Does parkinsonism affect periodontal health? A cross-sectional study in a tertiary hospital.

BACKGROUND: Muscular rigidity, tremors, and bradykinesia with diminished motor skills are the characteristic features of Parkinson's disease (PD). AIM: The study investigated the influence of reduced motor proficiency on the periodontal health of PD patients and compared it with controls. SETTING AND
DESIGN: A cross-sectional study was conducted on PD patients selected from outpatient section of a tertiary healthcare center and compared with age- and gender-matched controls.
MATERIALS AND METHODS: Oral health status of the subjects was graded based on decayed, missing, and filled teeth index, oral hygiene index (OHI), modified gingival index, probing pocket depth (PPD), clinical attachment level (CAL), tooth mobility, interproximal PPD, and interproximal CAL measurements. PD patients were categorized based on Hoehn and Yahr scale and duration to assess the influence of PD severity and progression. STATISTICAL ANALYSIS: Difference in the mean values of quantitative variables was analyzed by parametric t-test and Chi-square test for categorical variables.
RESULTS: In PD patients, 84.4% of subjects had moderate-severe gingivitis, while it was 2.4% in the control group. Mean number of interproximal sites with CAL >5 mm in PD patients and control subjects was 8.41 ± 6.37 and 1.12 ± 2.28, respectively (P < 0.05). The mean OHI was 2.90 ± 0.81 in patients with mild PD and increased to 3.77 ± 0.52 as PD severity exalted.
CONCLUSION: PD patients had impaired oral condition with higher OHI and increased gingival inflammation with a likelihood of male predisposition. Substantial interproximal tissue destruction, debilitated periodontal health as PD progresses, suggests early attention toward their oral health. Copyright:

INTRODUCTION

The WHO defined oral health as “a state of being free from mouth and facial pain oral and throat cancer, oral infection and sores, periodontal disease, tooth decay, tooth loss, and other diseases and disorders that limit an individual's capacity in biting, chewing, smiling, speaking, and psychosocial well-being.”[1] Hence, oral health is a complex entity which is affected by many factors, and the realization of these factors is important for its overall function and maintenance. Modifiable risk factors, such as poor diet and nutrition, tobacco use, psychological stress, and particularly insufficient personal/oral hygiene, are pivotal aspects to be considered for oral health.[2] Daily oral hygiene practices as well as periodic professional care are the basis in treatment programs, which are directed at the prevention and treatment of oral diseases. However, home care procedures are technically difficult, time-demanding and can be affected by the compliance and manual dexterity of the individual.

Parkinson's disease (PD) is a chronic, irreversible, slowly progressive, neurodegenerative disorder. It was first described by James Parkinson, who was a general practitioner in London in 1817.[3] The term “parkinsonism” refers to a clinical syndrome, including bradykinesia, rigidity, a slow shuffling gait, testing tremor, and imbalance. PD is characterized pathologically by early prominent death of dopaminergic neurons in the substantia nigra pars compacta of the midbrain, leading to pathophysiologic changes in the circuitry of the downstream basal ganglia.[4] In addition, there is an increased incidence of cognitive impairment and depression associated with the disease.[5]

The incidence and the prevalence of PD increase with advancing age, being present in 1% of people over the age of 65 years.[6] A prevalence rate of 27/100,000 was reported in Bangalore,[7] while a high crude prevalence rate of 328.3/100,000 among a population of Parsis living in Western India was documented by Bharucha et al.[8] Altered motor behavior as well as cognitive disturbances may have adverse effects on the frequency and quality of daily oral hygiene care by patients with PD. Disordered oral health may result in periodontal diseases, caries, and eventually loss of teeth. An ailing dental condition produces physical and mental deterioration, affecting the quality of life, and results in increased mortality.[9]

There are incompatible findings regarding the oral health status of patients with PD. In the survey by Fukayo et al.,[10] it was reported that oral health of PD patients was better than expected in terms of less number of carious teeth and increased number of remaining teeth. Similar reports were made by Persson et al.[11] However, results published by Hanaoka and Kashihara[9] as well as by Pradeep et al.[12] showed increased frequencies of periodontal disease, caries, and tooth loss in patients with PD. Hence, an investigation was carried out to test our hypothesis that the prevalence of gingival inflammation and periodontal diseases is higher in patients with PD than in control subjects. The objectives of this study accordingly were to determine the state of periodontal health in patients with PD and to correlate them with a control cohort.

MATERIALS AND METHODS

A cross-sectional study was conducted on 32 PD patients (test subjects) and 42 control subjects (control group), who were willing to participate in the study. The study was approved by the institutional ethical committee (Ref. No. IEC/M/17/2019/DCK, dated November 14, 2019). The patients in the test subject group were selected from the outpatient section, Department of Neurology, Government Medical College, Kottayam, Kerala. The patients were diagnosed based on the clinical features of PD, which was identified by the neurologist.

Control subjects included age- and gender-matched by-standers of PD patients and also of the patients who attended Department of Periodontics, Government Dental College, Kottayam, Kerala. Subjects under antibiotic or any hormone replacement therapy, those who had undergone oral prophylaxis therapy within 6 months, pregnant or lactating mothers, and those who had presence of other systemic disorders such as diabetes mellitus which could influence the periodontal status, who were current or having a history of smoking, and who had history of dementia were excluded from the study.

Information pertaining to duration of PD was obtained from the patient's medical records. Using the Hoehn and Yahr score, PD progression of test subjects was classified into five stages.[13] All the participants of the study were examined in a standard manner, while being seated on a dental chair under illumination, using mouth mirror (#5, Hu-Friedy, Chicago, IL, USA), Williams graduated periodontal probe (Hu-Friedy, Chicago, IL, USA), and explorer. Personal oral health practices were assessed based on the patient's oral hygiene method, frequency, and technique, as well as the dentifrice used.

Information regarding status of teeth was estimated using decayed, missing, and filled teeth (DMFT) index.[14] Tooth mobility (TM) was examined manually and graded into: 0 – No mobility greater than normal, 1 – First distinguishable movement greater than normal, 2 – Movement of crown up to 1 mm in any direction, and 3 – Movement of crown greater than 1 mm in any direction and/or vertical depression of crown in its socket.[15] Additional data which were recorded to assess oral health condition were the oral hygiene index (OHI), which is composed of the combined debris index and calculus index.[16] Periodontal health stature was evaluated based on (a) modified gingival index (MGI),[17] (b) Probing pocket depth (PPD), (c) gingival recession, and (d) clinical attachment level (CAL). All the computable values were recorded as full-mouth measurements. Each tooth was assessed at mid-buccal, lingual/palatal, and interdentally at mesial and distal surfaces. From the total scores obtained, the mean score for the entire dentition was calculated.

Statistical analysis

The data collected were organized into a spread sheet using a computer program (Excel, Microsoft, Redmond, USA). Using data processor (SPSS v.19 IBM Chicago, IL, USA), statistical analysis was carried out with the P-value (level of significance) set at 0.05. Normality testing was done using Kolmogorov–Smirnov test. All variables were found to follow normal distribution. Difference in mean values of quantitative variables was tested by parametric t-test. Among the categorical variables, difference in proportions between the groups was tested by Chi-square test.

RESULTS

In the study, 32 PD patients (test group), comprising 18 males and 14 females, with mean age of 58.41 ± 10.62 years, and 42 control subjects (control group), comprising 22 males and 20 females, with mean age of 54.36 ± 9.72 years, were examined. Analysis showed no significant difference in age and gender between the two groups. Demographic data and oral hygiene practices of the test and control subjects are presented in Table 1. No significant difference was observed in oral hygiene method, frequency of oral hygiene, and dentifrice used between the two groups. However, technique of oral hygiene method varied between the groups with a statistically significant difference (P < 0.05). The test group subjects used horizontal method more common (84.4%).

Table 1

Demographic data and oral hygiene practices of the study groups

Group	Number of subjects	Number of males, n (%)	Number of females, n (%)	Age (years) mean±SD	Oral hygiene method, n (%)		Frequency of oral hygiene, n (%)		Technique of oral hygiene, n (%)			Dentifrice, n (%)
					Finger	Tooth brush	Once daily	Twice daily	Horizontal	Vertical	Any other	Tooth paste	Tooth powder
Test	32	18 (56.3)	14 (43.8)	58.41±10.62	2 (6.3)	30 (93.8)	23 (71.9)	9 (28.1)	27 (84.4)	2 (6.3)	3 (9.4)	31 (96.9)	1 (3.1)
Control	42	22 (52.4)	20 (47.6)	54.36±9.72	1 (2.4)	41 (97.6)	20 (47.6)	21 (50)	28 (66.7)	12 (28.6)	2 (4.8)	36 (85.7)	6 (14.3)
SS		NS (χ2)		NS (t)	NS (χ2)		NS (χ2)		S (χ2)			NS (χ2)

S – Significant at P<0.05; χ2 – Chi-square test; T – T-test; SD – Standard deviation; SS – Statistical significance; NS – Nonsignificant; n – number of subjects

General oral health and gingival status

The mean score of all the parameters pertaining to general oral health status was higher in the test group, and significant difference was present compared to control subjects [Table 2]. Based on the clinical presentation of gingival inflammation, subjects were categorized into two groups, namely mild gingivitis and moderate-to-severe gingivitis (based on mean MGI score ≤1 and >1, respectively). In the test group, 84.4% of the patients had moderate-to-severe gingivitis, while in control group, 97.6% of the subjects had only mild form of gingivitis, which showed a statistical difference in the analysis.

Table 2

Oral health parameters of test and control group

Variable	Mean±SD		SS
	Test group	Control group
DMFT score	7.72±4.45	4.57±3.58	S (t)
Oral hygiene index	3.09±0.83	1.32±0.41	S (t)
Modified gingival index	1.52±0.38	0.69±0.18	S (t)
PPD score	2.59±0.68	1.61±0.36	S (t)
Gingival recession score	1.34±0.57	0.58±0.34	S (t)
CAL score	3.92±1.11	2.18±0.51	S (t)
IPPD score	2.77±0.74	1.62±0.45	S (t)
Interproximal gingival recession score	1.55±2.08	0.46±0.35	S (t)
ICAL score	3.96±1.06	2.07±0.58	S (t)
Mild gingivitis, n (%)	5 (15.6)	41 (97.6)	S (χ2)
Moderate to severe gingivitis, n (%)	27 (84.4)	1 (2.4)

S – Significant at P<0.05; χ2 – Chi-square test; T – T-test; SD – Standard deviation; SS – Statistical significance; DMFT – Decayed missed filled teeth; PPD – Probing pocket depth; CAL – Clinical attachment level; IPPD – Interproximal probing pocket depth; ICAL – Interproximal clinical attachment level

Periodontal health assessment

For comparative assessments, patients were categorized based on mean PPD score as mild and deep pockets (score of 3–5 mm and >5 mm, respectively) and based on mean CAL score as moderate and severe periodontitis (score of 3–5 mm and >5 mm, respectively). In the test group, more number of patients had mild pockets (93.8%) and deep pockets (31.3%). Similar findings were obtained with regard to periodontitis severity, and a significant difference was present in the severe category of periodontitis (CAL score >5 mm). Among the PD patients, 29 subjects had at least one tooth with Grade I mobility. In the same group, 20 subjects had Grade II TM, while Grade III TM was present in 10 subjects. Notably, none of the control group subjects had Grade III TM [Table 3].

Table 3

Comparison between test and control group based on categorization of probing pocket depth and clinical attachment level and tooth mobility

Group	Number of subjects with PPD (mm)		Number of subjects with CAL (mm)		Mean number of sites with PPD, mean±SD (mm)		Tooth mobility (grades)
	3-5, n (%)	>5, n (%)	3-5, n (%)	>5, n (%)	3-5	>5	I	II	III
Test	30 (93.8)	10 (31.3)	32 (100)	31 (96.9)	41.69±19.98	2.03±5.0	29	20	10
Control	35 (83.3)	5 (11.9)	41 (97.6)	21 (50)	10.38±9.99	0.36±1.57	13	3	0
SS	NS (χ2)	S (χ2)	NS (χ2)	S (χ2)	S (t)	NS (t)	S (χ2)	S (χ2)	S (χ2)

S – Significant at P<0.05; χ2 – Chi-square test; T – T-test; SD – Standard deviation; SS – Statistical significance; NS – Nonsignificant; PPD – Probing pocket depth; CAL – Clinical attachment level

Interproximal periodontal status

For better reflection of periodontal disease, interproximal probing pocket depth (IPPD) and interproximal CAL (ICAL) values were compared between the test and control groups. Results showed that subjects with IPPD of 3–5 mm and ICAL of >5 mm were more in the test group [Table 4]. Similarly, the mean number of IPPD sites of 3–5 mm, ICAL 3–5 mm, and ICAL >5 mm was higher in the PD group and was statistically significant when compared to control group.

Table 4

Comparison of interproximal parameters between test and control group

Group	Number of subjects with IPPD 3-5 (mm), n (%)	Number of subjects with ICAL >5 (mm), n (%)	Mean number of sites with IPPD, mean±SD (mm)		Mean number of sites with ICAL, mean±SD (mm)
			3-5	>5	3-5	>5
Test	29 (90.6)	30 (93.8)	13.47±8.20	1.25±2.79	19.25±10.07	8.41±6.97
Control	23 (54.8)	16 (38.1)	2.33±3.32	0.38±1.44	7.05±6.23	1.12±2.28
SS	S (χ2)	S (χ2)	S (t)	NS (t)	S (t)	S (t)

S – Significant at P<0.05; χ2 – Chi-square test; T – T-test; SD – Standard deviation; SS – Statistical significance; NS – Nonsignificant; IPPD – Interproximal probing pocket depth; ICAL – Interproximal clinical attachment level

Comparison between male and female patients with Parkinson's disease

Graph 1 illustrates the data pertaining to the oral hygiene practices, gingival health, and periodontal parameter categorization, of both genders, which were relevant in the current study. The duration of PD in males was 53.6 ± 38.49 months and that of females was 32.92 ± 15.84 months. Out of 18 males, 16 patients (88.9%) brushed their teeth only once per day, which was a significant difference compared to 50% in the female group. Further, more male patients had moderate-to-severe form of gingivitis, as well as severe category of PPD and CAL. Mean OHI score of males was 3.11 ± 0.81 compared to 3.05 ± 0.89 of females, and the mean IPPD of males and females was 2.84 ± 0.78 and 2.67 ± 0.69, respectively. However, the difference between the groups was not significant.

Graph 1

Comparison of data between males and females of test group, PPD - Probing Pocket Depth; ICAL - Interproximal Clinical Attachment Level

Effect of duration and stage of Parkinson's disease

The mean duration of PD of the test group subjects was 44.56 ± 32.03 months. For analytical purpose, based on duration, the patients were categorized into two groups, namely those with <3 years, in which there were 17 patients, and those with duration >3 years, which comprised 15 patients. In this study, PD severity was graded into 4 scores according to Hoehn and Yahr criteria as, score I (20 subjects), score II (5 subjects), score III (4 subjects), and score IV (3 subjects). The influence of PD progression on oral health status was analyzed based on the dichotomization of stages into mild (score 1 and 2) and moderate (score 3 and 4) groups. Table 5 and Graph 2 depict the data related to the analysis. There was a positive correlation of most of the clinical parameters with PD duration and severity (except for DMFT score with regard to PD duration). Equivalently, IPPD and ICAL scores showed an ascending trend as PD progressed. However, the analysis was not significant. Furthermore, OHI and MGI values were significantly more as severity of PD increased.

Table 5

Oral health parameters based on duration and severity of Parkinson’s disease

Parameter	PD of duration (years) mean±SD		SS	PD severity, mean±SD		SS
	<3	>3		Mild	Moderate
DMFT score	8.0±65.1	7.33±3.73	NS (t)	7.24±4.06	9.43±5.68	NS (t)
OHI	2.98±0.82	3.2±10.85	NS (t)	2.90±0.81	3.77±0.52	S (t)
MGI	1.47±0.39	1.57±0.39	NS (t)	1.44±0.38	1.82±0.25	S (t)
PPD score	2.47±0.59	2.73±0.76	NS (t)	2.54±0.60	2.80±0.94	NS (t)
CAL score	3.84±0.89	4.01±1.34	NS (t)	3.79±1.10	4.38±1.09	NS (t)
IPPD score	2.62±0.69	2.94±0.77	NS (t)	2.71±0.65	2.97±1.02	NS (t)
ICAL score	3.82±0.92	4.12±1.22	NS (t)	3.87±1.03	4.29±1.2	NS (t)
Mean number of sites with PPD 3-5 (mm)	35.71±19.5	48.47±18.87	NS (t)	41.64±17.92	41.86±27.88	NS (t)
Mean number of sites with CAL >5 (mm)	15.0±10.43	19.33±17.63	NS (t)	14.64±12.76	25.57±16.73	NS (t)
Mean number of sites with ICAL >5 (mm)	7.24±4.77	9.73±8.84	NS (t)	7.16±5.71	12.86±9.56	NS (t)

S – Significant at P<0.05; T – T-test; SD – Standard deviation, SS – Statistical significance; DMFT – Decayed, missed, filled teeth; OHI – Oral hygiene index; MGI – Modified gingival index; PPD – Probing pocket depth; CAL – Clinical attachment level; IPPD – Interproximal probing pocket depth; ICAL – Interproximal clinical attachment level; PD – Parkinson’s disease; NS – Nonsignificant

Graph 2

Data related to duration and severity of Parkinson's disease (based on number of subjects), PPD - Probing Pocket Depth; CAL - Clinical Attachment Level

DISCUSSION

Any factor(s) which can adversely affect the healthcare practices such as daily personal oral hygiene and regular professional interventions will be inimical to have a noble oral health.[18] PD is a progressive neurodegenerative disease, which militates against the person's capacity to achieve adequate plaque control. The present study, to the best of our knowledge, was the first attempt to investigate the effect of PD on periodontal health at the tertiary care level. In the study, PD patients with mild-to-moderate severity were compared with age- and gender-matched control subjects, in terms of oral hygiene practices and periodontal parameters. Several results of the present study display the meager periodontal health status in PD patients, which is in par with other reports in literature.[1920]

The mean score of all the major determinants of periodontal health was significantly higher in PD patients, which could be attributed to their motor and cognitive dysfunction. Since both the study cohorts did not differ in the method or frequency of oral hygiene, the higher values of local factors can be related to the reduced potential of PD patients in plaque control. This can be substantiated by the facile form of horizontal technique of oral hygiene being followed more by PD patients. Barbe et al. (2017)[21] reported that one-third of PD patients (17.8% of females and 33.3% of males) had limited ability to perform oral hygiene. The novel finding of increased number of PD patients in having moderate–severe form of gingivitis (84.4%, P < 0.05), demonstrated the increased propensity of gingival inflammation progression to its severe form. This advocates the importance of early interventional procedures in such patients.

Studies have reported greater periodontal tissue destruction in terms of PPD and loss of gingival attachment in PD patients.[1222] Identically, the present study also showed higher elements of periodontal breakdown in PD patients with significantly greater surge in number of subjects with PPD >5 mm (31.5%) compared to control group (11.9%). Similarly, 96.9% of PD patients had CAL >5 mm, while for control group, it was 50%. Further, the mean number of sites with deeper periodontal pockets was more in PD patients than control subjects. Analysis of these data suggested that, similar to gingival inflammation, PD patients have the tendency to develop severe form of periodontitis also. This finding is very much in harmony with the report of Einarsdottir et al.[19]

The data related to TM, which is a consequence of loss of tooth-supporting tissues, also point to the poor state of periodontal health of PD patients, which is shown by the significant higher number of mobile teeth compared to control subjects. Recently, in the case–control study, more number of PD patients stating biting problems and TM was reported.[3] The absence of Grade III TM in control group in this study, and also reported by Cicciu et al.[23] is of particular importance, as it ascertains the superior health status of the same group. In other words, PD patients had a substantially higher destruction of tooth-supporting tissues, which resulted in the presence more teeth with hopeless prognosis.

The 2017 World Workshop on the classification of periodontal and peri-implant diseases and conditions states that the key to periodontitis case definition is the detectable interdental CAL.[24] Hence, as an original investigation, data analytics of interdental periodontal health of PD patients with that of control subjects showed significant higher number of PD patients with greater ICAL scores and the involvement of more number of sites. However, lack of radiographic images due to inherent difficulties limited the further assessment of interdental tissues. Hence, in future studies, radiographic assessments should be performed to supplement the clinical information.

Gender differences in clinical presentations have been established for periodontitis with deep periodontal pockets and increased prevalence in males.[25] In this study, a male preponderance in having poor oral health was observed in PD group. Schwarz et al.,[26] on the contrary, found a significant greater risk of female PD patients to develop periodontal pathology, even though their participants consisted of more males. In another study, the researchers concluded that gender had no impact on the oral health status of PD patients.[22] Despite the lack of a significant difference with female cohort, the present study showed that more number of males had severe PPD and CAL. It can be explained to a certain extend by the reduced frequency of mechanical home care plaque control measures and significant longer duration of PD. However, in the fore mentioned studies, duration of PD was not a parameter in analysis.

In confirmation with other studies, the present study also showed poorly maintained periodontal health of PD patients in relation to its duration and severity.[912] Progressive nature of PD affects the motor and cognitive function of patients and results in their reduced ability to manage oral hygiene. Even with less number of subjects with score 3 and 4 of PD severity, the mean values of oral health parameters were higher and this affirms the above-cited aspects. This is also in agreement with the observational study by Lyra et al.[27] in 28 PD patients, which identified the prevalence of severe form of periodontitis with PD stage advancement. Nonetheless, few limitations to mention pertaining to the current cross-sectional study are as follows: the less number of participants which were examined, lack of information regarding the level of different orofacial dysfunction, nonassessment of advanced dexterity level, and impact of drug regimen on the observed data.

CONCLUSION

The results of this study on PD patients, in a tertiary care setting, showed that their oral and periodontal health is generally worse than the age- and gender-matched control subjects. There is increased severity of gingival inflammation and periodontal disease as evidenced by the higher MGI value and IPPD and ICAL measurements. However, significant correlation of severity of PD and its duration on periodontal health could not be established in the current study. Future studies which will consider the observed limitations, as well as the effects of socioeconomic backgrounds on oral health of PD patients, should be carried out. This preliminary study has highlighted need for early oral interventional procedures and role of periodontists in establishing strategies for future action in this field.

Financial support and sponsorship

Nil.

Conflicts of interest

There are no conflicts of interest.