1. Background
It may seem a little odd that work in the fields of speech, hearing
and language should impinge on, and stand to benefit from, a knowledge
of the physiological processes basic to deglutition. The intricately
coordinated mechanisms of voice production are, however, linked
to those of swallowing and there is a potentially useful overlap
of experimental approaches, equipment, and understanding.
1.1 Characteristics of a normal swallow
The act of swallowing is ordinarily described as consisting of
four stages (eg Logemann, 1983):
| oral initial | oral final | pharyngeal | oesophageal |
The first two of these stages are under conscious control. The second two stages are normally autonomic and occur as parts of a complete peristaltic gesture in which food and drink are, as it were, swept from pharynx to stomach. Although the pharyngeal and oesophageal stages have here been given special experimental attention, the following brief overview of all four stages is intended to place them in the context of the complete process (figures based on Logemann, 1983).
2. Phases of a swallow
2.1 Oral initial phase
Figure 1
During the oral initial phase of swallowing, tongue movements differ between subjects; the oral enclosure is, however, relatively consistently defined. Typically a labial seal prevents the escape of liquid from the front of the mouth. Escape of liquid into the pharynx is prevented by a rear oral cavity enclosure produced by the positioning of the velum against the back of the elevated tongue.
2.2 Oral final stage
Figure 2
The oral final stage occurs when the tongue is moved so as to squeeze the bolus or liquid volume against the hard palate so that it is propelled past the anterior faucal arches. It is at this stage that the automatic reflexive gesture of swallowing is triggered. Normally this gives rise to the coordinated peristaltic reflex sequence described below with reference to figures 3 and 4.
2.3 Pharyngeal stage
Figure 3
The triggering of the peristaltic reflex is the beginning of the pharyngeal stage of swallowing. This stage has four main phases:
2.4 Final stage
Figure 4
In the final stage of the swallow, the bolus is transferred in a continuation of the peristaltic gesture from the cricopharyngeal to the gastro-pharyngeal juncture at the entrance to the stomach.
2.5 Aspects of abnormal swallowing
Disorders of swallowing may manifest themselves in a variety of
ways. During the neonatal period, persistently poor feeding,
characterised by weak sucking, and coughing and choking, leading
to prolonged feeding times, are typical signs. There may be associated
respiratory difficulty and even apnoea. Alternatively, difficulties
may emerge when weaning is attempted with the introduction of
spooned solids. Swallowing dysfunction in childhood may also present
more unusually as an isolated weakness in the absence of other
signs and presents in adults as a part of other neurological disorders.
The clinical sequelae of swallowing dysfunction may include repeated "penetration", when food gets between the vocal folds, and "aspiration", when food is inhaled into the tracheal airway. Poor oral intake leads to malnutrition and consequent failure to thrive - adversely affecting the child's growth and development. The results of abnormal swallowing can also lead to recurrent chest infections and the development of chronic lung disease.
Clinically, it is essential that swallowing be monitored in individuals in order to ensure that safe feeding protocols can be established. A number of approaches have been developed to assess swallowing.
3. Methods of monitoring
3.1 Established approaches
All methods depend on at least an initial assessment which involves
taking an appropriate history together with making a clinical
examination. This approach has many advantages but it is not
quantifiable, may not define the precise nature of the trouble
and may not detect silent aspiration - when the client inhales food into the lungs but does not cough
or show discomfort. Complementary methods have been introduced
to reduce these disadvantages. The three most frequently used
methods are listed below in order of relative importance.
3.1.1 Videofluoroscopy
This method makes it feasible to examine both the structure and
function of the organs involved (Ekberg, 1992). Dysphagia can
be identified and silent aspiration detected. Recordings can
be made and used for reference and, if required, measurement.
Its success depends, however, on the swallowing of a controlled
quantity of radio-opaque material, which may be unpleasant, and
exposure to radiation, which must be brief. The method cannot
be used frequently. It may be rather daunting in application
for the child, and it is not a basis for interactive therapy.
3.1.2 Endoscopy
Fibrescopic Endoscopic Examination of Swallowing (FEES: Langmore,
Schatz, & Olsen, 1988) makes use essentially of a nasopharyngolaryngoscope - a flexible endoscope
of the type used in the voice clinic. Although it is an invasive
procedure it is more acceptable for some adult patients and avoids
the gagging associated with rigid oral endoscopy. It also can
be used for biofeedback but it is in essence a cumbersome technique
and not adapted for ready use with children.
3.1.3 Electromyography
EMG (Cooper & Perlman, 1996) recordings are also used and
they confer the advantages of precision in identification and
accuracy of temporal measurement. This method is, however, dependent
to a large extent on signals derived from electrodes inserted
subcutaneously. Whilst EMG is a valuable research tool it is
not well suited to routine clinical investigation.
3.1.4 Cervical Auscultation CA
This method involves the placement of a sensor (originally a stethoscope
was used) on the neck of the subject and either listening and/or
recording the acoustic signals which are produced from a microphone
as by-products of the swallowing processes. These signals are
typically visually presented and examined as waveforms or spectrograms.
The first work using these signals led to the description by
Bosma and his colleagues of the normal swallow as being associated
with two discrete and perceptually distinct sounds - the "Initial Discrete Sound"
(IDS) and the "Final
Discrete Sound" (FDS)
(Bosma 1992; Heinz et al 1994). Many other investigators have
explored the use of this approach for the examination of dysphagia.
A variety of sensors have been employed in attempts to define
an optimal configuration but the best choice of sensor, or of
sensor combination, is still not clear.
3.2 Other sensors
The essential advantage of the CA method is that it provides useful
information in a rapid and simple non-invasive fashion. Its essential
disadvantage is that the auditory/acoustic information that it
provides is not readily linked to particular physiological sources
and is often not very clear physically. Data are generated not
as a direct result of the processes of swallowing but rather as
an adventitious side product. It is the intrinsic and relative
movements of the organs associated with deglutition that are important
in the understanding of normality and the detection of pathology.
Following Bosma's initial lead, auditory CA has, nevertheless,
made a substantial contribution to the clinical detection and
management of swallowing problems and this has led to the investigation
of the possible use of other sensors in place of the microphone.
3.2.1 Ear Probe
This sensor has been shown to respond to the "intrinsic
sounds of swallowing". An advantage of the ear probe is its site of placement.
Whilst scars and skin changes post-radiation can make neck mounting
of a sensor difficult (poor mounting can lead to extraneous noise
in the signal) no such difficulties are encountered with the ear
probe. This sensor also has the advantage that it may be more
acceptable for children than the more standard techniques (and
it might be useful for biofeedback).
3.2.2 Accelerometer
The accelerometer is a neck mounted sensor which is held in place
by a lightly adhesive strip. It has a wide frequency response
range and can be obtained in miniature unobtrusive formats. It
is vibrated by the "epidermal
vibrations caused by internal sounds and vibrations reaching the
surface where it is attached"
(Kuhn, 1995), i.e. it responds to the movements of internal organs.
The acoustic information the accelerometer provides, whist not
'sounding'
like a swallow mediated by CA, appears closely related to the
discrete swallow sounds detected on the neck by a stethoscope
or a microphone.
3.2.3 Electrolaryngograph
The time constants used in the design of the normal laryngograph
were chosen to give useful responses to impedance changes associated
with vocal fold vibration. Any neck impedance change between
the electrodes will, however, have an effect on the Lx signal
output as a function of the magnitude and rapidity of the change.
Swallowing has an effect which is greater or less directly as
a function of these internal time constants. In the limit it
is possible to arrange for a response down to zero frequency (Gx
setting). It has previously been suggested within the dysphagia
literature (Sorin, McClean, Ezerzer & Meissner-Fishbein, 1985;
Perlman & Grayhack, 1991) that including an electroglottograph
as a sensor in swallowing studies may be of benefit to clinical
work. Perlman earlier (personal communication) attempted to convert
a standard Laryngograph in her own laboratory so as to obtain
Gx for swallowing studies. The results were not encouraging and
this possibility is revisited later in the present description.
The output of an environmental microphone was also included in the set of recorded data. It was used to register the name of the subject, the condition of the test, and also to provide clear information regarding the moment when the pharyngeal stage of the swallow was initiated on a separate monitor channel. This ensured that no 'dry' swallows, coughs or vocalisations were included within this study accidentally.
3.3 Outstanding problems in sensor selection
Although the use each of these sensors has been investigated in
many separate swallowing studies no clear best choice has as yet
emerged. One major difficulty arises from the lack of a basis
for rigorous cross comparison. This is only feasible when sensors
are used simultaneously to monitor the same swallow and when each
of a representative group of subjects undertakes the same swallowing
task. Two further difficulties will then remain. The first is
to arrive at a videofluorographic calibration of the best sensor
or sensor combination. The next arises, in the present context,
from the need to have a system which is readily applicable with
children.
4. Experimental aims and procedures
The present work was necessarily limited in scope and the main
part of the investigation was designed only to provide information
directly relating to the optimal choice of sensor. This led to
the definition of two primary objectives.
4.1 Objectives
4.1.1 Which sensor provides the most accurate, consistent
and reliable basis for the identification of the characteristics
of a 'normal' swallow?
And, as a closely allied aim:
4.1.2 Using this approach, what are the main characteristics of the 'normal' swallow?
4.2 Sensors used
Each of the four sensors described above was included in the study
using techniques which had already been proved in related applications.
4.2.1 The ear probe (EM 3046)
The ear probe was provided by courtesy of Otodynamics. This
is a standard audiological wide band acoustic receiver ordinarily
used for the detection of otoacoustic emissions in a combined
transmitter and receiver housing. Otodynamics also provided the
range of ear plugs needed for adaptation to individual subjects.
4.2.2 The accelerometer (BU 1771)
The accelerometer was obtained from Laryngograph Ltd. It was
used together with a processing circuit originally designed for
the detection of nasal wall vibration as part of a system for
the display and measurement of nasality in speech.
4.2.3 The Laryngograph
The Laryngograph used in the main investigation was typical of
the current range employed in voice clinics and had a "normal
Lx" time constant In order to provide background information
concerning the use of the laryngograph, a small amount of swallowing
data was also obtained using a Gx, zero frequency coverage, laryngograph.
Although true Gx requires a care in adjustment, which makes it
difficult to apply in a clinical environment, it can be helpful
in the interpretation of the Lx waveform itself.
4.2.4 Neck mounted microphone (EK3132)
The fourth sensor was a miniature neck mounted microphone (EK3132)
of the type used for free field speech recordings. This followed
the tradition of CA itself without, however, using a stethoscope
coupling.
4.2.5 Audio microphone
During the data gathering a fifth sensor, provided by a standard
audio microphone, was used to monitor the experimental sequences.
4.3 Subjects and sensor placement
Twenty normal young adult volunteers, 7 men and 13 women, with
no history of dysphagia took part in the tests. Each subject
was seated and requested to swallow 20 ml of water on three separate
occasions. On each occasion the subjects held the liquid in their
mouths until a signal was given for them to swallow. This procedure
was followed in an attempt to ensure that a common initial swallowing
starting point was obtained for all observations.
Figure 5 Sensor Placement
The placement of the sensors was consistent for all subjects and resulted from reference to prior work (Takahashi, Groher & Michi, 1994; Reddy, Gupte, Green and Camilang, 1994; Hamlet, S., Penney, D.G. & Formolo, J. (1994)) and our own initial exploratory experiments.
4.4 Signal acquisition assessment and evaluation
The outputs from the four main sensors plus the monitoring microphone
were saved simultaneously for each swallow on an ADAT recorder
(an eight channel digital audio recorder using special VHS tape
to give standard 16 bit CD audio quality for each channel). Subsequent
display and analysis of the data was based on the use of the Laryngograph
Ltd SPG program.
Figure 6 Sensor outputs for a typical swallow
The four signal presentations shown in this figure are those used for the measurements reported here. Whereas 200 Hz analysis bandwidth spectrogams were used for the two microphone based sensors, ear probe at the top (1) and neck microphone (3), the raw waveforms are shown for the accelerometer (2) and laryngograph (4) signals. These modes of presentation were chosen heuristically simply to obtain the clearest bases for interpretation - further work is quite likely to lead to more sensitive techniques.
The data obtained for the sixty individual swallows from these
normal subjects were very consistent both within and between subjects.
This made it feasible to assess the outputs from each of the sensors
on the basis of a simple rating protocol based on the application
of subjective visual criteria.
| Poor | No change in signal, and therefore no indication of the presence of the precursor, IDS, FDS or end of swallow.
Rating = 0 |
| Variable | During some swallows there were indications of the presence of the precursor, IDS, FDS or end but this was unreliable
Rating = 0 |
| Good | Reliable indication of different aspects of swallow, but needs confirmation from another sensor
Rating = 1 |
| Very Good | Sensor which accurately indicates the presence of different aspects of each swallow and does not require another sensor to confirm this.
Rating = 2 |
4.5 Table 1 Rating Protocol
The criteria defined in Table 1 were applied for the family of
outputs from each subject, rather than for each separate sensor
type. This approach was chosen since it gave a practical clinically
relevant coherence to the overall appraisal.
Quantitative measurements were made on the combined plots of the form shown in Figure 6. Each swallow was treated separately and its data used in combination to get the best estimates of the three main temporal intervals shown - precursor to IDS; IDS to FDS and FDS to end of swallow.
5. Experimental results
5.1 Sensor output comparisons
When the results of applying the protocol of Table 1 to every
one of the sixty sets of individual swallow data were collated
the rather unexpectedly clear set of overall rating comparisons
shown in figure 7 emerged.
Figure 7 Sensor Rating Comparisons
The electrolaryngograph and accelerometer outputs were both distinctly
more useful in identifying three of each of the four main swallowing
events than either of the other two sensors. The exception was
in respect of the precursor. The beginning of a swallow was better
identified, from these data, when outputs from either the ear
probe or the neck microphone were used than when the accelerometer
was employed. On a single sensor basis, the Lx signal from the
electrolaryngograph was the most reliable source of information
for each main temporal event. The visual appraisal of these two
sources of information in combination produced an improvement
in detection score for the end of the swallow from 67% for the
laryngograph alone to 80% in combination with the accelerometer.
There was a reduction, however, from 70%, using the Lx signal
alone for the identification of the precursor to 50% when both
signals were used in combination.
5.2 Subject differences
Figure 8 Individual Subject Mean Swallow Durations
| Mean (ms) | Male
(n = 7) | Female
(n = 13) | p level* |
| Total duration | 956.33 ms | 880.62 ms | 0.08 |
| Precursor to IDS | 112.34 ms | 151.44 ms | 0.10 |
| IDS to FDS | 701.78 ms | 585.69 ms | 0.00 ** |
| FDS to end of swallow | 142.23 ms | 143.47 ms | 0.96 |
* independent samples t-test (2-tailed)
Table 2 Mean Swallow durations for male and female subjects
When an independent samples t-test was applied to the four sets of temporal intervals taken for each swallow for each subject the only significant difference between male and female subjects was for the IDS to FDS interval (see also Figure 7 in regard to the dominance of these individual events).
6. Discussion
Qualitatively, on the basis of the present observations, the electrolaryngograph
has provided the most consistent and reliable indications relating
to the main swallow events which have been established by prior
work in the field of Cervical Ausculation. Quantitatively, the
timing characteristics, which have been measured here, correspond
to those found using other indirect methods of observation. Absolute,
as opposed to relative, accuracy, however, can only be established
with simultaneous use of videofluorography and this has not been
done in this necessarily limited study, although the present results
certainly make this extension worthwhile.
The second most useful sensor found in this study was the accelerometer and it appears that there could be a slight advantage in the combination of the outputs from the two sensors. A further significant advantage could come from the simultaneous use of more than one set of electrolaryngograph electrodes. Perhaps a specially significant aspect of this result, however, is that both of the best sensors respond directly to internal organ movement as opposed to the acoustic by-products of movement. This may prove to be an essential indicator in regard to the best way forward in respect of the choice and future development of non-invasive means for the monitoring and measurement of swallowing. Finally, the use of biofeedback could be another fruitful result of introducing speech-based techniques into the management of dysphagia by the provision of clear real-time visual and or auditory displays of abnormal and normal function.
Acknowledgement
We would like to thank Mahen Goonewardane and David Cushing for
their technical support. This work was done partly with the help
of funding from the North West Thames Health Authority.
References
Allaire, J.H., Riordan, B. & Gillies, G.T. (1994) A Swallowing
Frequency Device. Presented at the Second Workshop on Cervical
Auscultation, Ritz Carlton Hotel, Tyson's Corner, VA, October
13, 1994
Bosma, J. (1992) Introduction to the Cervical Auscultation Workshop, Department of Paediatrics, University of Maryland, Baltimore, Maryland, April 22, 1992
Cooper D.S., & Perlman, A.L. (1996) Electromyography in the Functional and Diagnostic Testing of Deglutition In Deglutition and its Disorders pp255-285; Singular London UK
Ekberg, O. (1992) Radiographic Evaluation of Swallowing. In Dysphagia: Diagnosis & Management (2nd edition) ed Groher, M.E. Butterworth Heinemann, USA
Hamlet, S. (1992) Auscultation of Feeding Sounds at the Ear. Presented at the Cervical Auscultation Workshop, Department of Paediatrics, University of Maryland, Baltimore, Maryland, April 22, 1992
Hamlet, S., Penney, D.G. & Formolo, J. (1994) Stethoscope Acoustics and Cervical Auscultation of Swallowing. Dysphagia 9 : 63 - 68
Heinz, J.M., Vice, F.L. & Bosma, J.F. (1994) Components of Swallow Sounds. Presented at the Second Workshop on Cervical Auscultation, Ritz Carlton Hotel, Tyson's Corner, VA, October 13, 1994
Kenny, D., McPherson, K., Kasis, M. &Judd, P. (1992) Possible Applications of Cervical Auscultation in Observations of Swallow: Respiration Interaction in Dysphagic Children. Presented at the Cervical Auscultation Workshop, Department of Paediatrics, University of Maryland, Baltimore, Maryland, April 22, 1992
Kuhn, P.M. (1995) A Review of sensing Devices for Cervical Auscultation. Presented at the Year in Cervical Auscultation, Tyson's Corner, McLean Virginia, October 26, 1995
Langmore, S.E., Schatz, K. & Olsen, N. (1988) Fiberoptic endoscopic examination of swallowing safety: A new procedure Dysphagia,2, 216-219
Logemann, J.A. (1983) Evaluation and Treatment of Swallowing Disorders. College-Hill Press
Morrell, R.M. (1992) Neurological Disorders of Swallowing. In Dysphagia: Diagnosis and Management (2nd ed) Eds Groher, M.E. Butterworth-Heinemann, USA
Perlman, A.L. & Grayhack, J.P. (1991) Uses of Electroglottograph for Measurement of Temporal Aspects of the Swallow: Preliminary Observations. Dysphagia 6 : 88 - 93
Reddy, N.P., Gupta, V., Prahbu, D.N.F., Green, P., and Canilang, E.P. (1994) Aceleration Measurments During Swallowing & Coughing. Second Workshop on Cervical Ausculation VA October 13, 1994
Sorin,R., McClean, M.D., Ezerzer, F., & Meissner-Fishbein, B. (1985) Electroglottographic evaluation of the swallow. Archives of Physical Medicine and Rehabilitation
Takahashi, Groher & Michi, (1994) Methodology for Detecting Swallowing Sounds Dysphagia 9; 54-62
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