Evaluation of dysphagia in different phenotypes of early and idiopathic Parkinsonism

Parkinson’s disease (PD) is a common neurodegenerative disorder with prevalence 140 per 100,000 [1, 2].

Most of the patients with PD develop dysphagia in the late stage of the disease in spite of early pathological changes of brainstem structures [3–6].

Dysphagia in IPD may occur in up to 100% of the patients in advanced disease stages [7, 8] which impairs the quality of life, interferes with medication intake, and leads to malnutrition and aspiration pneumonia, which is the major cause of death in PD [9].

A recent meta-analysis showed that the prevalence of oropharyngeal dysphagia is 35% on using subjective tools like questionnaires, and this percent increases to 82% by using the more objective measures like FEES [7].

Fiberoptic endoscopic evaluation of swallowing (FEES) is considered one of the gold standard tests for the diagnosis of dysphagia, which can be replaced by a simple questionnaire like SDQ when FEES is not available [10].

Previous studies reported that patients with postural instability/gait disorder (PIGD) have greater problems of swallowing than tremor dominant phenotype (TD) which indicate a positive relationship between dysphagia and range of motor skills, including falling, postural instability, and gait dysfunction [11, 12].

To the best of our knowledge, most of the studies underestimate the frequency and severity of dysphasia in radiologically documented dysphagia, and the simple, sensitive, and specific bedside tests available for diagnosis of dysphagia in IPD are lacking [13–16].

This cross-sectional study was done to detect dysphagia in early and idiopathic parkinsonism by using SDQ and the more accurate FEES and to evaluate the frequency of dysphagia in different phenotypes of IPD as the early detection of dysphagia reduces bad impact on the quality of life of patients.

The mean age of the 54 participants in the study (38 men and 16 women) was 62.3 (age range 51–75 years). We selected our participants in the early stage of the disease with mean disease duration 4.7 ± 2.2. The mean of UPDRS part II score and UPDRS part III score was 15.5 ± 8.9 and 37.5 ± 16.3, respectively, while modified Hoehn and Yahr rating was 2.1 ± 0.6.

When the PD patients were questioned, the percentage of dysphagia was 35.1% particularly the oral phase which nearly doubles the percentage of the pharyngeal phase and this percentage increased to 40.7% when using the more accurate and objective method (FEES) (Table 1 and Fig. 1).

	Mean	Standard deviation (SD)
Age (mean ± SD)	62.30	5.642
Diagnosis
Disease duration (mean ± SD)	4.7	2.2
Disease severity
Mini-Mental State Examination (MMSE) (30 = normal)	26.8	1.8
Unified Parkinson’s Disease Rating Scale (UPDRS)
UPDRS part II score (68 = severe)	15.5	8.9
UPDRS part III score (108 = severe)	37.5	16.3
Modified Hoehn and Yahr rating (5 = severe)	2.1	0.6
	Number of patients	Percentage
Sex
Male	38	70.4
Female	16	29.6
Parkinsonism phenotype
Tremor dominant	46	85.2
Postural Instability and gait instability	8	14.8
Swallowing disturbance questionnaire
Normal	35	64.8
Dysphagia	19	35.2
Oral phase	13	24
Pharyngeal phase	6	11.1
FEES
Normal swallowing	32	59.3
Residual	20	37.0
Aspiration	2	3.7
Salivation scale
Normal salivation	17	31.5
Sialorrhea	37	68.5

The mean age of patients with normal swallowing and dysphagia was 63.5 ± 5.9 versus 60.5 ± 4.8, respectively, with a P value of 0.05.

Most of the patient with dysphagia have a longer disease duration (5.3 ± 2.1) than those with normal swallowing (4.3 ± 2.1) with a P value equal to 0.1.

The percentage of dysphagia in PIGD and TD type was 75 and 34%, respectively, with a P value equal to 0.02.

The mean MMS examination in dysphagia group is significantly lower (but still within normal range) than the normal group (25.8 ± 1.0 versus 27.56 ± 2.0 with a P value = 0.001).

Dysphagia was significantly correlated with UPDRS part II score, UPDRS part III score, and modified Hoehn and Yahr scale Table 2.

Parkinsonism phenotype and activity of daily living (ADL) were independent predictors of dysphagia Table 3 and Fig. 2.

	B	S.E.	Wald	df	Sig.	Exp(B)	95% C.I. for EXP(B)
							Lower	Upper
Parkinsonism phenotype	1.947	0.913	4.543	1	0.033	7.007	1.170	41.973
Total UPDRS	− 0.042	0.037	1.271	1	0.260	.959	0.891	1.032
II_ADL	0.330	.144	5.232	1	0.022	1.391	1.048	1.846
Sialorrhea	0.426	0.664	.411	1	0.521	1.530	.417	5.619
Constant	− 3.546	1.675	4.480	1	0.034	0.029

UPDRS Unified Parkinson’s Disease Rating Scale, ADL activity of daily living

Normal swallowing depends on smooth coordination of the oral and pharyngeal phase. An impaired oral phase may impair the airway during the pharyngeal phase [25, 26].

The prolonged oral transit time which may be a factor that predispose to dysphagia in PD, a finding reported from a radiological study [27].

Aspiration and pneumonia are common complications of dysphagia and may occur at any stage of PD but more with advanced stage [28].

More than 35% of patients experience dysphagia on SDQ, and this percentage increases to about 40% when using FEES which is similar to the results of previous studies which reported that the occurrence of dysphagia is between 20 and 40% in patients with IPD [16] in contrast to previous work of Manor and colleagues which stated a higher percentage of dysphagia (63.2%) [3]; this difference may be related to the selection of patient as most of our participants are outpatients, and their H&Y scale was less than 3 which is classified as an early stage of IPD. Also, the mean duration of illness in our PD patients was 4.7 which means a relatively short duration of PD.

Oral phase of dysphagia is more commonly affected than pharyngeal phase (24% versus 11.1% respectively) like other studies which confirmed the affection of oral phase more than pharyngeal phase of swallowing in PD [29].

Like previous studies, the present study revealed that dysphagia is significantly correlated with UPDRS and modified Hoehn and Yahr scale [30, 31] in contrast to the others [32, 33] which showed that the disease stage (UPDRS total and Hoehn and Yahr rating) was not correlated to swallowing difficulties which may be explained by the relatively early stage of PD in our patients (H&Y scale< 3), the shorter duration of illness (4.7 ± 2.2) and the usage of different scores for evaluation of dysphagia.

The present work emphasized the greater percentage of dysphagia in PIGD group than tremor dominant group (75% versus 34.8% respectively). This finding was in line with the previous studies which reported that dysphagia may be associated with more “axial” motor disturbance, increased postural instability, and more falls [11, 12].

The mechanism of dysphagia in PD may be related to extrapyramidal and autonomic system disorders into which degeneration of the dorsal nucleus of the vagus and esophageal myenteric plexus is responsible for dysphagia [34], and this neurodegeneration in the autonomic nervous system occurring not only in the late stage but also in the early stages of PD [35]; this finding may be confirmed by the fact that dysphagia is partially improved by dopaminergic therapy [12, 35, 36].

Our results showed a strong correlation between PD severity on UPDRS and dysphagia, so the severity could be a predictor of dysphagia in PD patients like many previous studies with apparently larger sample sizes which documented the significant association between the severity of PD and dysphagia [15, 25, 26]. On the other hand, Ali and Wallace did not observe any correlation between the clinical severity of PD and dysphagia, which may be explained by a smaller sample size of their participants and most of their patients had advanced PD (H&Y stage more than III) [37].

The major limitation of this study was the relatively small sample size and lack of follow-up of patients with dysphagia especially the asymptomatic group and the effect of different dopaminergic drugs on dysphagia.

In spite of these limitations, the present study has shown that dysphagia is a common symptom even in an early stage of PD. The simple and available SDQ may be a useful screening tool for detection of dysphagia in PD and the patients with abnormal SDQ better to be referred to a speech therapist.

In conclusion, the present work is one of few studies that exhibited the association between dysphagia and early PD and showed that dysphagia symptoms is more prevalent in PIGD phenotype. Dysphagia could be easily detected by SDQ and confirmed by FEES as the early detection of dysphagia decreases the deleterious impact on quality of life of PD patients.