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1181

Altered Swallowing
Function
in
Elderly Patients
Without
Dysphagia:
Radiologic Findings in 56
Cases

..

Olle Ekberg12
J. Feinberg3

Michael

Swallowing
disorder is an increasing
problem in our aging population.
A majority of
these patients have a functional
abnormality
of the oral, pharyngeal,
and/or esophageal
stage of swallowing.
However,
what constitutes
normalcy
is not well understood,
and
baseline
swallowing
in elderly
persons
without dysphagia
has not been adequately
described.
We therefore
evaluated
56 persons with a mean age of 83 years who had no
symptoms
of dysphagia
or eating difficulty. Videofluoroscopy
and radiographs
with the
subject erect and recumbent
were obtained.
Normal deglutition,
as defined
in young
persons,
was present in only 16%. Oral abnormalities
(difficulty
ingesting,
controlling,
and delivering
bolus relative to swallowing
initiation)
were seen in 63%. Pharyngeal
dysfunction
(bolus retention
and lingual propulsion
or pharyngeal
constrictor
paresis)

was seen in 25%. Pharyngoesophageal

(mostly cricopharyngeal
in nature) were observed

segment

muscle dysfunction).
in 36%.

What has been described

as swallowing

abnormalities

Esophageal

dysfunction

Received
October
1 5, 1990; accepted
after revision December
31, 1990.
1 Department
of Radiology,
Hospital
of the University of Pennsylvania,
phia, PA 19104.
2
address:
MalmO
Address

3400

Spruce

Department

of

Hospital,

S-21401

MalmO,

reprint

requests

to 0. Ekberg.

Radiology,

motor

may not be

of normal

aging

June 1991

Swallowing
impairment
increases
in prevalence
with advancing
age and is a
major health care problem
in the aged [1-5].
Dynamic
imaging
has become
an
important
part of the diagnostic
workup of elderly patients with signs or symptoms
of deglutition
problems.
The oral, pharyngeal,
and esophageal
stages are not as
efficient
or synchronous
in these persons.
However,
it is not always clear when
the observed
alterations
represent
pathologic
changes
or are caused by the aging
process itself. Developing
criteria of normalcy for such a complex function is difficult
even in younger
populations.
Previous
studies
[6, 7] of pharyngeal
function
in
asymptomatic
persons
have demonstrated
considerable
variation
in morphodynamics.
Recently,
small cross-sectional
investigations
of normal oropharyngeal
function have documented
changes
in the duration of bolus movement
and various
other events
that are related
to aging [8-1 0]. To our knowledge
no studies
examining
the prevalence
of functional
alterations
that are commonly
considered
abnormal
in the very aged have been done. The purpose
of our work was to
examine
deglutition
in an asymptomatic
elderly population.

Materials

and

Methods

Sweden.

of Radiology,
Albert Einstein MedYork and Tabor Ads., Philadelphia,
PA

0361-803X/91/1
566-1181
American Roentgen Ray Society

the effect
changes.

in 39%

St., Philadel-

General

ical Center,
19141.

156:1181-1184,

(mostly

in young persons

abnormal
in very elderly persons.
It is difficult to distinguish
from the effects of specific diseases
or gradual degenerative
AJR

were observed

abnormalities

Patients
to

who were referred

participate.

examination,
fluoroscopy

During

the

for examination
routine

upright

of the upper
ingestion

the ingestion,
oral cavity,
pharynx,
and video (VHS), in lateral and frontal

the esophagus

The patients

with

were

the

patient

asked

prone

of

gastrointestinal
liquid

barium

tract
for

were asked

double-contrast

and esophagus
were examined
during
projection,
as well as oblique projection
of

or supine.

to take a mouthful

of barium

from

a cup and then

hold it in the

I1
.

1182

EKBERG

mouth

to test

not

controlled

tion.

They

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swallows
centered
centered

for

adequacy

of containment.

or registered
were

then

but

asked

was

that

The
of the

to swallow

on

volume

patients

taken
own

command.

AND

At

was
discre-

least

two

in lateral projection
centered
over the oral cavity and two
over the pharynx were imaged. An additional
two swallows
over the mouth and pharynx
in frontal
projection
were

imaged.

In an erect

position,

the patient

also

was

given

one

teaspoon

of barium paste, which was monitored

in lateral projection,
following
the paste from ingestion
until it reached
the stomach.
Oral and
pharyngeal
function was assessed
only in an erect position and not
recumbent.
The esophagus
was then examined
with the patient erect.
The barium used was EZ-HD, with a barium content of 250% w/v.
When deemed
necessary,
the esophagus
was examined
with the
patient

recumbent

also,

with

a SOC/a w/v

barium

suspension.

This

triphasic examination
was attempted
in all nonaspirators.
A total of 56 patients were included. They denied any prior or
present difficulties
with swallowing.
Caregivers
accompanying
some
patients

confirmed

the

presence

of a normal

swallowing

behavior.

There were 22 men and 34 women ranging in age from 72 to 93

years (mean, 83 years). Of the patients, 3i had no history of neurologic disease known to impair swallowing.
The rest of the patients

(25 persons)

had such a history,

Parkinson
disease
three patients.

in seven

namely dementia

patients,

in 15 patients,

and cerebrovascular

disease

in

Results

The results are summarized

in Table 1 . A synchronous
and
symmetric
swallowing
function
without
morphodynamic
abnormalities
was seen in only nine patients
(1 6%). Few strucTABLE
1: Swallowing
Dysphagia

Function

in 56 Elderly

Persons

Function

Normal function
Oral, pharyngeal,

esophageal
Misdirected

Without

No.

pharyngoesophageal

segment,

and

(%)

9 (i 6)

function

swallowing

In subepiglottic
segment of laryngeal vestibule
Minor into supraglottic
segment of laryngeal vestibule
or trachea
Oral dysfunction
Sensorimotor
incoordination
Too large or rapid ingestion
Leak

i 1 (20)
25 (45)

Dissociation
Pharyngeal
dysfunction

20 (36)

Defective closure of laryngeal vestibule

Retention
Defective oropharyngeal
propulsion
Defective down tilt of epiglottis
Constrictor
paresis
Pharyngoesophageal

Defective

segment

9 (i 6)
8 (14)
7(i3)

3 (5)
1 i (20)
6 (ii)
4 (7)
5 (9)

dysfunction

opening

13 (23)

Early closure (only)

Web
Killian-Jamieson
diverticuluma

4
3
2

Zenker diverticulum

1 (2)

Esophageal
Dysfunction
Esophagitis
a

This

laterally

diverticulum
[11].

(7)
(5)
(4)

20 (36)

3 (5)
protrudes

inferior

to the

cricopharyngeal

muscle

and

FEINBERG

AJR:156,

June 1991

tural or morphodynamic
abnormalities
were seen; these included webs, rings, diverticula,
esophagitis,
and hiatal hernia.
The most common
dysfunction
was found in the oral stage
of swallowing.
The oral stage is voluntarily
controlled,
although it is largely automatic.
Incoordination
of sensorimotor
behavior refers to the bolus being held in an abnormal
position
or processed
for a considerable
time before
swallowing.
Ingestion
of too big a bolus or ingestion
that was too rapid
was common.
The structure
and function
of the oral cavity in
these elderly persons
are not sufficient
for what they put in
their mouths.
This may also explain why a high frequency
of
dissociation
between
the oral and pharyngeal
stages
was
found. Muscular
weakness
or impaired
afferent
information
caused leakage of barium from the oral cavity over the back
of the tongue in seven patients.
Altered function
in the pharyngoesophageal
segment
was
most frequently
seen as defective
opening at the level of the
cricopharyngeal
muscle.
Other abnormalities
in the pharyngoesophageal
segment
were morphodynamic,
such as webs
and diverticula.
Webs were moderate
in depth and seen only
during maximal
distension
of the pharyngo-esophageal
segment. They caused no retention
of barium craniad to them.
Interestingly,
diverticula
of Killian-Jamieson
type were more
common
than those of Zenker type.
Patients
with a history
of neurologic
disease
known
to
impair swallowing
had a higher frequency
of dysfunctions
than did patients
with no such history. This was particularly
true for oral sensorimotor
incoordination
(32% vs 3%), dissociation
between
the oral and pharyngeal
stages (48% vs
26%, Fig 1), and constrictor
paresis (20% vs 0%).
Of 36 patients
(64%) who had misdirected
swallowing,
16
(44%)
had oral dysfunction
only, four (1 1 %) had pharyngeal
dysfunction
only, and eight (22%) had both oral and pharyngeal dysfunction.
Esophageal
dysfunction
was present in 20 patients
(36%).
Twelve
patients
had hiatal hernia, and three of these had
esophagitis
due to gastroesophageal
reflux as well.

Discussion
Swallowing
in younger persons without dysphagia
has been
shown to be symmetric
and synchronous
[6, 7]. Compared
with an earlier study [6] that addressed
swallowing
in asymptomatic younger persons (mean age, 52 years), we found that
elderly persons had a much higher frequency
of abnormalities.
The frequency
of normal function
in that series of younger
persons
was about 20% and is of the same magnitude
as
that observed
in a prior study of dysphagic
patients
that
included patients over the age of 75 years. This circumstance
may indicate
that there is a subpopulation
of patients
who
have a more stable swallowing
function
then the rest have.
In the nondysphagic
population,
they may represent
those
with a true normalcy,
whereas
in the dysphagic
population,
they may have dysphagia
for other reasons,
and the reason
is not revealed
during the radiologic
study. Selection
of patients may be biased in that they already were scheduled
for
a barium examination
of the upper gastrointestinal
tract. Our

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AJA:156, June 1991

ALTERED

SWALLOWING

IN ELDERLY

1183

PATIENTS

Fig. 1.-A-F,
Sequence from a videoradiographic
examination
of barium swallow in an elderly patient without dysphagia. Barium flows over back of
tongue into valleculae (A). Barium also reaches into subepiglottic segment of laryngeal vestibule (B) and further down into supraglothc segment (C). A 3sec delay occurs before pharyngeal swallow is elicited (D). Barium is squirted infenorly beyond vocal cords into trachea (E). After swallowing, no barium
is retained in pharynx (F). Misdirection
of barium was solely due to dissociation
of oral and pharyngeal
stages of swallowing.
lt is not clear whether
this
is due to afterent or efferent deficit or a central-processing
impairment.

inclusion
criteria were the same as we used before [6], but
were not as rigorous
as those of Curtis et al. [7].
The effect of aging on response
programming
has been
shown to imply an increase
in reaction
time, especially
with
increasing
complexity
of the movements;
that is, older people
require progressively
more time to react after interpretation
of afferent
information
[1 2]. Any afferent
stimulus
needs to
be coded and identified
and the appropriate
response
determined. Older persons
require more time for processing
the
signal. However,
older persons
are not different
in the processing of complex
movement,
but simply slower [13].
It has been shown that muscle strength
declines
with age
[1 4]. This is primarily
related to a decline in muscle mass but
also to a change
in morphology
and biochemistry,
that is,
alteration
of muscle fiber composition
with decrease
in size
of fast-twitch
fibers (type 2) [1 5]. However,
the number
of
functioning
muscle motor units declines
with age [1 6]. The
remaining
motor units are enlarged
and tend to have fewer
fast-twitch
fibers. These enlarged
motor units partially main-

tam muscle
mass, even when strength
deteriorates.
The
pressure created between
the tongue and the palate also has
been shown to decrease
with age [9]. Oral transit time also
decreases
with age [1 0]. To such neuromotor
impairment
is
added the decrease
in chemosensory
perception
with age
that diminishes
the senses of taste and smell [17].
Altered function
in the pharyngoesophageal
segment
was
six times as common
in older persons as in younger
asymptomatic subjects
[6]. A prior study also has shown a decrease
in time of opening
of the pharyngoesophageal
segment
with
age [8]. Moreover,
compliance
of the pharyngoesophageal
segment
diminishes
with age and is seen as decreased
maximal opening
[1 0]. In two prior studies of patients
with dysphagia, the close correlation
between
age and cricopharyngeal dysfunction
was pointed out [1 1 8]. A close relationship
also exists between such incoordination
and other swallowing
dysfunctions
[1 9]. The underlying
pathophysiology
is not well
understood.
However,
a high frequency
of fibrosis was found
in a histopathologic
study [20]. In patients
with a visible
,

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1184

EKBERG

AND

cricopharyngeus
during the whole span of swallowing,
fibrosis
is likely, whereas
a neuromotor
dysfunction
is seen as a
transient
indentation.
Such dysfunction
also is likely to account for defective
closure between
swallows.
Only two prior studies seem to have approached
the changing function
of the esophagus
in very old persons.
In one of
these studies,
dysfunction
(i.e., absent
or weak peristalsis
and tertiary peristalsis)
was prevalent
[21 ]. In another study,
however,
disordered
motility
was regularly
associated
with
disease
[22]. The prevalence
of motor
dysfunction
in our
study may indicate that these persons in fact have subclinical
disease.
The observed
aberrations
may be explained
merely by the
test situation.
Many patients
complain
about the taste and
consistency
of the barium suspension.
Also, the unfamiliar
environment
in the radiography
suite may add to a stressful
situation.
A highly standardized
technique
must be used to
position
the patient.
Alignment
and slight extension
of the
neck may induce decompensation.
However,
every effort was
made to keep the patient as comfortable
as possible
during
the test.
The altered function observed
may be due to normal aging
(primary
aging).
However,
we do not know
if our study
population
suffered
from subclinical
disease, or disease in an
early stage, such as neuromuscular
disease (secondary
aging). Such disease
might affect afferent
or efferent
control
and include central dissociation.
This is a likely explanation
in
the patients
with different
types of neurologic
disease.
The
degenerative
changes
may already
have involved
areas of
importance
for swallowing,
even though
the patients
were
asymptomatic.
However,
some of the patients
did not have
any disease
known to potentially
involve swallowing.
Such
neurologic
disease
might involve the CNS as, for example,
gray and white matter disease
does. Neuropathy,
such as
that seen in diabetes
and alcoholism,
also may be subclinical
but still have importance
for oral and pharyngeal
function.
Our conclusion
is, therefore,
that nondysphagic
elderly
persons have altered function
without
impairment.
The most
common
problem
is oral sensorimotor
incoordination.
However, the gaps in our knowledge
of the true cause of dysphagia and swallowing
dysfunction
do not invalidate
the observations
made during radiologic
evaluation
of barium swallowing.
These facts also make assessment
of dysphagic
elderly persons
difficult,
because
the distinction
between
altered function
due to normal aging and altered function
due
to disease is not clear. However,
misdirection
of barium into

FEINBERG

AJA:156,

the airways
was always minor
sons. Therefore,
major aspiration
and not to be a result of normal

June

1991

in asymptomatic
elderly peris likely to be due to disease
aging.

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