Dysphagia 15:173–179 (2000)
DOI: 10.1007/s004550000024
Kinematic Analysis of Laryngeal Movements in Patients with
Neurogenic Dysphagia before and after Swallowing Rehabilitation
Mario Prosiegel, MD,1 Michaela Heintze, MA,1 Edith-Wagner-Sonntag, MA,1 Thomas Schenk, PhD,2 and
Alexander Yassouridis, PhD3
1
Neurologisches Krankenhaus München; 2Neurologische Klinik, Klinikum Grosshadern, Ludwig-Maximilians-Universität München; and
3
Department of Statistics, Max-Planck-Institut für Psychiatrie, Munich, Germany
Abstract. To examine whether kinematic analysis of la-
ryngeal movements (which are closely linked to pharyn-
geal swallowing) can differentiate between normal and
disturbed swallowing, we used a three-dimensional ul-
trasound movement recording system to measure the
movements of the larynx during swallowing in 32 pa-
tients with neurogenic dysphagia caused by central ner-
vous system lesions and in 32 age- and sex-matched
healthy individuals. At the beginning of an inpatient re-
habilitation swallowing program, laryngeal movements
in 24 patients were highly disturbed in terms of velocity
curve irregularities. After rehabilitation, the majority of
patients with hitherto irregular velocity profiles exhibited
laryngeal kinematics that were indistinguishable from
those of 32 healthy subjects. Kinematic analysis of la-
ryngeal movements, therefore, is suitable for monitoring
motor recovery of swallowing disturbances in patients
with neurogenic dysphagia while undergoing swallowing
rehabilitation.
Key words: Neurogenic dysphagia — Laryngeal
movements — Kinematic analysis — Ultrasound move-
ment recording device — Motor recovery — Rehabili-
tation — Deglutition — Deglutition disorders.
As in other areas of motor rehabilitation, motor learning
plays a pivotal role in functional swallowing therapy.
This research was supported by a grant from the Deutsches Bundes-
ministerium für Bildung, Wissenschaft, Forschung und Technologie
(01K09404/1).
Some of these data were presented at the IVth Scientific Meeting of the
European Study Group for Dysphagia and Globus (EGDG), Vienna,
October 1998.
Correspondence to: Mario Prosiegel, M.D., Neurologisches Kranken-
haus München, Tristanstr. 20, D-80804 München, Germany
© Springer-Verlag New York Inc. 2000
Patients undergoing such rehabilitation often have to
learn new motor tasks, e.g., techniques like the Mendel-
sohn maneuver [1,2] which requires “the patient to in-
crease concentration on swallowing [3].” Mathematical
models [4] predicted that skilled movements following
successful motor recovery are characterized by single-
peaked, bell-shaped velocity profiles [5,6]. This has been
confirmed by measuring the kinematics of hand and arm
movements [7–10] and of movements of hand and fin-
gers during writing [11]. Kinematic analysis (i.e., the
analysis of the velocity and acceleration) of swallowing
movements enables the researcher to study in more detail
the motor recovery that takes place during motor learn-
ing. To the best of our knowledge, the kinematics of
swallowing movements before and after rehabilitation of
patients with dysphagia have not been investigated.
Laryngeal movements play a pivotal role in the
pharyngeal phase of swallowing. One of the swallowing
techniques, the Mendelsohn maneuver [1,2], is based on
the volitional prolongation of anterior–superior larynx
movement, which widens the pharyngoesophageal seg-
ment (PES) and decreases the pressure within the PES
[12–14]. To analyze swallowing movements, we mea-
sured laryngeal kinematics in patients with neurogenic
dysphagia as well as in healthy controls. Because of the
high degree of spatial and temporal resolution needed for
this purpose, a three-dimensional (3D) ultrasound move-
ment recording system was used.
Material and Methods
Subjects
Thirty-two sequential patients admitted to an inpatient rehabilitation
swallowing program participated; 23 men and 9 women ranging in age
174
from 28 to 87 years (mean ⳱ 57.7 years). Inclusion criteria were
neurogenic dysphagia resulting from disease of the central nervous
system (CNS) as defined by history, clinical examination, and magnetic
resonance imaging (MRI); dependence on nasogastral or PEG feeding
on admission; age ⱖ18 and ⱕ90 years; acquisition of the Mendelsohn
maneuver indicated in all cases because of PES dysfunction as shown
by videofluoroscopy [15]. Characteristics of the patient sample are
shown in Table 1. Thirty-two age- and sex-matched healthy individuals
with no known history of significant oral/pharyngeal anomaly served as
controls.
Data Acquisition
Position and movement of the larynx during swallowing were tracked
using a 3D movement registration system (CMS 50, Zebris, Isny, Ger-
many). This system uses small markers (diameter ⳱ 1.0 cm, weight ⳱
1 g) which continuously emit an ultrasonic signal at a sampling fre-
quency of 200 Hz every 5 ms. Three microphones arranged within a
plane at fixed distances to each other and mounted on a stationary
frame (40 × 40 × 5 cm) receive the signals. The system measures the
transmission time from the markers to the three microphones and uses
the differences in transmission time for the different microphones to
calculate the spatial position of the markers. The system works reliably
in a workspace of 2 × 2 × 2 m and has a spatial resolution of 0.1 mm.
Movements are registered and the data stored for later offline analysis
on a PC (Pentium II fitted with PC card for the ISA Bus, developed by
Zebris). We used one marker attached with double-sided tape to the
skin just at the area of the thyroid notch midline. The distance between
the frame and the subject was 1 m. This method does not permit
measurement of the full range of laryngeal movements because the
marker, which is attached to the skin and not to the larynx itself, cannot
fully follow the movement of the larynx. Nevertheless, it is still pos-
sible to measure the velocity characteristics of the larynx.
The same device used in this study has already been used for
kinematic analysis of hand and arm movements [9,10].
The 3-D movement registration system is illustrated in Figure 1.
Data Analysis
The positional data coming from the CMS 50 are associated with a
random spatial error of approximately ±0.58 mm. If unfiltered, this
results in a dynamic error of 82 mm/s and 11,600 mm/s2 for the first
and second derivatives, respectively. We used a nonparametric estima-
tion of regression functions based on kernel estimates [16]. This
method has been evaluated using simulated and real data sets. The
results obtained with the kernel estimates are very similar to those
obtained with more conventional filter methods [far infrared (FIR) and
butterworth filters]. Although kernel estimates show a slightly elevated
bias for the second derivative, they reduce the residual variance in the
derivatives more efficiently than both FIR and butterworth filters. In
addition, filtering with kernel estimates offers a very fast method of
data smoothing. This filter method was initially developed for the
analysis of positional data coming from a digitizing board [11], but it
can be adapted to the analysis of 3D position data coming from the
CMS 50. However, since the error characteristics are different for the
CMS 50 (see above) and the digitizing board, the bandwidths of the
filters have to be adapted. Simulation studies showed that the optimal
bandwidths for data coming from the CMS system are 50 ms/12 Hz, 70
ms/10 Hz, and 90 ms/8.5 Hz for the zeroth, first, and second deriva-
tives, respectively [11].
M. Prosiegel et al.: Motor Recovery in Swallowing Rehabilitation
In order to assess “normality” or “abnormality” of laryngeal
movements, we compared the duration and velocity profiles of down-
ward movements in patients with neurogenic dysphagia before swal-
lowing treatment with those of healthy controls. Duration of movement
is an obvious choice, because it describes the efficiency of a movement
in a simple way. If the same movement can be performed in less time,
this is clearly an advantage. Since the velocity profiles of skilled and
overlearned movements are highly stereotyped, the velocity profile is
an attractive yardstick for distinguishing between normal and abnormal
movements. In the case of prehensile movements, handwriting, and
saccadic eye movements, it has been shown that the velocity profile for
a single movement (i.e., one prehensile movement toward an object,
one upward or downward stroke in handwriting, one saccade) has a
characteristic bell-shaped form, is almost symmetrical, and has only
one peak [7,11,17]. In contrast, during skill acquisition [18] or in patho-
logical cases [19], the velocity profile is multipeaked and irregular.
In the present study, we investigated whether kinematic mea-
sures that have been applied successfully for distinguishing normal
from abnormal movements in other domains of human movements can
also be used to characterize normal or abnormal swallowing move-
ments. For quantitative characterization of the velocity profile, we used
the number of positive peaks, the duration of movement, and the peak
amplitude of the velocity profile (peak velocity).
We restricted our analysis to the downward movement for three
reasons: First, healthy individuals did not exhibit substantial differ-
ences in kinematics between posterior–anterior (forward), inferior–
superior (upward), and superior–inferior (downward) movements. Sec-
ond, the Mendelsohn maneuver requires volitional prolongation of up-
ward and forward movements of the larynx. Thus, the downward
movement is least susceptible to the effect of this swallowing tech-
nique. Third, the signal–noise ratio is much worse for movements in the
posterior–anterior axis than for those in the superior–inferior axis, since
the range of movement in the forward direction is less than that in the
downward direction.
Procedure
Laryngeal kinematics were measured twice for each patient, the first
time prior to commencing the rehabilitation program and the second
time at discharge. The patients as well as the controls were instructed
to sit as comfortably as possible and to try to swallow normally. In
order to avoid significant aspirations, only dry swallows were per-
formed by each person five times during each session. After each
swallow, the acquired data were stored. During offline analysis, the
beginning and the end of movement (i.e., velocity is zero at the begin-
ning and at the end of the movement under analysis) were marked in
order to ensure that the curve really did reflect a dry swallow. The time
needed for this procedure took about five minutes and was, therefore,
long enough to enable the patient to gather saliva for the next swallow.
Positive peaks as indicators of irregularities within velocity
curves were counted by two blinded raters for both healthy controls and
patients (Kendall’s tau-b ⳱ 0.937 and 0.975, respectively). The mean
values of the velocity curve characteristics (number of positive peaks,
duration of downward movement, and peak velocity) over the five dry
swallows were chosen for the final assessment of the healthy controls
and the patients (at the time of first and second measurement). At the
end of the rehabilitation program each patient was asked if he/she
needed to concentrate on his/her swallowing.
In six patients laryngeal movements were also measured during
therapy sessions, i.e., when explicitly instructed to perform the Men-
delsohn maneuver volitionally.
M. Prosiegel et al.: Motor Recovery in Swallowing Rehabilitation
Table 1. Characteristics of the 32 patients (mean ± SD)
Men/ Age
women (years) Etiologies
23/9 57.7 ± 16.0 Dorsolateral medullary
(28–87) infarction (n ⳱ 17)
Middle cerebral artery infarction (n ⳱ 8)
left/right: 5/3
Unilateral pontine infarction (n ⳱ 2)
Brainstem encephalitis (n ⳱ 2)
1 postvaccinal (polio)
1 viral of unknown cause
Severe head injury (n ⳱ 2)
Medullary cavernoma (n ⳱ 1)
Fig. 1. Three-dimensional ultrasound movement recording system for
measurement of laryngeal movements. 1 Ultrasound emitting marker
attached to the skin just at the area of the thyroid notch midline. 2 Three
microphones receiving the signals, arranged within a plane at fixed
distances to each other and mounted on a stationary frame (40 × 40 ×
5 cm). 3 PC for movement registration and data storage for later offline
analysis. The distance between the frame and the subject is 1 m.
Statistical Analyses
Three parameters that seemed to characterize the velocity curves best
(number of positive peaks, duration of movement, and peak velocity)
were used for statistical analysis. For purposes of comparison between
the patient and control group, a one-factorial multivariate analysis of
variance (MANOVA) in relation to these parameters was performed
following a log-transformation of the parameter values [y ⳱ log10 (x +
1)] in order to approach the normality and homogeneity conditions of
MANOVA. For comparison of variables between the responders (total
oral feeding) and nonresponders (tube feeding), multivariate analysis of
covariance (MANCOVA), with gender as a covariate, was applied. A
significant group effect was followed by univariate F-tests to identify
those parameters contributing significantly to this effect. A value of a
⳱ 0.05 was accepted as a nominal level of significance and corrected
according to the Bonferroni procedure in order to keep the type I error
< 0.05.
175
Time since onset Feeding at end Duration of
of disease (days) of therapy therapy (days)
96 ± 668 Total oral n ⳱ 22 81.9 ± 76.3
(11–3500) PEG n ⳱ 10 (10–310)
Results
Bell-shaped curves without positive peaks were observed
in 16 controls: one positive peak occurred in 10, two
positive peaks in 4, and three positive peaks in 2. Based
on this information and on the 95% confidence interval
(CI) of the mean number of positive peaks for the con-
trols (95% CI ⳱ 0.88–1.66) and the patients (95% CI ⳱
4.81–8.06), those curves showing more than three posi-
tive peaks may be defined as pathological. Even if few
positive peaks were present, all velocity curves of the
controls were unaltered in terms of their bell-shaped pro-
file that is typical of skilled movements.
When the first measurement was taken, the lar-
ynx movements in 24 of 32 patients with dysphagia
showed irregular (multipeaked) velocity profiles. Table 2
shows characteristics of the velocity curves during
downward movement of the larynx in the patients and
controls. Analysis of variance revealed a significant
group effect [Wilks multivariate test of significance; ef-
fect of group: F(3,50) ⳱ 12.79, sig of F < 0.0001], to
which the number of positive peaks and the duration of
movement contributed significantly (univariate F-tests: p
< 0.05). The peak velocity revealed no difference be-
tween the patients and controls (mean ± SD ⳱ 40.2 ±
26.1 and 43.0 ± 27.4 mm/s, respectively).
When the second measurement was made at dis-
charge, the kinematics of 16 of the 24 patients with hith-
erto pathological velocity profiles were normal and in-
distinguishable from those of healthy individuals.
Twelve of these 16 patients stated that they no longer
needed to concentrate on their swallowing, and 7 of these
12 patients showed a prolonged laryngeal elevation, re-
flecting the “Mendelsohn component” during swallow-
ing, of which they were no longer aware.
The feeding status at the end of therapy was com-
pletely oral in all eight patients who exhibited normal
curves, even before commencing therapy. The eight pa-
tients who had abnormal curves both prior and subse-
176
Table 2. Parameters of velocity curves (mean ± SD and range) obtained by assessment of laryngeal kinematics with a 3D ultrasound movement
recording system in patients with neurogenic dysphagia at the time of admission as well as in healthy controls
Patients (n ⳱ 32)
Number of positive peaks 6.4 ± 4.5
(2–22)
Duration of movement (msec) 846.3 ± 423.3
(250–1850)
a
Univariate F-tests in MANOVA.
quent to therapy were dependent on tube feeding. Of the
16 patients who had pathological curves before and nor-
mal curves after therapy, 14 became completely oral
feeders and 2 remained dependent on tube feeding. There
was no difference between the patients who were depen-
dent on tube feeding (N ⳱ 10) and those who were oral
feeders (N ⳱ 22) with regard to age, duration of therapy,
time since onset of dysphagia, or gender [Wilks multi-
variate test of significance: F(3,22) ⳱ 0.906, p > 0.05].
The etiological groups were too heterogeneous and too
small for statistical analysis. It seems worth mentioning,
however, that of the 22 total oral feeders, the majority
suffered from Wallenberg’s syndrome (N ⳱ 13) or from
unilateral middle cerebral infarction (N ⳱ 6), reflecting
the fact that prognosis is rather good in these diseases.
Within the group of six patients in whom laryn-
geal kinematics were also assessed during the therapy
phase (i.e., while performing the Mendelsohn maneu-
ver), there was no elongated period of laryngeal eleva-
tion in any of them prior to treatment, but it was present
in all six during the therapy phase while volitionally
performing the Mendelsohn maneuver. At the end of
therapy, two of these patients showed an upward move-
ment without prolonged elevation and four patients
showed an upward movement with an elongation, al-
though the latter claimed “to swallow quite normally.”
Figure 2 shows the laryngeal movements of a healthy
individual; Figure 3 shows that in a patient with Wallen-
berg’s syndrome on admission; and Figure 4 shows rep-
resentative curves of a patient before, during, and after
swallowing rehabilitation.
Note that an elongated elevation was not found in
any healthy volunteer.
Discussion
Because of its spatial and temporal resolution, the 3D
ultrasound movement recording system allows assess-
ment of laryngeal movements. For measurement pur-
poses we selected the downward movement because it is
M. Prosiegel et al.: Motor Recovery in Swallowing Rehabilitation
F-value Significance of the
Controls (n ⳱ 32) (df ⳱ 1;52) F-valuea
1.3 ± 0.88 28.06 p < 0.05
(0–3)
336.6 ± 111.4 30.28 p < 0.05
(125–500)
Fig. 2. Laryngeal movements in a healthy individual. Top left Upward
and downward movement (Z axis) of the larynx (the vertical bar indi-
cates the end of the upward and the beginning of the downward move-
ment). Bottom left Corresponding bell-shaped velocity profile during
upward and downward movement of the larynx (at the left and at the
right side of the vertical bar, respectively). Top right Forward and
backward movement (X axis) of the larynx (the vertical bar indicates
the end of the forward and the beginning of the backward movement).
Bottom right Corresponding bell-shaped velocity profile during for-
ward and backward movement of the larynx (at the left and at the right
side of the vertical bar, respectively). Note the different scaling reflect-
ing the smaller range of movement in the X axis.
least susceptible to the effect of the Mendelsohn maneu-
ver, which requires volitional prolongation of upward
and forward movement of the larynx. Furthermore, la-
ryngeal downward movement was suitable for kinematic
analysis since it is not a simple passive return of the
larynx (and hyoid) to the resting position (e.g., mediated
by ligaments), but is caused by activation of infrahyoid
muscles in conjunction with relaxation of the suprahyoid
muscles [13].
In healthy persons the laryngeal movements
showed a smooth and bell-shaped velocity profile typical
of skilled movements. There was a statistically signifi-
cant lower number of positive peaks as well as shorter
movement duration in healthy persons than in the pa-
tients. In contrast, the larynx movements in 24 of 32
patients with dysphagia showed irregular (multipeaked)
velocity profiles. In 16 of these 24 patients, the velocity
M. Prosiegel et al.: Motor Recovery in Swallowing Rehabilitation
Fig. 3. Laryngeal movements in a patient with Wallenberg’s syndrome
on admission (same movement directions but other scaling than in Fig.
2). Top left Upward and downward movements (Z axis) of the larynx
(the left and right vertical bars indicate the end of the upward and the
beginning of the downward movement, respectively). Note the pro-
longed duration of the upward as well as of the downward movement.
Bottom left Corresponding velocity profile during upward and down-
ward movements of the larynx. Note the irregularities during the up-
ward as well as the downward movements. Top right Forward and
backward movements (X axis) of the larynx (the vertical bars indicate
the end of the forward and the beginning of the backward movement,
respectively). Note the same (prolonged) duration of both movement
components as in upward and downward directions (bottom left), but
the smaller range of motion. Bottom right Corresponding velocity
profile during forward and backward movements of the larynx. Note
the irregularities during both movement components, which are, how-
ever, not as pronounced as in the upward and downward directions
(bottom left) with regard to number of positive peaks.
profiles at discharge were indistinguishable from those
of healthy individuals.
Interestingly, these kinematic changes were
closely related to the functional improvement as assessed
by the patients’ feeding status. Patients with kinemati-
cally normal swallowing movements were mostly oral
feeders, whereas those with abnormal velocity profiles
were dependent on tube feeding. Therefore, the results
indicate that kinematic analysis of laryngeal movements
is suitable for distinguishing normal from disturbed
swallowing as well as for monitoring functional recov-
ery.
Since Buchholz et al. [20] were able to demon-
strate that many swallowing deficiencies can be compen-
sated before decompensation occurs, the question arises
whether irregular kinematic profiles might reflect a use-
ful compensatory mechanism. Although there is no de-
finitive answer to this question, in our opinion irregular
velocity profiles are the result of a general motor rule
being broken. At least in the case of swallowing distur-
bances caused by CNS lesions, this might reflect a dys-
function of the medullary pattern generators, which nor-
mally generate the motor control of swallowing sequence
and transmit the timed output to the cranial nerve motor
177
Fig. 4. Laryngeal movements in a patient with Wallenberg’s syndrome.
The left side shows three curves reflecting upward and downward
movement (Z axis) of the larynx (the vertical bar indicates the begin-
ning of the downward movement). The right side shows the corre-
sponding velocity profiles of the downward movement only. A Before
swallowing rehabilitation. B During the rehabilitation phase while per-
forming the Mendelsohn maneuver. C After swallowing rehabilitation.
Note the prolonged duration of the upward and downward movement
(A left) and the irregularities in the velocity curve (downward move-
ment) before rehabilitation (A right). During performance of the Men-
delsohn maneuver the upward movement is markedly prolonged (B
left) and the velocity profile (downward movement) shows irregulari-
ties (B right), which are, however, no longer as pronounced as before
rehabilitation (A right). After rehabilitation the larynx shows a pro-
longed upward movement, reflecting the “Mendelsohn component”
during swallowing, which was no longer consciously noticed by the
patient (C left). The velocity curve of the downward movement shows
a bell-shaped profile typical of skilled movements (C right). The
curves in B and C clearly indicate that use of the upward movement for
kinematic analysis would have produced an artificially irregular veloc-
ity curve as a result of the Mendelsohn maneuver (“disturbing” the
upward movement). Therefore, the downward movement was used for
kinematic analysis in this study.
nuclei, thus guaranteeing a highly overlearned, auto-
mated sequence of swallowing events [21]. The medul-
lary pattern generators are under the control of certain
cortical and subcortical forebrain regions [22,23]. There-
fore, apart from medullary lesions, damage to the cere-
bral cortex or its descending fibers is also likely to lead
to disturbed laryngeal kinematics.
Interestingly, some patients who claimed to be
swallowing the same way they used to before the disease
were not aware of at least partly using the Mendelsohn
maneuver while swallowing. Indeed, the 3D measure-
ment of laryngeal kinematics showed curve profiles typi-
cal of skilled movements but at the same time revealed a
prolonged elevation of the larynx. Thus, some patients
178
make use of the Mendelsohn maneuver so automatically
that they are not really aware of performing this newly
learned technique.
Certain limitations of this study need to be men-
tioned. First, the patient group was not homogeneous and
the control group consisted of healthy persons. We are
currently conducting studies on a more homogeneous
sample of dysphagic patients with respect to etiology as
well as of nondysphagic neurological patients. Prelimi-
nary results show that the velocity profiles of the non-
dysphagic neurological patients do not differ from those
of healthy individuals. Second, the specificity and sen-
sitivity of the method still have to be studied more ex-
tensively, including the measurement of laryngeal up-
ward and forward movement characteristics, which are
strongly expected to be influenced by certain swallowing
techniques. Third, since it cannot be ruled out that subtle
differences in velocity profiles depend on whether the
medullary pattern generators or the cerebral cortex are
affected, further studies with larger patient groups are
needed in order to answer this question. Fourth, on the
basis of our results, it is not possible to give a definitive
answer to the question of whether normalization of hith-
erto abnormal curves reflects only motor recovery or also
motor learning processes, including automaticity of
movements. According to Fitt’s stage theory [5] of skill
learning, during the first (cognitive) stage the basic pro-
cedures to be followed are learned, e.g., by verbal cues
with a considerable amount of attention. The second (as-
sociative) stage represents a transition from conscious
control to more automatic control. In the third (auto-
matic) stage, movements can be performed quickly and
consistently with little conscious involvement and are
characterized by single-peaked, bell-shaped velocity pro-
files. Ongoing studies are examining the swallowing pat-
tern of dysphagic patients while performing parallel (at-
tentional) tasks (i.e., dual task condition). Preliminary
results indicate that normal velocity profiles are posi-
tively correlated with automaticity of swallowing move-
ments as defined above and thus with motor learning
processes. Automaticity of swallowing is especially im-
portant as it can be expected to have positive conse-
quences for the disability and for the handicap level as
defined by the WHO [24]. For example, the patients’
independence of tube feeding and their ability to swallow
either without or with only minor concentration would
make them feel safer when dining out with other people.
Finally, we would like to stress that this study was not
intended to assess the efficacy of swallowing therapy.
Therefore, on the basis of the method we used, no state-
ment can be made as to whether normalization of swal-
lowing movements during swallowing therapy was due
to swallowing therapy or spontaneous recovery or a com-
bination of both.
M. Prosiegel et al.: Motor Recovery in Swallowing Rehabilitation
In summary, kinematic analysis of laryngeal
movements is a suitable method for distinguishing nor-
mal from disturbed swallowing and for monitoring the
degree of motor recovery achieved during swallowing
rehabilitation.
Acknowledgments. The authors wish to thank Anita Wuttge-Hannig,
M.D., and Christian Hannig, M.D., who performed the videofluoro-
scopic examinations.
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