.17e Rest Tremor Amplitude (Lip/Jaw) | rho | n.s. | 0.118* | n.s. | 0.141* | 0.167* | 0.134* |
| 95% CI | 0.020, 0.214 | 0.043, 0.236 | 0.070, 0.261 | 0.036, 0.229 | |||
| 3.18 Constancy of Rest Tremor | rho | n.s. | 0.126* | n.s. | n.s. | n.s. | n.s. |
| 95% CI | 0.029, 0.222 | ||||||
Abbreviations: CI, Confidence Interval; MDS-UPDRS, the Movement Disorder Society Unified Parkinson’s Disease Rating Scale; CPITN, Community Periodontal Index for Treatment Need; DI-S, Simplified Debris Index; CI-S, Simplified Calculus Index; R, Right; L, Left; LUE, Left Upper Extremity; RUE, Right Upper Extremity; LLE, Left Lower Extremity; RLE, Right Lower Extremity; n.s., not significant
* Applying the Bonferroni correction, the accepted significance level was p < 0.00019
For non-motor symptoms, spearman’s rank correlation coefficient showed that deterioration of cognitive impairment (rho = 0.192). depressed (rho = 0.210) and anxious mood (rho = 0.238), fatigue (rho = 0.194), eating tasks (rho = 0.188) and hygiene on daily activities (rho = 0.225) were weakly correlated with worsening of oral hygiene (CI-S). Increased number of decayed teeth were correlated with increased difficulties in chewing and swallowing (rho = 0.218). No correlations were detected between number of filled teeth and any assessed PD motor and non-motor symptoms.
Discussion
Due to xerostomia, motor and cognitive impairment, oral dysbiosis and neuroinflammation, the physiopathology of oral disorders in PD individuals is complex and not fully understood. This study is one of the few studies to assess the caries status, periodontal status and oral hygiene status across different HY staging of PD patients, and to investigate the correlation between each dental parameter and each PD motor manifestation. To our knowledge, this is also the first published Chinese cohort examined with calibrated indices to study the said population.
It is concerning to observe that 38.7% of PD patients brush their teeth less than the recommended twice a day. Additionally, a significant proportion of PD patients, 18.9%, reported never having visited a dentist before, and the median duration since their last dental consultation was 2.3 years—substantially longer than the American Dental Association’s suggested interval of every six months. These findings highlight a concerning trend of neglect in oral healthcare among PD patients in our cohort, which may reflect broader issues within certain segments of the Chinese population; nevertheless, caution is needed when generalizing these findings.
Regarding caries status, the result of present study showed that after adjusting age, gender, civil status, years of education and place of residence, increased number of untreated caries was significantly associated with worsened motor impairment (β = 0.066, 95% CI: 0.046; 0.086, p < 0.001), increased number of missing teeth was significantly associated with longer PD disease duration (β = 0.202, 95% CI: 0.093; 0.312, p < 0.001). Although these associations were statistically significant, the effect sizes were modest; for example, a β of 0.066 indicates that every 15-point increase in MDS-UPDRS part III corresponds to approximately one additional untreated carious surface. Taken together, these findings suggested that as PD persist and progress over time, there may be a cumulative impact on dental health. To our knowledge, comparison of DMFT between different severity of PD patients have not been evaluated in the previous studies, but there were evidence proving that compared to healthy control, lower number of teeth, more dental carious lesions, more subjective chewing difficulties and more subjective denture discomfort were observed in PD subjects [10, 17, 18]. It is not difficult to speculate the rationale behind the said findings, as increased motor impairment would lead to reduced competence of PD patients to properly perform oral hygiene, increasing their risk of acquiring dental diseases.
Aside from that, emerging evidence suggested that oral microflora may be altered in PD patients from the early stages, with higher amounts of cariogenic and periodontal pathogens such as Streptococcus mutans, Lactobacillus, and Firmicutes compared to controls, potentially increasing the risk for caries and periodontitis [19, 20]. Some researchers have hypothesized that oral microbiota may play a role in PD pathogenesis. For instance, Streptococcus mutans may promote amyloid formation and α-synuclein aggregation [19], while increased Lactobacillus reuteri might enhance α-synuclein release into enteric nervous system [21]. However, these mechanisms were not assessed in our study and remain speculative. Further research is needed to confirm these hypotheses.
Several articles have reported the higher prevalence of periodontal disease and poorer oral hygiene in PD population [18, 22, 23, 24, 25]. Our data through regression analysis showed similar findings that the more deteriorated PD motor symptoms, the worse oral hygiene (β = 0.030, 95% CI: 0.024; 0.036, p < 0.001) and periodontal status (β = 0.040, 95% CI: 0.026; 0.054, p < 0.001). Using the MDS-UPDRS, postural tremor of hands and rigidity of upper extremities were associated with increased plaque accumulation, which is congruent with the findings of Lyra et al. [26]. In addition, other motor manifestations, including deteriorated finger tapping, hand movements, freezing of gait, and reduced leg agility and toe tapping, showed weak but statistically significant correlation with more advanced stages of periodontitis. These PD symptoms may help identifying populations at higher risk for developing dental disease and highlight the importance of neurologists to involve dental teams for early prevention efforts. It is also important to note that, as this study is cross-sectional, causality cannot be inferred.
The question of whether a causal relationship exists between periodontitis and PD has drawn researcher’s attention over the past decade, but remains controversial. A retrospective cohort study conducted in 2013 claimed that there is an increased risk of developing parkinsonism during 5 years of periodontitis diagnosis [27]. Another population-based cohort study showed similar result that patients with periodontal disease were 1.4 times more likely to develop PD [28]. However, a recent large population cohort study in South Korean reported that the association between periodontitis and PD is weak [29]. Similar result was reported by a recent meta-analysis that no bidirectional association was identified between periodontitis and PD risk [30]. The recent mendelian randomization study in European population also found no bidirectional causal genetic liability between two diseases [31].
Nevertheless, a few hypotheses linking two diseases were proposed. Yilmaz et al. found that compared to PD without periodontitis, there was an increase of neurodegenerative marker YKL-40 levels in serum, saliva and GCF levels in PD patients with periodontitis. The periodontal pro-inflammatory cytokine IL-6 may trigger STAT3 pathway, which result in increased production of YKL-40 and accelerate PD pathogenesis [32]. Botelho et al. found higher level white blood cells count, segmented neutrophils and basophils in PD patients with periodontitis [33]. Lyra et al. also reported significantly higher level of high-sensitive C-reactive protein found in PD cases with periodontitis [34]. All that evidence suggested that similar to other systemic diseases, the chronic neuroinflammation resulted from periodontitis systemic outcomes may play a role in PD pathogenesis and progression. The inflammatory mediators (IL-1, IL-6, TNF- α, and reactive oxygen species) and the bacterial endotoxin lipopolysaccharide initiated from periodontitis could possibly translocate into systemic circulation, and initiate the conversion of primed microglia into active microglia in midbrain, inducing dopaminergic neurons necrosis and apoptosis, and consequently leading to PD [35].
Other groups of researchers proposed that the two diseases shared several common risk factors (smoking, oxidative stress, chronic inflammation, etc.) and comorbidities (diabetes mellitus, osteoporosis, hypertension, etc.). This could contribute to potential similar underlying mechanism and render certain subgroups with comorbidities more vulnerable to develop the other disease [36]. Furthermore, in the most recent bioinformatic analyses, several identical genes (CXCR4,CXCL8,CD19,RPTN) were found in both periodontitis and PD, further suggesting possible presence of susceptible individuals for both diseases [37]. Future longitudinal and interventional studies are needed to further investigate and confirm the causality of periodontitis-PD link.
It is also important to highlight the complex role that salivation plays in both PD and the development of oral disease. Notably, the symptom of drooling and xerostomia may occur independently or concurrently on the same PD patient [38]. Drooling, possibly caused by oropharyngeal bradykinesia, hypomimia and abnormal flexed head posture, may lead to angular cheilosis and disruption of oral microbiome homeostasis [39]. Xerostomia, on the other hand, may result from dopaminergic or anticholinergic medication side effects or autonomic dysfunction-associated hyposalivation in PD. Reduced salivary flow may compromise saliva’s antibacterial and cleansing actions, thereby increasing the risk of acquiring dental caries and other oral lesions [10]. Several studies have reported that altered salivary flow negatively affects the oral health–related quality of life in PD patients [40, 41]. Unfortunately, due to equipment and space limitations, we were unable to measure salivary secretion in our cohort. Future studies should incorporate both subjective assessments and objective measurements of salivation to explore its association with the dental disease progression in PD population.
The essential role that neurologists play in the early and close collaboration of dental team should be emphasized. On one hand, non-motor symptoms of PD, including orofacial manifestations such as dysphagia, drooling and xerostomia can begin well before motor symptoms onset, which could be critical to defining at-risk population for PD prevention [42, 43]. On the other hand, our data confirmed that increased difficulties in chewing and swallowing were experienced in PD patients with more decayed teeth (rho = 0.218). This is because the presence of carious lesion could hinder the mastication process, causing patient to ingest insufficiently masticated food, which may in turn, put patients at higher risk of dysphagia and malnutrition. Oral diseases are preventable at early stage, even in vulnerable populations. The authors advocate neurologists to actively advice PD patients to seek regular dental care and explain the urgency thereof.
The main strength of this study was its collaborative nature between the Department of Dentistry and the Department of Neurology. This partnership enabled a multidisciplinary assessment of participants’ oral health and neurological status by calibrated professionals, who followed internationally standardized procedures. This approach provided reliable assessments of the participants’ dental status and PD status.
This study also has a few limitations. The first is the nature of the cross-sectional study does not permit to analyze the causal association between PD and oral diseases, and the results of our findings need to be validated in greater detail by future longitudinal studies. Furthermore, the number of patients in HY stages IV and V was limited in our study, which may due to reduced access to healthcare services as a result of severe motor impairments. Future studies should consider adopting a multi-center design that includes both outpatient and inpatient populations, to ensure a more representative and evenly distributed cohort. Another limitation is the lack of further detailed dental and PD examination, which might have resulted in inadequate assessment of dental and PD status. Additionally, the hospital-based outpatient sample may introduce selection bias and limit generalizability, while self-reported tooth brushing frequency, unmeasured confounders such as diet and xerostomia-inducing medications, and conducting all oral examinations while patients were in the ‘on’ state may have influenced the assessment of oral health outcomes. Future efforts should include longitudinal and multi-center studies to further characterize the nature of the relationship between PD and oral health. Ultimately interventional studies are needed to evaluate the effects of dental therapy on the progression rate of PD, which would bring significant implications to the health of the public.
Conclusion
The result of current study revealed that patients with more advanced HY stage have more advanced periodontal disease. Patients with more deteriorated motor impairment exhibit a higher number of decayed teeth, poorer oral hygiene and worse periodontal status. Increased difficulties in chewing and swallowing were experienced in PD patients with more unfilled caries. Although oral health is probably subordinate to other PD symptoms, clinical observations suggested that they may still have a meaningful impact on patients’ overall well-being. Therefore, the authors advocate PD medical management teams to pay more attention to patient’s oral health. Given the cross-sectional design of this study, further longitudinal research is needed to develop evidence-based guidelines for integrating oral care into professional general health care for PD patients.
Electronic supplementary material
Below is the link to the electronic supplementary material.
Acknowledgements
The authors would like to thank all patients who took part in the study.
Abbreviations
- PD
Parkinson’s disease
- DMFT
Decayed, missing, and filled teeth index
- CPITN
Community periodontal index for treatment needs
- OHI-S
Simplified oral hygiene index
- MDS-UPDRS
The movement disorder society unified parkinson’s disease rating scale
- HY
Modified hoehn and yahr scale
- WHO
The world health organization
- DI-S
Debris index
- CI-S
Calculus index
Author contributions
Ziyu Ge: Conceptualization; Data collection; Data analysis; Writing original draft; Writing–review & editing. Jing Chen: Data collection; Writing review & editing. Xinhui Chen: Data analysis; Writing–review & editing. Rundong Zhang: Data interpretation. Yanzhen Zhang: Conceptualization; Resources; Supervision; Validation; Writing– review & editing. Wei Luo: Conceptualization; Resources; Supervision; Validation; Writing–review & editing. All authors reviewed the manuscript.
Funding
This work was supported by the State Administration of Traditional Chinese Medicine of Zhejiang Province (No. 78GZY-ZJ-KJ-24078).
Data availability
Data supporting the findings of this study are available from the corresponding author on reasonable request.
Declarations
Ethics approval and consent to participate
This study was performed in compliance with the Helsinki Declaration of 1964 and its later amendments. Ethics approval was obtained from the Research Ethics Committee of the Second Affiliated Hospital Zhejiang University School of Medicine (approval number: IR2020001108). All participants provided written informed consent regarding the use of their clinical data for scientific research and have their data published in a journal article.
Consent for publication
Not applicable.
Competing interests
The authors declare no competing interests.
Footnotes
Publisher’s note
Springer Nature remains neutral with regard to jurisdictional claims in published maps and institutional affiliations.
Contributor Information
Yanzhen Zhang, Email: 2191004@zju.edu.cn.
Wei Luo, Email: luoweirock@zju.edu.cn.
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Associated Data
This section collects any data citations, data availability statements, or supplementary materials included in this article.
Supplementary Materials
Data Availability Statement
Data supporting the findings of this study are available from the corresponding author on reasonable request.