Keywords
neurology - speech therapy - swallowing - parkinson's disease - deep brain stimulation
Introduction
Deep brain stimulation (DBS) of the subthalamic nucleus (STN) is an established treatment
for Parkinson's disease (PD). The beneficial effects of DBS in reducing motor symptoms
in individuals with PD are robust, and have been reported in the literature.[1]
[2]
[3] However, there is little evidence regarding the effect of DBS on the non-motor symptoms
of PD, such as dysphagia.[1]
[4]
[5]
[6]
According to the literature, dysphagia may occur independently of the phase of PD,
and have a prevalence of 31% to 100% of patients with PD.[7] Among the clinical signs of dysphagia observed in patients with PD are: increased
oral transit time; difficulty in forming the bolus; residue in the oral cavity; weak
ejection of the bolus; multiple swallows; posterior escape of the bolus, reflecting
decreased swallowing; change in the closing of the vocal folds; reduction in pharyngeal
and esophageal motility; food stasis in the pharynx; laryngeal penetration and aspiration;
dysfunction of the esophageal sphincter; and gastro-esophageal reflux.[8]
[9]
[10]
[11]
Some complications that may be caused by dysphagia are: malnutrition; dehydration;
and aspiration pneumonia. Pneumonia is the most common cause of death in patients
with PD.[12]
Various screening tests, including clinical evaluations of pulse oximetry, have been
used to detect silent aspiration. These tests have sensitivities of 27 to 100%, and
specificities of 39 to 97%. Thus, the clinical evaluation of dysphagia is important.[13]
Existing studies on DBS claim that the surgery does not negatively affect swallowing,
but there is still no evidence that it is an effective form of treatment for dysphagia
in patients with PD.[1]
[14]
[15]
[16] In the studies by Ciucci et al[14] and Lengerer et al,[15] no significant change in the swallowing evaluation after the completion of DBS was
observed. Corroborating these findings, Kulneff[1] also did not observe clinical changes in swallowing, but found an improved self-evaluation
of swallowing after DBS. However, the Silbergleit study[16] reported improvements in oral motor control of the oropharynx regarding solid food
consistency. It thus appears that the evidence for the effects of DBS on dysphagia
is still inconclusive and conflicted. The objective of this study is to compare the
swallowing and quality of life of individuals with PD before DBS surgery to their
swallowing after DBS surgery.
Material and Methods
We performed a longitudinal descriptive study. Our sample consisted of people who
had undergone bilateral DBS of the subthalamic nucleus between January 2014 and March
2015 in a referral hospital in the city of Porto Alegre, Rio Grande do Sul, Brazil.
All individuals who had undergone surgery during this period participated in the research.
The inclusion criteria were a diagnosis of PD according to the United Kingdom Parkinson's
Disease Society Brain Bank criteria for idiopathic PD[17] and having undergone DBS surgery. All participants were informed of the purpose
of the research, and signed an informed consent form. The study was approved by the
research ethics committee of the hospital.
Procedures
The following procedures were performed before (a maximum of thirty days) and after
(between six months to one year) the surgery: anamnesis, clinical evaluation, evaluation
using the the Functional Oral Intake Scale (FOIS), staging of PD using the Modified
Hoehn and Yahr (H&Y) scale, and classification of the motor subtype of the patient
as either hard/akinetic or trembling based on a records review. The motor subtype
assessments were performed by a neurologist who is an expert in movement disorders.
The anamnesis was used to gather information regarding age, gender, education, and
duration of the disease.
These procedures were performed in two stages (pre- and post-surgically), and were
designed to not only observe a single moment of swallowing during an objective examination,
but also to assess functionally how the patients ate a full meal by checking for the
clinical signs of dysphagia described below.
The clinical evaluation of swallowing was performed by a certified speech therapist,
previously trained to apply the protocols. All the assessments were conducted by the
same professional. This assessment had the purpose of checking for signs and symptoms
of oropharyngeal dysphagia. We used solid food consistency (half portion of bread)
and liquid (100 mL of water) evaluated by free demand using cervical auscultation
and an oximeter. The signs and symptoms were analyzed based on the literature on this
field.[18]
[19] We assessed the presence or absence of coughing, gagging, tongue projection, side
head projection, head projection, noise, food residue, periorbicular contraction,
and lip interposition.[14]
[16]
[20]
At the end of the clinical evaluation, the intake of food was scored according to
the FOIS. This scale scores the level of oral food intake of the patients at particular
levels, from 0 (restricted to alternative food pathway) to 7 (total oral intake without
restrictions), with the aim of monitoring the patients' evolution during the therapeutic
process. The valid and reliable instrument has a coefficient of inter-rater reliability
that ranges from 0.98 to 0.99, with Kappa coefficient average values between 0.86
and 0.91, with appropriate consensual validity (Kendall 0,90 agreement) and criterion
validity (based on The Mann Assessment of Swallowing Ability).[21] A translated and validated version for Brazilian Portuguese was used.[22] At the end of the evaluation, the swallowing of the individual was classified as:
-
– Normal: normal for both consistencies and all items.
-
– Functional: it can be normal or changed, but does not result in worsening efficiency
of swallowing or aspiration; it is possible to maintain adequate nutrition and hydration
orally.
-
– Dysphagia: when there is a risk of penetration and laryngeal aspiration.
To classify the patients' stage of PD, we used the H&Y Degree of Disability Scale,
which has the purpose of indicating the general state of the patient. It consists
of five classification stages used to assess the severity of PD, and it essentially
measures global signs and symptoms.[23]
The instruments Parkinson Disease Questionnaire-39 (PDQ-39), translated to Portuguese,
and the Beck Depression Inventory (BDI) were applied. These tests were used to verify
the influence of depression and quality of life in the swallowing function.
We performed a descriptive analysis of the data for the continuous variables (age,
education, disease duration, PDQ-39, BDI, and FOIS). The results were expressed as
means and standard deviations (SDs). For the nominal variables, which were swallowing
and signs and symptoms of dysphagia, the results were presented as percentages. We
used McNemar's test to assess the differences between the signs and symptoms of dysphagia
pre- and post-DBS. The analyses were performed using the Statistical Package for the
Social Sciences (SPSS, SPSS Inc., Chicago, IL, US) software, version 18.0. All tests
were stipulated to have a 5% error.
Results
Our sample consisted of 10 male individuals, 63.6% were married. The average age was
57.3 years (±4.7), the mean duration of the disease was 13.0 years (±2.4), and the
mean level of education was 8.1 years (±4.0).
Concerning the motor symptoms, clinical improvement was observed in all patients after
DBS during a medical evaluation, and no modification was associated with the motor
subtype (postural tremor and rigidity). This information was extracted from the patients'
medical records. The levodopa equivalent dose was not modified before and after surgery
during the period of this study.
[Table 1] contains the patients' sociodemographic information and their clinical and swallowing
profiles.
Table 1
Sociodemographic and clinical profile pre- and post DBS
|
Age
|
Level of education
|
Disease duration
|
H&Y
|
Motor
|
FOIS
|
Swallowing
|
|
Pre
|
Post
|
Pre
|
Post
|
|
01
|
60
|
2
|
14
|
3
|
Rigid
|
7
|
7
|
Functional
|
Functional
|
|
02
|
54
|
4
|
14
|
4
|
Tremor
|
7
|
7
|
Dysphagia
|
Functional
|
|
03
|
64
|
5
|
12
|
2
|
Tremor
|
7
|
7
|
Dysphagia
|
Functional
|
|
04
|
49
|
15
|
10
|
3
|
Rigid
|
7
|
7
|
Functional
|
Dysphagia
|
|
05
|
52
|
7
|
15
|
3
|
Rigid
|
4
|
4
|
Dysphagia
|
Dysphagia
|
|
06
|
56
|
12
|
8
|
2
|
Rigid
|
7
|
7
|
Dysphagia
|
Dysphagia
|
|
07
|
63
|
6
|
15
|
3
|
Rigid
|
7
|
7
|
Dysphagia
|
Functional
|
|
08
|
56
|
8
|
13
|
3
|
Tremor
|
6
|
4
|
Dysphagia
|
Dysphagia
|
|
09
|
60
|
10
|
16
|
3
|
Rigid
|
7
|
7
|
Functional
|
Functional
|
|
10
|
59
|
12
|
13
|
3
|
Rigid
|
7
|
7
|
Functional
|
Functional
|
Abbreviations: DBS, deep brain stimulation; FOIS, Functional Oral Intake Scale; H
& Y, Hoehn & Yahr staging Scale.
As shown in [Table 2], we observed no significant differences in the presence or absence of signs and
symptoms of dysphagia before and after surgery.
Table 2
Findings in the swallowing evaluation pre and post-DBS
|
Signals and symptoms
|
Pre
n (%)
|
Post
n (%)
|
p
|
|
Alteration of orbicular contraction
|
6 (60)
|
1(10)
|
0.063
|
|
Alteration in mentalis contraction
|
3 (30)
|
1 (10)
|
0.5
|
|
Head movement
|
6 (60)
|
2 (20)
|
0.219
|
|
Noise during swallowinge
|
5 (50)
|
4 (40)
|
1.00
|
|
Residue after swallowing
|
4 (40)
|
5 (50)
|
1.000
|
|
Tongue projection during swallowing
|
4 (40)
|
0
|
*
|
|
Choking during swallowing
|
3 (30)
|
2 (20)
|
1.000
|
|
Coughing during swallowing
|
1 (10)
|
2 (20)
|
1.000
|
Abbreviation: DBS, deep brain stimulation.
Notes: McNemar's test; * we could not perform statistical tests; e = sample.
We observed a positive impact of DBS on the quality of life of the individuals. Regarding
depression and cognitive aspects, we observed no changes between pre- and post-DBS.
These data are presented in [Fig. 1].
Fig. 1 Comparison of cognitive assessment, depression, and quality of life pre- and post-DBS.
Abbreviations: BDI, beck depression inventory; PDQ, Parkinson disease questionnaire;
MMSE, mini mental state examination; MOCA, Montreal cognitive assessment.
Discussion
Our results demonstrate that there was no significant improvement in swallowing in
the patients after DBS. These findings corroborate those reported in the literature,[1]
[3]
[14] and indicate that there are no significant changes in the swallowing evaluation
in the patients after DBS. Previous studies, however, did not address a possible relationship
between the effects of DBS on the triad of PD motor symptoms and post-surgery swallowing.
They also did not report whether patients with tremor motor symptoms had patterns
of swallowing pre- or post-DBS that differed from those of patients who had postural
tremor and rigidity. As in our study, the motor subtype was not associated with swallowing.
However, the patients showed mild changes in the clinical evaluation that interfered
with the improvement in their quality of life.
With the motor improvements, the patients decreased the oropharyngeal compensation
during the feeding process. Six patients had their orbicular contraction changed pre-DBS,
and just kept those changes post-DBS. Regarding the head movement, six patients had
preoperatively, which can cause a new exhaust feed and only two maintained postoperatively.
Some studies[1]
[3]
[14]
[24] with samples similar to ours and one study with a larger sample (18 subjects)[3] indicate that there is a maintenance of the standard swallowing pattern after the
completion of the DBS, regardless of the position of the electrodes and the stimulator
settings (amplitude, frequency, pulse width). Even though the aforementioned studies
found improvements in some aspects of swallowing and tongue movement, including in
the swallowing reflex during the laryngeal phase and the pharyngeal transit time,
none found overall improvements in swallowing. The same was observed in our study.
Even though clinically an improvement in swallowing due to an improvement in motor
aspects was expected, perhaps a long-term follow-up of these patients in order to
determine the effect of the motor issues in swallowing is necessary.
In the literature review, the articles that evaluate swallowing and DBS[1]
[3]
[14]
[24] do not mention the individual parameters of each patient; the only article that
refers to the parameters describes them in function of evaluating with DBS on and
off. The parameters are different in each patient, and because of our small sample,
it was not possible for us to evaluate the correlation with these data. According
to the following parameters, there is no first and post-surgery, the data are being
collected, and the new evaluation of swallowing will be performed later.
In the study analyzing post-DBS swallowing with the largest sample so far, Lengerer
et al[15] used videofluoroscopy to analyze 18 subjects without dysphagia who underwent DBS
in the pre-operative period, and suggested a little improvement in swallowing after
surgery. Even though they observed a significant decrease of up to 70% in the late
pharyngeal reflex, a decline by up to 16% in pharyngeal transit time after surgery
was observed. The pharyngeal reflex time decreased by up to 18% following DBS. Moreover,
the duration of the opening of the cricopharyngeus was decreased by up to 21% after
the operation.
These results were also corroborated by a study by Kitashima et al3 in which there was some improvement in the signs and symptoms of dysphagia without
an improvement in the overall function of swallowing.
We observed an improvement in the total quality of life (QoL) scores following DBS,
which is in agreement with the studies by Volkmann et al[25] and Tykocki et al[26], who found a significant reduction in the depressive symptoms and motor signs, and
an improved QoL in patients with PD after DBS.
Even though these studies compare QoL before and after DBS,[25]
[26]
[27] they do not analyze swallowing in the same manner as we do here. However, since
swallowing is a factor with a significant impact on QoL, it is evident that we need
to analyze it in studies of QoL.
We found no significant changes in the average BDI score after DBS. Our findings corroborate
previous reports in the literature,[28]
[29]
[30]
[31]
[32] which indicate that there are no significant variations in the symptoms of depression
after DBS. The same is observed when comparing individuals with PD who have undergone
DBS with those who have not undergone DBS. Aono et al[33] noted an improvement in the depressive symptoms one month after DBS. However, this
improvement was not sustained over the period of one year, and was not correlated
with the state of motor function. Thus, the findings regarding the effects of DBS
on depressive symptoms are inconclusives.
Conclusion
We concluded that there was an improvement in the QoL of the patients after DBS. However,
the decrease of the clinical signs and symptoms of dysphagia did not impact the overall
improvement in the swallowing function. Additionally, we observed the relationship
between PD motor subtype and swallowing pre- and post-DBS in this sample.
