Self-Perception of Voice and Swallowing Handicap in Parkinson’s Disease

INTRODUCTION

An estimated 1% of the population over 60 and many millions of persons are affected with Parkinson’s disease (PD) [1]. As an aging disorder, its prevalence is estimated to double by 2030 [2, 3]. Dysphagia, or difficulty swallowing, and hypokinetic dysarthria are common problems in PD [4–6]. Speech production in PD commonly involves the dysphonia of low vocal volume, monopitch, and monoprosody [5, 6]. While speech problems can be stigmatizing and interfere with communication, dysphagia has more serious consequences in that it can lead to aspiration pneumonia and death [7–13]. Typical signs of dysphagia in PD include repetitive and dysfunctional tongue rocking attempting to initiate posterior bolus propulsion through the oral cavity, delayed swallowing response, impaired pharyngeal stripping leading to collection of food in the valleculae or pyriform sinuses, and silent aspiration into the lungs [4, 10–12]. Poor tongue control and impaired tongue initiation of movement, uncoordinated oropharyngeal timing of bolus movement and impaired sensation to the larynx also contribute to dysphagia in PD [4, 12]. Impairment of upper and lower gastrointestinal dysfunction in PD is also common with dysphagia being the first symptom [14]. With worsening of effective and safe swallowing, patients with advanced PD may be forced to adapt alternative feeding methods such as avoidance of liquids and percutaneous gastrostomy tube (PEG) [15]. While some reports indicate that the swallowing question in the ADL portion of the Unified Parkinson’s Disease Rating Scale (UPDRS) is insensitive for identifying dysphagia, others have shown that slower swallowing speed and reduced bolus volume are significantly associated with declining Hoehn and Yahr scores [16, 17]. However, the clinical severity of PD does not predict either the presence or severity of dysphagia [18].

Several studies have shown that swallowing abnormalities may be under-recognized in routine clinic care, as objective swallowing evaluations have found impairment, with some over 50%, of PD patients who had denied any perceived swallowing deficits when questioned, including silent aspiration [12, 18–23]. Low correlations of perceived dysphagia compared to objective analysis has been reported in neurologically impaired individuals in general [24]. In PD, impaired sensory/perceptual feedback appears to contribute to this discrepancy [7]. Among patients followed long term, latency to developing dysphagia may be 10 years or longer [25]. As PD progresses, the incidence of dysphagia increases to an estimated 80% or more of this population with risk factors attributed to combinations of age, sex, PD duration, development of dementia, and overall lack of attention to swallowing problems [26, 27]. When recognized to be a problem, dysphagia can interfere with the socialization of eating and cause depression [20, 28]. Given that dysphagia may be under-recognized in early stages of PD, it is important to identify swallowing problems in PD as soon as possible using specific questioning, as intervening might not only reduce the personal and social burden on a patient, but it also might decrease the chance of aspiration pneumonia, and its risk of death on this basis [13, 29].

The low vocal volume associated with the hypokinetic dysarthria in PD has the potential to impair social communication and interpersonal relationships [30]. Recently, the Voice Handicap Index (VHI), a patient reported outcomes measure, was found to differentiate individuals with PD, particularly mild PD, from controls. The authors established construct validity, reliability, and feasibility of the VHI in a group of PD subjects, making it a useful tool in assessing patient perceptions of the handicapping effects of dysphonia in PD [31]. Voice changes may occur at early or later stages of PD, and patient perceptions of vocal changes tend to be unrelated to UPDRS scores [32]. One longitudinal case study revealed that changes in the acoustic vocal signal were demonstrable in the prodromal stages of PD up to seven years before clinical diagnosis [33]. Reduced vocal frequency range has been positively correlated with both activities of daily living score and motor performance score on the UPDRS [34]. Changes in voice and swallowing in PD are highly correlated to decreased measures pertaining to quality of life [35].

While changes in voice and swallowing are known in PD, there is a paucity of objective information on patient perceptions of the handicapping effects imposed by voice and swallowing disturbances in PD compared to disease duration and the relationship of voice and swallowing handicap compared to each other.

Past studies have included small numbers of participants, used informal interviews as to swallowing performance or used yes/no questions (thus prohibiting a range of responses) [16, 32]. Other failing of past research includes assessment of swallowing problems only focused on liquid intake [21,36, 21,36]. Some studies have used patient reported outcomes questionnaires specifically designed for other patient populations (such as the head and neck cancer population) [35]. In addition, the emotional (e.g., fear of choking or embarrassment of poor vocal quality), physical (e.g., coughing while eating or using great effort to talk), and functional (e.g., changes in diet or repeating to be heard) handicapping effects of swallowing and voice problems in PD have not been explored as related to disease duration. While a disruption in sensory/perceptual feedback in PD may exist, it remains important to explore the self-perceived handicapping effects of dysphagia and dysphonia. Understanding timing of self-perceived voice and swallowing handicap in PD adds to the overall clinical picture of the patient and may assist in timely intervention for communication and swallowing preservation.

The Voice Handicap Index (VHI) and the Dysphagia Handicap Index (DHI) patient reported outcomes measures, validated with a variety of medical disorders, identify physical, emotional, and functional handicapping effects of voice and swallowing [37–38]. The aim of this study was to determine if significant differences exist in self-perception of voice and swallowing handicap in individuals with PD as related to time since diagnosis. A secondary aim was to determine if there is a significant relationship between self-perceived voice and swallowing handicap from time of diagnosis in PD.

METHODS

The DHI and VHI were administered to 277 PD patients who attended a movement disorders clinic in a suburban outpatient hospital setting during a one-year period. Patient name, age, gender, and medical record number were identified prior to questionnaire administration based upon review of the daily clinic schedule. Exclusion criteria were defined in the IRB protocol and chart review took place after questionnaire completion to exclude subjects from the study if they had deep brain stimulation (DBS), history of a significant neurological disorder besides PD, history of head and neck disorders (for example, head and neck cancer, vocal fold paralysis), prior swallowing or voice therapy or significant cognitive disorder. Cognitive impairment was based upon the patient’s history and the physicians’ informal assessment of the patient’s mental status at the time the questionnaires were completed. Date of PD diagnosis by a movement disorders specialist was also established through chart review. Patients were asked to complete the DHI and VHI questionnaires at the beginning of their appointments by the medical assistants who also collected the completed questionnaires at the end of the appointment. Since the DHI and VHI are self-reported questionnaires, there were no specific instructions given to the patients.

For assessing the relationships between duration of PD and the DHI/VHI measurements, three duration groups were selected to represent short, medium, and long duration of PD. The definitions for these three levels were 0–4 years, 5–9 years, and 10 or more years. Demographic and DHI/VHI information were compared among these three duration groups using chi-squared tests (gender), analysis of variance (ANOVA) methods (age and DHI/VHI scores) and Wilcoxon two sample tests (self-severity and overall voice). Since all three pairwise comparisons of duration were of interest, an alpha level of 0.05 was used for all comparisons. No adjustments were made for multiple comparisons. All analyses were done using SAS version 9.4. Comparisons of correlations between VHI and DHI measurements and comparing correlations of duration of PD with VHI and DHI were performed. Pearson’s correlation coefficients were compared to assess both the relationship between the VHI and DHI measurements, and the relationship of duration of PD with the VHI and DHI measurements. Williams’ test was used to compare the correlations of PD duration with VHI measurements to the correlations of time with DHI measurements [39].

The research was performed in accord with the Helsinki Declaration of 1975 and was approved by the Henry Ford Hospital institutional review board (IRB). Given the low risk of patient harm for completing a written survey, informed consent was waived by the IRB for this study.

RESULTS

Of the 277 individuals with PD included in the analysis who completed the DHI assessment, 117 (42%) were female and 160 (58%) were male. The mean age was 69.2 (s.d. = 10.9) years (range:35–95). The mean duration of PD was 6.2 (s.d. = 5.3) years (range: 0 to 26 years). There were 123 (44%) of the subjects in the shortest (0–4 years), 101 (36%) in the medium (5–9 years) and 53 (19%) in the longest (10 + years) duration groups. There were no significant differences in gender and age among the three PD groups with different durations (Table 1).

There were no significant differences for the DHI measurements and self-severity score when comparing the duration groups of 0–4 years with 5–9 years. However, the differences emerging between the longest duration (10 + years) and the shortest duration groups were significant for all DHI measurements, as well as for the self-assessment severity score. When comparing the 5–9 years and 10 + years duration groups, the differences were significant for the functional, physical and total DHI measurements. For all significant comparisons the 10 + years duration group had higher averages for DHI measurements and higher self-assessment severity scores (Table 2).

There were no significant differences for the VHI measurements and self-severity score when comparing the PD duration groups of 0–4 years with 5–9 years. However, the difference between the longest duration (10 + years) and the other two shorter groups were significant for all VHI subscale measurements, as well as for the total VHI score. For all significant comparisons, the 10 + years PD duration group had higher averages for VHI measurements and higher self-assessment severity scores (Table 2).

All correlations of time between the VHI and DHI measurements for the sub-scales and total scores exceeded 0.45 (p < 0.001 for all). The correlations of PD duration groups with their corresponding VHI and DHI measurements were significant (p < 0.03 for all). No differences were detected when comparing the correlations of PD duration with VHI to the correlations of PD duration with the DHI measurements (Table 3).

DISCUSSION

The results of this study indicate that people with PD reported that they had significantly greater changes in the handicapping effects of dysphonia and dysphagia in the later stages of PD compared to earlier stages. In addition, responses of PD patients on the VHI and DHI demonstrate high correlations indicating that perceptions of vocal handicap closely match perceived severity of swallowing handicap over the duration of this illness. The DHI and VHI responses over the different PD duration groups, along with the positive correlation of these measures with PD duration, indicate that self-perceived emotional, physical and functional handicapping effects of voice and swallowing problems progress with the duration of PD.

From a vocal standpoint, with increasing PD duration, the increasing report of how much dysphonia is handicapping may be due partly to impairment in sensory/perceptual feedback [7, 40]. As compared to healthy controls, patients with PD can overestimate their vocal loudness (in decibels) during reading and conversation as well as during playback of their voice [41]. Furthermore, it is possible that people with PD expect their voice to worsen with age; therefore, if diagnosed with PD in mid-later life, a patient may assume that a quiet, harsh, or breathy voice is normal. Recognition of vocal problems may be unrecognized as a handicap until later in the illness as dysphonia worsens and when feedback from listeners to repeat utterances may be an increasing experience.

The results of self-perception of the handicapping effects of dysphagia indicate that although PD patients judge swallowing handicap to be significantly worse from a physical and functional standpoint in later years since diagnosis compared to earlier, their perception of emotional handicap is less clear. It seems that PD take longer to recognize fear or embarrassment of swallowing problems over more obvious physical threats (such as choking while drinking) or imperatives such as needing to change their diet. A levodopa regimen may effectively mask any inklings of dysphagia for some patients in the early stages of PD [22]. Therefore, the recently diagnosed PD group tends to benefit from dopaminergic therapy for improving swallowing function, an outcome that like other motor features may decline over time. Past studies indicate that only one quarter of individuals with advanced PD demonstrate improved swallowing on videofluoroscopic swallowing studies (VFSS) in the “on” condition (following administration of dopaminergic medication) compared to the “off” condition, when PD symptoms have re-emerged, possibly indicating that dysphagia, like other motor symptoms of PD, is difficult to control with advanced illness [42]. Individuals in later years of diagnosis reported significantly worse self-severity of overall dysphagia than those in the earlier and mid-years from diagnosis likely indicating that dysphagia had to become severe to be recognized as a handicap. This finding is consistent with past reports that self-reported voice and swallowing problems in PD worsen with disease progression [8, 43]. Reduced awareness of the handicapping effects of dysphagia is not unexpected in the PD population given the slow progression of the illness. Patients may have learned to adapt to slowly developing changes with smaller bolus sizes, careful swallowing, and taking more time during meals. Individuals with PD may also perceive dysphagia as a normal process of aging and learn to accept their new challenges as normal [44]. Research has shown that cortical areas modulate swallowing in a clinically relevant way in addition to brainstem and basal ganglia circuits [45]. It is therefore possible that the subjects in this study demonstrated recruitment of preserved cerebral motor pathways driven by sensory afferent input to maintain swallowing function until neurodegeneration progressed to the point of precluding adaptive strategies finally resulting in self-perceived dysphagia at the later stages of disease [45].

It has been reported that dysphagia in the first-year post diagnosis may indicate atypical PD or other neurological condition, such as multi system atrophy or progressive supranuclear palsy, possibly confirming that the subjects in the current study had typical idiopathic PD [25].

The longer one goes without dysphagia the lower the risk of aspiration and the greater the survival time further supporting the need for early recognition of swallowing skills and perception of swallowing handicap in this population [25]. However, correct diagnosis of PD may be limited in the early prodromal stages of the disease [46]. In order to capture the most reliable time of diagnosis of PD in this study, the date of a physician’s medical diagnosis of PD in the patient records was used to determine PD onset instead of time of first symptoms. It is likely that the subjects in this study may have had PD for years before diagnosis therefore awareness of the handicapping effects of dysphagia or dysphonia may have been closer to the onset of PD than represented.

The results of this study indicate that there is a linear trend of self-perceived handicapping effects of voice and swallowing throughout disease progression. Since patients with PD identify changes in voice and swallowing at a similar pace, close monitoring of both symptoms in the earliest stages of disease is important.

Currently, there is an emphasis on the need to use clinically meaningful markers of disease progression in PD for clinical trial development and improving patient care [47]. The VHI and DHI patient reported outcomes measures provide clinically relevant information on voice and swallowing handicap in a quick, non-invasive manner. Progression of dysphagia and dysphonia in PD is a slow process and there can be a lack of awareness until symptoms are relatively severe. However, since symptoms of PD may appear years before diagnosis is made, it is important to identify handicapping effects of the disease as soon as possible by using robust and validated patient reported outcomes measures. This study did not screen for medication “on-off” status since the VHI and DHI are general questionnaires about the overall physical, emotional and functional perceptions of handicap in daily living. Future studies may include more specific comparisons to medication schedules. A further limitation of this study is the absence of test-re-test reliability data from the questionnaires which would have assisted in further establishing reliability of patients’ perceived impressions of their voice and swallowing handicap. This is particularly important since PD patient’s perceived judgment of their dysphagia and dysphonia is frequently inconsistent with objective measures of voice and swallowing. Future studies should include test-retest reliability studies of patient reported outcomes questionnaires in individuals with PD. In addition, further studies of comparisons of valid and reliable patient reported outcomes measures with objective voice and swallowing data over the course of PD will provide a more robust picture of the progression of dysphagia and dysarthria in PD and assist in the care of individuals with PD.

CONCLUSION

This study provides new information regarding self-perception of the handicapping effects of voice and swallowing problems in PD as related to time since diagnosis. The handicapping effects of dysphagia and dysphonia are greater in later years compared to soon after PD diagnosis. Compensatory strategies for improving voice and swallowing may succeed until disease progression precludes the ability to make adaptive changes. DHI and VHI responses over the duration groups exhibited positive correlation with PD duration. Subjects also had changes in voice and swallowing handicap at a similar pace throughout the course of PD. The risks of silent aspiration from dysphagia and social isolation from poor communication in PD, support the use of robust validated and reliable patient reported outcomes measures to identify voice and swallowing handicap and initiate voice and swallowing treatment as soon as possible in PD.