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Dysphagia

DOI 10.1007/s00455-009-9265-5

ORIGINAL ARTICLE

Longitudinal Changes of the Swallowing Process in Subacute


Stroke Patients with Aspiration
Han Gil Seo • Byung-Mo Oh • Tai Ryoon Han

Received: 5 July 2009 / Accepted: 24 November 2009


Ó Springer Science+Business Media, LLC 2010

Abstract The purpose of this study was to evaluate Introduction


longitudinal changes of the swallowing process in stroke
patients with aspiration using kinematic analysis. Twenty- Dysphagia after stroke is a common and disabling problem
eight subacute stroke patients with aspiration on fluid at that can cause significant clinical complications such as
initial videofluoroscopic swallowing studies (VFSS) were asphyxia, aspiration pneumonia, and malnutrition. The
included. Follow-up VFSS was performed at 2-4 weeks incidence of dysphagia has been reported to be as high as
after initial studies that were conducted at an average of 80% in stroke patients in videofluoroscopic swallowing
26 days after stroke. Temporal and spatial variables were studies (VFSS) [1]. Aspiration during videofluoroscopic
calculated by two-dimensional motion analysis of hyoid evaluations is an important finding with respect to an ele-
bone and epiglottic movements. Swallowing process delays vated risk of pneumonia during the subacute stage after
associated with hyoid bone and epiglottic movements were stroke [2]. Teasell et al. [3] reported that 18 of 42 patients
improved at follow-up studies, whereas spatial variables (43%) who demonstrated evidence of aspiration on thin
were not. Fourteen patients had recovered from aspiration liquids by VFSS, performed an average of 5 weeks fol-
at follow-up. Time to the start of the hyoid movement was lowing the onset of stroke, clinically stopped aspirating an
longer in the nonrecovered patient group at initial studies average of 6 weeks after the initial VFSS. On the other
(1.76 ± 1.07 s) than in the recovered group (0.90 ± hand, aspiration by VFSS can persist for over 6 months
0.82 s, P = 0.024). Although time-associated differences after stroke in some patients [4].
between the nonrecovered and recovered groups disap- The pharyngeal stage of swallowing starts with a verti-
peared at follow-up studies, aspiration persisted in the cal and a horizontal movement of the hyoid bone caused by
nonrecovered group. This study shows that recovery from contraction of the suprahyoid muscles [5]. The whole lar-
delays in the swallowing process is a conspicuous change ynx is pulled upward and forward by passive and active
during the subacute stage in stroke patients with aspiration. mechanisms with thyrohyoid muscle contraction. This
Our findings suggest that delayed swallowing triggering at displacement tucks the larynx under the base of the tongue
initial VFSS is a useful predictor of poor recovery from [6]. Furthermore, a downward tilt of the epiglottis occurs
aspiration in stroke patients. with this laryngeal elevation and tongue retraction occurs
to seal the laryngeal vestibule [7]. These movements of the
Keywords Stroke  Deglutition  Deglutition disorders  hyoid bone and epiglottis importantly prevent aspiration
Respiratory aspiration  Recovery of function during swallowing.
Several studies have analyzed the motions of pharyngeal
and laryngeal structures using kinematic methods. These
studies investigated vertical and horizontal displacements
H. G. Seo  B.-M. Oh  T. R. Han (&) of the hyoid bone in normal subjects [8–10] and the tem-
Department of Rehabilitation Medicine, Seoul National
poral properties of pharyngeal swallowing in normal sub-
University Hospital, 101, Daehang-ro, Jongno-gu,
Seoul 110-744, Republic of Korea jects [11–13] and in stroke patients [14]. In a previous
e-mail: tairyoon@snu.ac.kr study, we examined the use of two-dimensional kinematic

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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).

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H. G. Seo et al.: Swallowing Process Changes in Stroke Patients

divided into two groups according to the occurrence of


aspiration on liquid at T2. The v2 test or Fisher’s exact test
was used to compare baseline characteristics between the
recovered and nonrecovered groups. Student’s t test was
used to determine the significance of differences between
group variables. Clinical scores were compared using a
nonparametric test such as Wilcoxon’s signed ranks test or
the Mann-Whitney test. All statistical analyses were per-
formed using SPSS 12.0 (SPSS Inc., Chicago, IL). Values
given are mean ± standard deviations(SD). P values of
less than 0.05 were deemed significant.

Results

Patient characteristics are given in Table 1. All patients


showed aspiration on diluted barium at T1: 15 patients on
2 ml and 13 patients on 5 ml of liquid. Aspiration was
noted before, during, and after swallowing in 5, 22, and 1
patient, respectively. Mean VDS scores of all 28 patients
Fig. 1 Digital coordination of the hyoid bone and epiglottis and the
control frame for the x and y axes. The zero point (0, 0) is showed no significant difference between T1 and T2
operationally defined as the anterior-inferior border of the fourth (36.0 ± 15.0 and 31.1 ± 15.8, P = 0.202), whereas the
cervical vertebra. The y axis is the line drawn from the zero point to mean ASHA NOMS score was significantly improved at
the anterior-inferior border of the second cervical vertebra, and the x
T2 (3.3 ± 1.9 and 4.5 ± 1.9, P \ 0.001).
axis is the line perpendicular to the y axis. A coin was used as a
dimensional reference Table 2 gives the differences between temporal and
spatial variables at T1 and T2. All temporal variables of
Measurements hyoid and epiglottic motion were significantly delayed at
T1 as compared with T2. However, spatial variables and
Latencies (sec) from time 0 to initiation, peak, and termi- durations of movement showed no significant differences at
nation of hyoid excursion and epiglottic downward tilt T1 and T2.
were measured. The durations (seconds, s) of hyoid and Maximal angles of epiglottic tilt showed different dis-
epiglottic motion from initiation to termination were also tributions at T1 and T2. The distribution was definitely a
recorded (Fig. 2b). Maximal excursions (mm) of the hyoid dichotomous pattern at T1 and no patient had a tilt angle of
bone in vertical and horizontal directions and maximal 50-80°. However, considerable overlap occurred between
angles (°) of epiglottic tilt were measured (Fig. 2b). All these two initially dichotomous groups at T2 (Fig. 3).
measurements were made using MATLAB 7.4 (The Of the 28 patients, 14 recovered from aspiration at T2.
MathWorks, Inc., Natick, MA). Table 3 gives patient characteristics of recovered and
The reliabilities of the measurements were confirmed by nonrecovered groups. Patients that experienced aspiration
reliability testing using the VFSS images of ten patients. on only the 5 ml of liquid at T1 tended to recover from
Briefly, the analysis was performed by two well-trained aspiration at T2 better than patients with aspiration on the
researchers using the same images, and 2 weeks later these 2 ml of liquid (P = 0.058). VDS scores showed significant
images were reanalyzed by the same researchers for the differences between the recovered and nonrecovered
variables analyzed in this study. Intrarater reliability testing groups at T1 (31.6 ± 17.3 and 40.3 ± 11.3, P = 0.048)
showed excellent agreement with intraclass correlation and at T2 (21.2 ± 12.8 and 40.9 ± 12.2, P \ 0.001),
coefficient (ICC) values ranging from 0.861 to 0.996. whereas AHSA NOMS scores showed a significant dif-
Interrater reliability testing also produced good to excellent ference between the two groups at T2 only (5.6 ± 1.2 and
results, with ICC values ranging from 0.752 to 0.995. 3.4 ± 1.9, P = 0.002).
Differences between temporal and spatial variables in
Statistical Analysis the recovered and nonrecovered groups are presented in
Table 4. Almost all temporal points at T1 were signifi-
The paired t test was performed to compare temporal and cantly delayed in the nonrecovered group with the excep-
spatial variables between T1 and T2 to evaluate longitu- tion of the initiation of epiglottic tilt. Delayed swallowing
dinal changes of the swallowing process. Subjects were in the nonrecovered group was improved at T2 and no

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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

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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*

Age (years) 70.4 ± 8.9 63.4 ± 12.2 0.091 Mean SD Mean SD


Gender (n) 0.225 Initial study
Male 8 11 MaxHV (mm) 15.22 5.48 15.79 5.40 0.787
Female 6 3 MaxHH (mm) 11.84 2.49 12.24 2.49 0.680
Type of stroke (n) 1.000 MaxEA (°) 89.83 29.11 71.45 39.53 0.174
Ischemic 12 11 Hi (s) 0.90 0.82 1.76a 1.07 0.024
Hemorrhagic 2 3 Hm (s) 1.46 1.01 2.29a
1.07 0.044
Location of lesion (n) 0.705 Ht (s) 2.15 1.04 3.24a 1.05 0.011
Supratentorial lesion 8 7 Hd (s) 1.26 0.40 1.48 0.76 0.347
Infratentorial lesion 6 7 Ei (s) 1.05 0.95 1.71a 1.16 0.110
Side of lesion in 0.127 Em (s) 1.49 1.03 2.48a 1.04 0.018
the brain (n)
Et (s) 2.12 1.12 3.09a 1.06 0.026
Right side 10 6
Ed (s) 1.07 0.32 1.45 1.02 0.200
Left side 4 8
Follow-up study
Amount of liquid 0.058
caused aspiration at MaxHV (mm) 15.36 4.91 14.25 6.77 0.623
initial study (n) MaxHH (mm) 12.08 5.04 11.38 2.48 0.646
2 ml 5 10 MaxEA (°) 93.45 27.67 69.81 34.44 0.056
5 ml 9 4 Hi (s) 0.63 0.84 0.72a 0.83 0.771
Initial MMSE a
19.4 ± 8.6 21.8 ± 7.9 0.427 Hm (s) 1.22 0.85 1.29a 0.88 0.834
Initial MBIa 36.2 ± 22.9 46.8 ± 22.1 0.228 Ht (s) 1.76 0.97 2.00a 0.89 0.492
Time from onset to 26.9 ± 13.5 25.1 ± 13.5 0.731 Hd (s) 1.20 0.34 1.28 0.49 0.616
initial study (days) Ei (s) 0.80 0.95 0.83a 0.92 0.918
Interval between 23.1 ± 7.9 22.9 ± 7.5 0.961 Em (s) 1.26 0.99 1.29a 0.99 0.937
2 studies (days)
Et (s) 1.85 0.98 1.86a 1.00 0.977
MMSE mini mental state examination, MBI modified Barthel index Ed (s) 1.05 0.36 1.02 0.49 0.873
a
Initial MMSE and MBI scores were checked in 20 patients (12 in
MaxHV maximal vertical excursion of hyoid bone, MaxHH maximal
the recovered group and 8 in the nonrecovered group) and in 24
horizontal excursion of hyoid bone, MaxEA maximal angle of epi-
patients (13 in the recovered group and 11 in the nonrecovered
glottic downward tilt, Hi time to initiation of hyoid motion, Hm time
group), respectively
to maximal excursion of hyoid motion, Ht time to termination of
* P value by the Student’s t test, the v2 test, or Fisher’s exact test hyoid motion, Hd duration of hyoid motion, Ei time to initiation of
epiglottic tilt, Em time to maximal angle of epiglottic tilt, Et time to
studies. One patient with a decreased angle at T1 (33.46°) termination of epiglottic tilt, Ed duration of epiglottic tilt
a
showed a definite improvement at T2 (82.7°) and recovered P \ 0.05 by the paired t test for comparisons between initial and
follow-up studies
from aspiration. Two patients with reduced angles at T1
* P value by the Student’s t test
(28.14° and 48.31°) had intermediate angles at T2 (71.7°
and 66.97°, respectively) but no recovery from aspiration.
Furthermore, one patient with a normal angle at T1 reported no significant difference between aspirators and
(108.85°) showed an intermediate angle at T2 (54.41°) and nonaspirators in terms of maximal hyoid displacement
failed to recover from aspiration. The maximal angle of [22]. However, both our study and this recent study had
epiglottic tilt at T2 was greater in the recovered group than relatively small sample sizes. Furthermore, maximal ver-
in the nonrecovered group with a borderline significance tical displacement differed by more than 1 mm in the
(P = 0.056). Improved epiglottic tilt might contribute to recovered and nonrecovered groups at T2. A further
recovery from aspiration after stroke but appears rarely investigation is warranted in a larger cohort if we are to
over a relatively short period of 2–4 weeks. understand the influence of hyoid displacement on aspira-
The present analysis of vertical and horizontal dis- tion in stroke patients.
placement of the hyoid bone produced no significant This study focused on the temporal and kinematic
finding. Although movement of the hyoid bone is important properties of the hyoid bone and epiglottic movements.
for swallowing, its influence on the occurrence of aspira- However, some other factors could influence the recovery
tion is questionable. A recent study in poststroke patients of aspiration. The timing of aspiration, usually classified as

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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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