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DOI 10.1007/s00455-009-9265-5
ORIGINAL ARTICLE
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H. G. Seo et al.: Swallowing Process Changes in Stroke Patients
swallowing-motion analysis in patients with dysphagia due upright in a chair for the duration of the study and were given
to different etiologies [15]. However, few reports have 2 and 5 ml of diluted barium (35% w/), pudding, curd-type
been issued on longitudinal changes in the swallowing yogurt, and boiled rice twice in a spoon. A 24-mm-diameter
process after stroke, especially changes related to recovery coin was taped under the chin at midline to serve as a
from aspiration using a kinematic analysis method. dimensional reference. Frame-by-frame images were
The purpose of this study was to investigate longitudinal acquired to digital imaging files using a computer-based
changes in the kinematic and temporal characteristics of image processing system equipped with a digital computer
the swallowing process in subacute stroke patients with frame grabber board (Pinnacle Studio MoviBox DV;
aspiration. We hoped to identify factors related to recovery Pinnacle System, Inc., Mountain View, CA) and image
from aspiration. processing software (Pinnacle Studio 9.0). The X-ray volt-
age was set at a 40-kV peak, which allowed the soft tissues of
pharyngeal structures to be visualized.
Materials and Methods The images were analyzed by two physiatrists who had at
least 2 years’ experience with VFSS and dysphagia
Subjects management under the supervision of a senior physician.
Conclusions were drawn by consensus. The videofluoro-
In this retrospective study, we reviewed our hospital’s VFSS scopic dysphagia scale (VDS) [17] and the American
database covering the period from May 2005 to May 2008. Speech-Language-Hearing Association National Outcome
Only patients diagnosed by a neurologist as having experi- Measure System (ASHA NOMS) swallowing scale [18]
enced acute stroke that was confirmed by computed tomog- were used to produce result scores. The VDS includes 14
raphy (CT) or magnetic resonance imaging (MRI) were items that represent oral and pharyngeal swallowing func-
selected. In the 337 stroke patients who were initially selected, tions in the VFSS, such as oral transit time, mastication,
28 cases that met the following inclusion criteria were inclu- premature bolus loss, laryngeal elevation, aspiration, and
ded in this study: (1) initial VFSS (T1) performed during the vallecular and pyriform sinus residue. The VDS is a negative
subacute stage from 1 to 12 weeks after stroke onset, (2) at rating system and provides a maximum possible score of
least one follow-up VFSS (T2) performed at 2-4 weeks after 100, that is, a score of zero means a completely normal
T1, and (3) definite subglottic aspiration on 2 or 5 ml of liquid finding. The ASHA NOMS scale represents the current state
at T1. Patients with a history of previous stroke or some other of diet in dysphagic patients.
disease that could affect swallowing function, such as Par-
kinson’s disease, bulbar palsy, brain tumor, or head and neck Two-Dimensional Motion Analysis
cancer, were excluded prior to the initial selection. Fifty-one
patients were excluded because their initial VFSS were per- Videofluoroscopic studies were recorded at a resolution of
formed before 1 week or after 12 weeks poststroke. In the 720 9 480 pixels at 30 frames per second. The images of
remaining 286 patients, definite aspiration was noted in only the first attempt to swallow 2 ml of liquid were analyzed as
71 patients. Twenty-eight patients who underwent follow-up we previously described [15]. In brief, locations of the
VFSS at an adequate period of time without any significant anterior-superior margin of the hyoid bone, the base-to-tip
medical aggravation, which was potentially hazardous to margin of the epiglottis, and the head of the bolus were
functional recovery, were finally selected. digitized for each frame using a motion analysis software
All patients were treated for dysphagia after an initial system (Ariel Performance Analysis System; Ariel
swallowing assessment using a routine protocol that Dynamics, Inc., Trabuco Canyon, CA). To calculate the
included diet modification and a daily treatment session coordinates of points, we defined the y axis as the straight
with a therapist, which involved posture education, exer- line connecting the anterior margins of the inferior end-
cise, and pharyngeal stimulation for 30 min. Patients with plates of the fourth (the zero point) and second cervical
persistent aspiration were allocated to the nonrecovered vertebral bodies, and we defined the x axis as the line
group, and those that recovered from aspiration at T2 were perpendicular to the y axis passing through the zero point
allocated to the recovered group. (Fig. 1). Data were transformed into actual distances and
The study protocol was approved by the Institutional angles using the dimensions of the above-mentioned coin.
Review Board at our hospital. The initial epiglottic angle was defined as 0°. The time
reference point (time 0) was defined as the moment when
Videofluoroscopic Swallowing Study (VFSS) the head of the food bolus passed the angle of the man-
dibular ramus at the base of the tongue [16]. The vertical
VFSS was performed using a modification of the protocol and horizontal motions of the hyoid bone and angles of
initially described by Logemann [16]. Subjects were seated epiglottic downward tilt were plotted (Fig. 2a).
123
H. G. Seo et al.: Swallowing Process Changes in Stroke Patients
Results
123
H. G. Seo et al.: Swallowing Process Changes in Stroke Patients
Fig. 2 a Example graphs of the vertical and horizontal motions of the initiation of hyoid motion; Hm, time to maximal excursion of hyoid
hyoid bone and angles of epiglottic downward tilt. b A superimposed motion; Ht, time to termination of hyoid motion; Hd, duration of
graph of the vertical motion of the hyoid bone, the angle of epiglottic hyoid motion; Ei, time to initiation of epiglottic tilt; Em, time to
downward tilt, and bolus location. Temporal and spatial variables are maximal angle of epiglottic tilt; Et, time to termination of epiglottic
represented. MaxHV, maximal vertical excursion of hyoid bone; tilt; Ed, duration of epiglottic tilt
MaxEA, maximal angle of epiglottic downward tilt; Hi, time to
Table 1 Patient characteristics (n = 28) difference was observed between the two groups. At both
a T1 and T2, the maximal angle of epiglottic tilt was smaller
Age (years) 66.9 ± 11.0
in the nonrecovered group than in the recovered group, but
Gender (M/F) 19/9
these differences were of marginal significance (P = 0.174
Type of stroke (n)
and P = 0.056, respectively).
Ischemic stroke 23
Hemorrhagic stroke 5
Location of lesion (n)
Supratentorial lesion 15 Discussion
Infratentorial lesion 13
Side of lesion in the brain (n) The results of this study show that significant improve-
Right side 16 ments in swallowing occur with respect to the temporal
Left side 12 aspects of the hyoid bone and epiglottic movements in
Timing of aspiration (n) subacute stroke patients with dysphagia. Furthermore, the
Preswallowing 5
majority of temporal variables of the hyoid bone and epi-
During swallowing 22
glottic movements in the nonrecovered group were delayed
Postswallowing 1
significantly compared to those in the recovered group at
T1. Although temporal differences between the two study
Time from onset to initial study (days)a 26.0 ± 13.9
groups disappeared at T2, aspiration persisted in the non-
Time from onset to follow-up study (days)a 49 ± 17.7
recovered group.
Interval between 2 studies (days)a 23 ± 7.6
The latency to the initiation of hyoid motion in this
All other values are the number of patients study is the same as stage transition duration (STD), which
a
Values are means ± standard deviation was defined by Robbins et al. [19] as the time from when
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H. G. Seo et al.: Swallowing Process Changes in Stroke Patients
Table 2 Comparisons of temporal and spatial variables at initial and aspirators on 5 ml was 1.28 s in this previous study, which
follow-up studies concurs with our T1 data (1.33 s). However, they did not
Variables Initial Follow-up P value* present changes over time. On the other hand, we studied
longitudinal changes between initial and follow-up studies
Mean SD Mean SD
in stroke patients. Although all patients in our study
MaxHV (mm) 15.51 5.35 14.80 5.83 0.543 showed greater delayed swallowing initiation at T1 com-
MaxHH (mm) 12.04 2.45 11.73 3.91 0.669 pared with normal data in previous studies, a significant
MaxEA (°) 80.64 35.33 81.63 32.93 0.795 temporal difference at T1 was found between the recovered
Hi (s) 1.33 1.03 0.68 0.82 0.002 and nonrecovered groups, and aspiration persisted after a
Hm (s) 1.88 1.11 1.25 0.85 0.003 significant improvement in swallowing initiation in the
Ht (s) 2.69 1.17 1.88 0.92 0.001 nonrecovered group. The above findings cast doubt on the
Hd (s) 1.37 0.60 1.24 0.42 0.270 notion that delayed swallowing initiation per se elevates an
Ei (s) 1.38 1.09 0.81 0.92 0.006 aspiration risk. Instead, these results suggest that delayed
Em (s) 1.98 1.13 1.28 0.97 0.004 swallowing triggering at initial VFSS is likely to portend
Et (s) 2.61 1.18 1.85 0.97 0.004 poor recovery from aspiration in subacute stroke patients.
Ed (s) 1.26 0.77 1.04 0.42 0.090 A recent study also showed that pharyngeal delay time at
an average of 3 months poststroke (range = 1–5 months)
MaxHV maximal vertical excursion of hyoid bone, MaxHH maximal
horizontal excursion of hyoid bonem, MaxEA maximal angle of
is a prognostic factor of persistent aspiration at 1 year in
epiglottic downward tilt, Hi time to initiation of hyoid motion, patients with stroke-related oropharyngeal dysphagia [20].
Hm time to maximal excursion of hyoid motion, Ht time to termi- The epiglottic downward tilt to seal the laryngeal ves-
nation of hyoid motion, Hd duration of hyoid motion, Ei time to tibule is an important protective mechanism against aspi-
initiation of epiglottic tilt, Em time to maximal angle of epiglottic tilt,
Et time to termination of epiglottic tilt, Ed duration of epiglottic tilt
ration, and as was shown by a previous study, a lack of
* P value by paired t test
functional epiglottic movement and abnormal epiglottic tilt
are highly associated with a risk of aspiration [21].
Although the maximal angle of epiglottic tilt did not
barium first passes the ramus of the mandible to the change during the follow-up period in the present study, the
beginning of maximum hyoid excursion. They also tested angle distribution among patients changed (Fig. 3). In
participants with 2-ml boluses as was used in the present particular, the dichotomous distribution of the angles
study, and STD for older normal subjects was found to observed at T1 suggested a decrease in epiglottic tilt after
range from 0.3 to 0.4 s. Kim et al. [14] reported that stroke stroke occurred in an ‘‘all or none’’ manner, which subse-
patients who aspirated had longer STD than nonaspirating quently gradually improved. However, few patients
stroke patients and normal subjects. The average STD of showed a definite change in epiglottic tilt between the two
Fig. 3 Distribution of maximal angles of epiglottic tilt at initial and distribution observed at initial and follow-up studies. The definite
follow-up studies. Left Scatterplot shows change in angle on a per- dichotomous pattern observed for initial studies was not evident for
subject basis. Right Histograms show the difference between the follow-up studies
123
H. G. Seo et al.: Swallowing Process Changes in Stroke Patients
Table 3 Comparisons of patient characteristics in the recovered and Table 4 Comparisons of temporal and spatial variables in the
nonrecovered groups recovered and nonrecovered groups
Characteristics Recovered Nonrecovered P value* Variables Recovered Nonrecovered P value*
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H. G. Seo et al.: Swallowing Process Changes in Stroke Patients
pre-, during, and post-swallowing aspiration, is one possible stroke and suggest that the VFSS may enable recovery to
factor [20]. The severity of aspiration could also play a role be predicted.
in recovery. Further analysis should incorporate these
important features of aspiration, which can be checked by
VFSS. In addition, previous studies have suggested other
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