Content uploaded by Salil Singh
Author content
All content in this area was uploaded by Salil Singh on Feb 09, 2014
Content may be subject to copyright.
REVIEW
Dysphagia in stroke patients
S Singh, S Hamdy
...............................................................................................................................
Postgrad Med J 2006;82:383–391. doi: 10.1136/pgmj.2005.043281
Swallowing musculature is asymmetrically represented in
both motor cortices. Stroke affecting the hemisphere with
the dominant swallowing projection results in dysphagia
and clinical recovery has been correlated with
compensatory changes in the previously non-dominant,
unaffected hemisphere. This asymmetric bilaterality may
explain why up to half of stroke patients are dysphagic and
why many will regain a safe swallow over a comparatively
short period. Despite this propensity for recovery,
dysphagia carries a sevenfold increased risk of aspiration
pneumonia and is an independent predictor of mortality.
The identification, clinical course, pathophysiology, and
treatment of dysphagia after stroke are discussed in this
review.
...........................................................................
See end of article for
authors’ affiliations
.......................
Correspondence to:
Dr S Hamdy, Department
of GI Sciences, Hope
Hospital, Stott Lane,
Manchester M6 8HD,
UK; shaheen.hamdy@
manchester.ac.uk
Submitted
11 November 2005
Accepted9December2005
.......................
B
efore discussing the clinical aspects of
dysphagia after stroke it is worth consider-
ing what exactly is meant by the term
dysphagia. In the context of stroke, oropharyn-
geal dysphagia is probably best defined as a
disruption of bolus flow through the mouth and
pharynx. As the function of swallowing is the
safe delivery of a food bolus into the stomach,
then the immediate complication of dysphagia is
food entering the airway. Dysphagia in this
context is not a subjective symptom and it does
not normally refer to any oesophageal abnorm-
ality.
A related but distinct term is aspiration, which
is the incursion of food material into the airway
and below the true vocal cords. Aspiration is thus
one of the most important consequences of
dysphagia along with malnutrition.
HOW COMMON IS DYSPHAGIA AFTER
STROKE?
Numerous studies have tried to establish the
incidence of dysphagia after stroke with figures
ranging from 23% to 50%.
1–11
At first glance,
these figures seem to represent a wide range. The
explanation for this lies in variations in study
design and in the identification of dysphagia,
both of which merit further discussion.
STUDY DESIGNS
Only a handful of studies have looked at sample
sizes greater than 100 and differences in reported
entry criteria for these studies have resulted in a
variable case mix. Studies are started at different
time points, which means a variable amount of
recovery will have taken place at the time of
assessment. Stroke severity may not be assessed
and comorbidity such as chronic obstructive
pulmonary disease may not be accounted for.
All these factors make it difficult to pool or
compare data. In addition, there are discrepan-
cies between different authors’ methods of
identifying dysphagia.
IDENTIFICATION OF DYSPHAGIA
Swallowing assessments are generally split into
bedside clinical examinations or instrumental
investigations. Because each approach provides
differing data with variable accuracy, the inci-
dence of dysphagia can fluctuate depending on
which assessment is used.
Bedside examination remains the cornerstone
of clinical practice in most hospitals. Clinicians,
nurses, and speech and language therapists are
taught to present small volumes of food or water
to patients and to watch for signs of dysphagia
and aspiration. Among other signs, clinicians
will look for loss of liquid from the mouth,
dyspraxia or poor coordination of muscles, facial
weakness, delayed pharyngeal/laryngeal eleva-
tion, coughing or throat clearing, breathlessness,
and changes in voice quality after swallow.
12
It
should be noted that the interpretation of an
intact gag reflex as an indicator of safe swallow-
ing has been largely discredited.
13
There are other
factors taken into account including some that
are not directly related to the stroke such as
background respiratory function. Patients with
advanced chronic lung diseases may aspirate not
because of a neuromuscular problem but because
they cannot maintain a sufficient period of
apnoea while swallowing. Despite the broad
assessments undertaken at the bedside, the
problem with this method is that it relies on
findings that are subjective and clinician depen-
dent.
Several investigators have tried to create
objective and reliable scoring systems for the
bedside assessment. Inevitably, as with most
screening systems, if the sensitivity of the scale is
improved, its specificity declines when compared
with the current gold standard; videofluoroscopy
(VFS) (see table 1). An important factor in the
low sensitivity of the bedside examination is
patients who aspirate without clinically overt
signs, known as silent aspirators. As many as
half of all patients aspirating on VFS will do so
silently.
14–17
In addition, patients will commonly
show varying responses to aspiration during a
single VFS assessment.
Abbreviations: VFS, videofluoroscopy; FEES, fibreoptic
endoscopic evaluation of swallowing; PEG, precutaneous
endoscopic gastrostomy; TMS, transcranial magnetic
stimulation; EMG, electromyography; NG, nasogastric
383
www.postgradmedj.com
VIDEOFLUOROSCOPY
Also known as a modified barium swallow, VFS has
traditionally been the gold standard for swallowing assess-
ments.
25
It entails the administration of radio-opaque barium
liquid with moving images captured in the lateral view.
Figure 1 shows a VFS image outlining the anatomy of the
oropharynx and figure 2 illustrates the flow of barium
through the oropharynx. Occasionally anterior-posterior
views are also obtained. The barium can be mixed with
water to varying consistencies or added to other foods.
VFS has the advantages of visualisation and quantification
of barium through the oral cavity as well as the pharynx and
oesophagus. It can be recorded and played back in slow
motion and differentiates between abnormal physiology,
penetration of barium into the airway, and true aspiration
(barium entering the airway below the true vocal cords).
Most hospitals will have fluoroscopy services on site and an
assessment often takes just 10 or 15 minutes. Most examina-
tions are undertaken with the aim of establishing which
consistencies would be safe for a patient to consume and
which posture or manoeuvre might aid safe swallowing.
Disadvantages of VFS include the exposure to radiation
albeit low dose. The procedure is carried out under ‘‘ideal’’
conditions that may not reflect events on the ward. Barium’s
density is significantly different to normal food and therefore
its passage may not indicate the aspiration risk with other
foods. There is no standard protocol for the volumes tested or
the consistencies delivered and it only judges a person’s
performance on one day. As with the bedside examination, it
is remarkably open to interpretation with an interrater
reliability (k values) for aspiration of between 0.4 and
0.8.
6182627
However, this correlation is improved with
training and experience.
228
FIBREOPTIC ENDOSCOPIC EVALUATION OF
SWALLOWING
In the past 20 years an alternative to VFS has been developed.
Fibreoptic endoscopic evaluation of swallowing (FEES) was
first reported in 1988
29
and entails the placement of a
nasendoscope to the level of the uvula or soft palate to give a
view of the hypopharynx and larynx (see fig 3). It has an
excellent safety record with epistaxis being seen in less than 1
in 1000 patients.
30
Various foods can be tested and it does not
entail radiation. It permits anatomical assessment as well as
sensory testing and crucially, it is performed at the bedside
with normal meals and can be repeated as often as necessary.
On the other hand FEES does require a skilled operator and
technical equipment that is not widely available. No
information is gained about the oral phase of swallowing
and there is a white out as the bolus passes through the
pharynx and the pharyngeal constrictors contract around the
lens. There also remains some controversy as to whether local
anaesthetic sprayed into the nostril affects swallowing
physiology or not. Table 2 shows the advantages and
disadvantages of VFS compared with FEES.
Direct comparisons of VFS and FEES have been under-
taken and have shown that there is unlikely to be a difference
between clinical management guided by either of these two
techniques.
31
OTHER ASSESSMENT TOOLS
Bedside assessments may be improved by the simple measure
of following oxygen saturations with pulse oximetry during a
swallowing task.
21
Zaidi et al first reported that a decrease of
N
In the context of stroke, oropharyngeal dysphagia is
probably best defined as a disruption of bolus flow
through the mouth and pharynx.
N
Aspiration is the incursion of food material into the
airway and beyond the true vocal cords.
Bedside clinical assessment tests a patient with varying
volumes and consistencies while observing for tell tale signs
of aspiration. As the sensitivity of screening tests improve, the
specificity declines.
Figure 1 VFS image illustrating the anatomy of the oropharynx. (1)
Ramus of mandible; (2) hard palate; (3) soft palate; (4) pharynx; (5)
epiglottis; (6) laryngeal vestibule; (7) vocal cords; (8) trachea; (9) region
of the upper oesophageal sphincter; (10) region of the oesophagus.
Table 1 Sensitivity and specificity for aspiration assessed with bedside swallow tests
compared with videofluoroscopy
Researchers Patients studied Sensitivity ( %) Specificity (%)
Smithard et al
18
83 47 86
DePippo et al
19
44 76 59
Splaingard et al
20
87 strokes 42 91
Smith et al
21
53 86 69
Daniels et al
22
59 92 67
McCullough et al
23
60 91 47
Nishiwaki
24
61 72 67
384 Singh, Hamdy
www.postgradmedj.com
2% in oxygen saturation after drinking 10 ml of water was
predictive of aspiration on a videofluoroscopy assessment.
32
One other institute has been able to replicate these findings
33
whereas two investigators have found contradictory
results.
34 35
Further work is required to establish which
patients might benefit from this additional assessment and
also to define whether serial measurements can be used to
track recovery.
Other screening tools have been advocated but remain
research tools only at present with limited data in stroke
patients. These include scintigraphy, ultrasound, and impe-
dance tomography.
36–38
OVERVIEW OF IDENTIFICATION OF DYSPHAGIA
Ideally a clinician should have access to bedside screening
tests, VFS and FEES. It is important to recognise the
strengths and weaknesses of each assessment and build a
risk profile rather than categorising patients into dysphagic
or non-dysphagic. The current best practice should be bedside
clinical testing with a low threshold for instrumental
examination both to identify silent aspirators and to guide
management.
CLINICAL COURSE
Despite the problems associated with diagnosis of dysphagia
the clinical impression is that ‘‘recovery’’ is comparatively
common and takes place over days to weeks.
5739
Two large
studies used the objective tool of VFS to plot the recovery. The
first was Smithard et al who found an aspiration incidence of
Figure 2 Serial VFS images showing
the normal passage of a barium bolus
through the pharynx. Image (1) is the
resting state. Barium appears black as it
passes through the pharynx (2), the
upper oesophageal sphincter (3), and
the proximal oesophagus (4).
Videofluoroscopy is a commonly available investigation for
the assessment of swallowing. Data are available on
anatomy, all stages of swallowing physiology, the presence
of aspiration, and the response to therapeutic manoeuvres. It
does however, entail ionising radiation and is performed in
somewhat artificial settings.
Figure 3 View with fibreoptic endoscopic evaluation of swallowing. (1)
Route to oesophagus; (2) trachea; (3) vocal cords; (4) aryepiglottic folds;
(5) epiglottis; (6) fluid with green dye. Image courtesy of KayPENTAX,
Lincoln Park, NJ, USA.
Dysphagia in stroke patients 385
www.postgradmedj.com
22% at a median of two days after stroke and 15% at one
month.
40 41
Mann et al prospectively studied 128 stroke patients with a
VFS at a median time of 10 days after symptom onset.
7
They
found dysphagia in 64% and aspiration in 22%. Their
definition of dysphagia on VFS was the delay, disorder,
and/or weakness of any component of swallowing that
adversely affected bolus delivery and increased the risk of
aspiration. Six months later 11 patients had been lost to
follow up and five had died. The remainder were reassessed
and those who were initially dysphagic underwent a repeat
VFS examination. VFS identified swallowing abnormalities
in 80% of the 67 repeat examinations and 25% were
aspirating. Despite this only 15 patients had not returned to
their pre-stroke diet. No further follow up beyond the initial
six months was reported.
Logemann reported a persistent delay in temporal mea-
sures of swallowing after recovery from dysphagia after
stroke.
12
There was also a slight increase in pharyngeal
residue and her suggestion was that swallowing may recover
functionally but may remain impaired at a more intricate
level. This may also account for the increased incidence of
dysphagia after a second or third stroke.
For those patients who fail to recover a safe swallow in the
short term, the alternative is enteral feeding via a percuta-
neous endoscopic gastrostomy (PEG) tube. However, PEG
feeding should not be seen as an end point in dysphagia
rehabilitation. James et al addressed the long term outcome
of this group in a retrospective manner.
42
They reviewed 126
patients who had a PEG in situ after an acute stroke. Median
length of follow up was 31 months (range 4–71). Over half
(57%) had died, almost a third (29%) had been able to
remove their PEG after improvements in their swallowing,
the remainder still had a PEG in situ. Others have also
reported recovery from dysphagia months or years after a
stroke but the rate of recovery remains slow.
43–45
DOES DYSPHAGIA MATTER?
With such a clear propensity for recovery, various authors
have tried to evaluate the impact of dysphagia on a wide
variety of clinical outcomes.
15
Several authors have correlated
clinical dysphagia with increased risk of chest infec-
tions.
571441
Of the studies using VFS to confirm aspiration,
Holas et al
46
and Kidd et al
47
found an increased risk of chest
infection. In a review of over 14 000 patients in the USA,
Katzan et al identified a threefold increased risk of death
among stroke patients if they developed pneumonia.
48
This
risk was calculated after adjustment for stroke severity.
Mortality for dysphagic stroke patients therefore stands at
between 27% and 37%.
41 48
Unpublished data from our
department suggest a poorer prognosis for patients aspirating
on VFS compared with those that demonstrated safe
swallowing and perhaps unsurprisingly, the difference in
mortality is over the first three to six months only.
An absolute correlation between aspiration and chest
infection would not be inevitable as numerous other factors
such as mental state, posture, dentition, immune status, age,
and respiratory comorbidity may also play a part.
49–51
Overall
around 12%–30% of all stroke patients will suffer a chest
infection during their inpatient stay.
3 7 47 52
Poor nutritional state has certainly been correlated with
increased mortality after admission with acute stroke.
53
Although this reflects pre-stroke status rather than post-
stroke dysphagia, one might infer that continued decline in
nutritional status may still be important in this group of
patients.
Dysphagia does therefore have prognostic implications and
should be assessed in all patients presenting with symptoms
of a stroke.
WHY DO HALF OF PATIENTS DEVELOP DYSPHAGIA?
CENTRAL NERVOUS SYSTEM CONTROL OF
SWALLOWING
A series of experiments from Hamdy et al have used
transcranial magnetic stimulation (TMS) to probe the role
of the motor cortex in health and after stroke. TMS is a safe
and non-invasive technique that can stimulate focal areas of
the cerebral cortex and thereby map connections from motor
cortex to target muscles. The strength of the projections from
motor cortex is denoted by the amplitude of electromyo-
graphic (EMG) traces at the target muscle. Initial studies in
healthy volunteers described how midline swallowing mus-
cles are represented bilaterally in the motor cortex but in an
asymmetric manner.
54
This has led to the hypothesis that
some subjects have a ‘‘dominant’’ swallowing hemisphere.
It was subsequently postulated that stroke affecting the
dominant hemisphere was more likely to result in dyspha-
gia.
55
Twenty patients were recruited after their first stroke
confirmed on computed tomography of the brain. TMS was
delivered to sites over both hemispheres in turn and any
resulting EMG response at the pharyngeus muscle was
recorded. Eight of the patients were dysphagic. Stimulation
of the affected hemisphere produced similarly small EMG
responses in both dysphagic and non-dysphagic patients. In
contrast, stimulation of the unaffected hemisphere produced
Fibreoptic evaluation of swallowing can be performed at the
bedside with a variety of food substances and has an
excellent safety profile. It can be repeated regularly and
permits sensory testing. In contrast it is not widely available
and requires both specialised equipment and trained
operators.
Table 2 Advantages and disadvantages of
videofluoroscopy and fibreoptic endoscopic evaluation of
swallowing
Videofluoroscopy
Advantages Widely available, rapid and safe
Assessment of all stages of swallowing
Variety of foods can be tested
Allows the assessment of therapeutic
manoeuvres
Disadvantages Radiation exposure
Findings may not reflect ward behaviour
Density of barium means aspiration may not
reflect risk with other foods
Training required for interpretation
Fibreoptic endoscopic
evaluation of swallowing
Advantages Performed at the bedside with normal meals
Gives better anatomical data of the pharynx/
larynx
Can be repeated regularly
Sensory testing can be undertaken
Disadvantages Not widely available
Requires skilled operators
White out often obscures the period of
aspiration
No information is gathered on oral control
Although up to half of acute stroke patients will be dysphagic,
most will have recovered a safe swallow by one month.
386 Singh, Hamdy
www.postgradmedj.com
significantly smaller responses in the dysphagic patients.
Although studied retrospectively, this did indeed suggest that
lesions of the dominant hemisphere were more likely to
result in dysphagia.
MECHANISMS FOR SWALLOWING RECOVERY IN
DYSPHAGIC STROKE
TMS was also used to scrutinise cortical connections over
time.
56
Twenty eight patients were recruited and their cortical
maps in response to TMS of both hemispheres were plotted at
one week, one month, and three months after stroke. VFS
assessment of their swallow was also undertaken and EMG
responses of the thenar muscle were used as a control. The
key finding was that dysphagic patients who recovered over
time showed an increase in their cortical maps over the
unaffected hemisphere at one month and three months. The
patients who remained dysphagic did not show this change
in their pharyngeal cortical maps. Cortical representation of
the thenar muscle reappeared in the affected hemisphere (see
fig 4) The conclusion drawn was that recovery from
dysphagia after stroke might follow reorganisation of the
unaffected motor cortex.
MANAGEMENT
Clearly the goals in dysphagia therapy are to reduce the
morbidity and mortality associated with chest infections,
improve nutritional status, and return patients to a normal
diet with resultant improvement of their quality of life.
Unfortunately, there is a paucity of evidence for dysphagia
therapy, which has been highlighted in a Cochrane review
57
as well as an American Gastroenterology Association
technical review.
58
Broadly speaking, therapy can be differ-
entiated into compensatory and rehabilitative strategies. The
former aims to keep patients safe when eating whereas the
latter aims to speed the recovery process. Because few active
measures have proved efficacy, the general aim is often to
prevent chest infections while spontaneous recovery takes
place.
COMPENSATORY STRATEGIES
Standard practice is to change the consistency of food and
fluids given to dysphagic patients with the most severely
affected patients left nil by mouth. The rationale for changed
consistencies comes from findings at the bedside and during
VFS. Although numerous studies have described the changes
in swallowing physiology with thickened fluids
59–64
none have
shown clinical efficacy in stroke patients. VFS regularly
identifies individual patients who endure reduced aspiration
with particular consistencies of food. It is therefore unlikely
that ethical approval would ever be gained to randomise
patients to normal diet and fluids when they have been noted
to aspirate on such consistencies, making an objective study
of food consistencies difficult.
In a similar manner, only expert consensus supports the
use of manoeuvres such as a chin tuck when swallowing,
head turn or the Mendelsohn manoeuvre. Chin tuck entails
asking patients to lower their chin towards their chest before
swallowing.
65
This brings the epiglottis and the aryepiglottic
folds closer to together and it is the apposition of these
structures that will close the airway during swallowing. Head
turn is a simple rotation of the head to the paretic side and
may increase bolus flow.
66
The Mendelsohn’s manoeuvre
requires a little more training and entails the sustained
contraction of the suprahyoid muscles in an effort to
maintain laryngeal elevation and thus upper oesophageal
sphincter opening and airway closure.
67
Swallowing assess-
ments are thus viewed as individual treatment trials and any
of these techniques can be advocated if an individual patient
is noted to swallow safely when exercising any particular
method. It should be noted however, that their efficacy
remains controversial.
There is more substantive literature on the use of
nasogastric (NG) and PEG feeding. The first question to
raise is do they improve outcome? Unfortunately, the answer
is probably ‘‘no.’’ Although the studies were not exclusively
in stroke patients, there are a handful of trials suggesting that
Figure 4 Graphical representation of
the changes in cortical maps after a left
hemisphere stroke over a period of
three months. Reprinted from Hamdy S,
Aziz Q, Rothwell JC, et al. Recovery of
swallowing after dysphagic stroke
relates to functional reorganization in
the intact motor cortex.
Gastroenterology 1998;115:1104–
1112 with permission from American
Gastroenterological Association.
Dysphagia after stroke carries a threefold increased mortality
risk and a sixfold to sevenfold fold increased risk of
aspiration pneumonia. It should be screened for on every
patient presenting with symptoms of a stroke.
Dysphagia in stroke patients 387
www.postgradmedj.com
NG and PEG feeding do not reduce the incidence of
pneumonia or death.
68–71
One study in stroke patients did
suggest a pronounced benefit from NG feeding but these
results have not been reproduced elsewhere in the litera-
ture.
72
Dziewas et al followed up 100 stoke patients fed by NG
tube and found a 44% pneumonia rate. Although there was
no control group for comparison it is clear that a large
proportion of patients fed by NG tube will still develop
respiratory infection.
73
Why a person without any oral intake should develop
pneumonia is best explained by the fact that the oral cavity is
rich in bacterial flora and that this is the source of pathogenic
organisms. Further evidence for this premise comes from
regression analyses identifying poor dentition (which is a
proxy for greater oral bacterial colonisation) as an indepen-
dent predictor of chest infection.
74
Although there may not be a reduced infection rate with
PEG feeding, there is certainly an improved nutritional status
because of more consistent delivery of feed.
75 76
There seems
little doubt that if patients are receiving a restricted oral diet,
then they will at least benefit from nutrition and hydration
albeit with questionable protection from pneumonia.
If we accept that NG and PEG feeding have a role, the next
question is when to start such a regimen and which of the
two to select. Fortunately, clinical decisions are at least
supported by a large multicentre randomised controlled trial.
The feed or ordinary diet (FOOD) trial recruited dysphagic
stroke patients to two studies relevant to this discussion.
77 78
The first trial randomised stroke patients within seven days
of admission to either early NG feeding or to no tube feeding
for more than seven days. An intention to treat analysis of
the 859 enrolled patients showed an absolute reduction in
death of 5.8% (95%CI 20.8 to 12.5%, p = 0.09) without
reducing the incidence of pneumonia. The absolute reduction
in the combined outcome of death or poor outcome was just
1.2% (24.2 to 6.6%, p = 0.7). Although statistical significance
at the 5% level was not reached, the authors suggested that
early enteral feeding may keep patients alive who would
otherwise have died but those patients remain severely
impaired and dependent. The reduced mortality could not be
attributed to reduced aspiration.
The second trial randomised dysphagic patients to either
NG or PEG feeding. The latter was associated with an
increased risk of death or poor outcome of 7.8% (0% to 15%,
p = 0.05). It might be concluded from these two studies that
early NG feeding is likely to be beneficial but PEG feeding can
be reasonably delayed for a period of weeks. In the longer
term PEG feeding does improve nutritional status and should
be considered when artificial nutrition and hydration is
required beyond two weeks.
Parenteral nutrition has never been tested in the stroke
setting but is likely to be associated with significant
complications and is rarely fruitful.
REHABILITATIVE STRATEGIES
In terms of head and neck exercises, the best evidence
supports an exercise aimed at opening the upper oesophageal
sphincter. In chronic dysphagic subjects including stroke
patients, Shaker et al described an exercise that improved
sphincter opening and thereby reduced post-swallow phar-
yngeal residue.
79
Briefly, it comprises the patient lying supine
on a bed and raising their head off the bed for a period of
seconds and repeating this 20 times. It was felt this would
reinforce the action of the suprahyoid muscles that are
Table 3 Grading of evidence base for rehabilitation strategies in dysphagic stroke
patients. National Institute of Health and Clinical Excellence criteria are used for grading
Intervention Level of evidence Comments
Head raising exercise Ib Specific exercises will improve opening of the
upper oesophageal sphincter in stroke
patients with sphincter dysfunction.
Pharyngeal stimulation Ib Pharyngeal electrical stimulation has shown
promising results in preliminary studies and
further trials are under way.
ACE inhibitors III No RCT
Biofeedback IV Two studies totalling 55 patients. No RCT
Oral exercises None No published evidence
Oral stimulation None Recent publications suggest no efficacy
RCT, randomised controlled trial.
There are few clinical trials guiding therapy. The mainstay of
management is to keep patients safe while spontaneous
recovery takes place. This is achieved through compensatory
strategies such as changing food consistencies, regulating
bolus size, head rotation before swallowing, and the chin
tuck manoeuvre.
Key references
N
Shaker R, Easterling C, Kern M, et al. Rehabilitation of
swallowing by exercise in tube-fed patients with
pharyngeal dysphagia secondary to abnormal UES
opening. Gastroenterology 2002;122:1314–21.
N
Hamdy S, Aziz Q, Rothwell JC, et al. Explaining
oropharyngeal dysphagia after unilateral hemispheric
stroke. Lancet 1997;350:686–92.
N
Mann G, Hankey GJ, Cameron D. Swallowing function
after stroke: prognosis and prognostic factors at
6 months. Stroke 1999;30:744–8.
N
Dennis MS, Lewis SC, Warlow C. Effect of timing and
method of enteral tube feeding for dysphagic stroke
patients (FOOD): a multicentre randomised controlled
trial. Lancet 2005;365:764–72.
N
Fraser C, Power M, Hamdy S, et al. Driving plasticity in
human adult motor cortex is associated with improved
motor function after brain injury. Neuron
2002;34:831–40.
Nasogastric and percutaneous gastrostomy feeding have not
been shown to reduce the rate of chest infections but will
improve nutritional status.
388 Singh, Hamdy
www.postgradmedj.com
critical to upper oesophageal sphincter opening.
A variety of oral stimulation techniques have been used
without clear evidence of efficacy. These include tactile and
thermal stimulation.
80
In contrast, pharyngeal electrical
stimulation may have a therapeutic role.
81
Fraser et al initially
investigated the effects of pharyngeal electrical stimulation in
healthy volunteers with TMS. They established that at
specific parameters, a sustained increase in swallowing
motor cortex excitability could be achieved. They then
applied the specified stimulation parameters to 10 of 16
dysphagic stroke patients while six patients received sham
stimulation. Standardised VFS was used before and one hour
after the stimulation/sham to assess any changes. Whereas
the sham group showed no change in aspiration, the
intervention group showed a 30% reduction in aspiration.
Although too early to make any strong recommendations,
these data show promise and a larger trial is underway to
establish for how long the effect might last and how often
this therapy needs to be repeated.
Limited numbers of drugs have been advocated to reduce
aspiration including nifedipine
82
and ACE inhibitors.
83
However, the trial data remain too limited to support their
use at present. Biofeedback for post-stroke dysphagia
rehabilitation has been pioneered over recent years
84 85
with
commercial systems becoming more widely available. As yet
no randomised controlled trial has been reported. Table 3
shows the levels of evidence for various treatment regimens.
SUMMARY
Dysphagia affects up to half of acute stroke patients and
carries a threefold to sevenfold increased risk of aspiration
pneumonia. With the subsequent mortality associated with
pneumonia, dysphagia has been recognised as an indepen-
dent predictor of mortality after stroke. Fortunately, most
patients will make a functional recovery over a period of days
to weeks.
This incidence and remarkable recovery rate may be
accounted for by the bilateral distribution of control of
swallowing musculature in the motor cortex. After hemi-
spheric stroke, neuroplastic adaptation permits the control of
swallowing musculature to be reorganised to the unaffected
hemisphere.
Identifying dysphagia can be done by bedside testing or
instrumental examination such as VFS and FEES but best
practice would combine both along with a global assessment
of the stroke patient.
Management should be aimed at facilitating safe swallow-
ing while spontaneous recovery takes place. Enteral feeding
tubes are commonly used when oral intake is not deemed
sufficient for nutrition and hydration purposes. However, this
approach has not been shown to reduce the incidence of
aspiration pneumonia in most of the studies published to
date although it does improve nutritional status. Manoeuvres
to aid safe swallowing can only be offered on an individual
basis by trained practitioners and are not universally
applicable to all dysphagic patients. Few of these techniques
have been tested in randomised controlled trials. Much more
work is required to investigate the true impact of current
dysphagia therapy and to work towards developing new
therapies of the future.
SELF ASSESSMENT QUESTIONS (ANSWERS AFTER
THE REFERENCES)
1. Regarding the incidence of dysphagia after an acute
stroke?
(A) all patients with a clinical diagnosis of stroke should be
screened for dysphagia
(B) only 10% will be dysphagic on admission
(C) up to 50% will be dysphagic on admission
(D) up to 10% will be dysphagic at discharge
2. What is meant by the term ‘‘silent aspirator’’?
(A) The patient is not aware of any problems with
swallowing
(B) The patient does not cough when swallowing
(C) There are no bedside signs of aspiration despite
aspiration seen on instrumental examination
(D) The patient has a normal instrumental swallowing
assessment but is still at risk of chest infections
3. Which of the following is an advantage of fibreoptic
endoscopic evaluation of swallowing?
(A) Can be undertaken at the bedside with normal food
(B) Can be performed by any ward staff
(C) Can detect anatomical as well as physiological abnorm-
alities
(D) Has a very low complication rate
4. Which exercises or manoeuvres have been shown to
improve upper oesophageal sphincter opening?
(A) Head raising exercises
(B) Tongue protrusion
(C) Chin tuck
(D) Mendelsohn manoeuvre
5. Which of the following statements about artificial
enteral feeding in dysphagic stroke patients is true?
(A) Enteral feeding reduces the risk of chest infection
(B) Enteral feeding reduces the risk of malnutrition
(C) Recovery of swallowing is unlikely after gastrostomy
tube placement
(D) Gastrostomy feeding is superior to nasogastric feeding
even in the first few weeks after stroke
6. Which factors other than oropharyngeal motor function
should be taken into account during a swallowing
assessment?
(A) Cognitive function
(B) Patient posture
(C) Dentition
(D) Respiratory status
Authors’ affiliations
.....................
S Singh, S Hamdy, Department of GI Sciences, Hope Hospital,
Manchester, UK
N
Specific exercises will improve opening of the upper
oesophageal sphincter in stroke patients with sphincter
dysfunction.
N
Pharyngeal electrical stimulation has shown promising
results in preliminary studies and further trials are
underway.
N
There are insufficient data to support biofeedback or
drug therapy for post-stroke dysphagia.
Dysphagia in stroke patients 389
www.postgradmedj.com
Competing interests: SS is a clinical research fellow employed by
Manchester University through grants from The Health Foundation and
the Medical Research Council. SH is a lecturer at Manchester University
and honorary consultant Gastroenterologist at Hope Hospital, Salford.
Neither author has any competing interests to declare.
REFERENCES
1 Daniels SK, Ballo LA, Mahoney MC, et al. Clinical predictors of dysphagia
and aspiration risk: outcome measures in acute stroke patients. Arch Phys Med
Rehabil 2000;81:1030–3.
2 Daniels SK, Brailey K, Priestly DH, et al. Aspiration in patients with acute
stroke. Arch Phys Med Rehabil 1998;79:14–19.
3 Johnson ER, McKenzie SW, Sievers A. Aspiration pneumonia in stroke. Arch
Phys Med Rehabil 1993;74:973–6.
4 Kidd D, Lawson J, Nesbitt R, et al. Aspiration in acute stroke: a clinical study
with videofluoroscopy. Q J Med 1993;86:825–9.
5 Gordon C, Hewer RL, Wade DT. Dysphagia in acute stroke. BMJ (Clin Res Ed)
1987;295:411–14.
6 Mann G, Hankey GJ, Cameron D. Swallowing disorders following acute
stroke: prevalence and diagnostic accuracy. Cerebrovasc Dis
2000;10:380–6.
7 Mann G, Hankey GJ, Cameron D. Swallowing function after stroke: prognosis
and prognostic factors at 6 months. Stroke 1999;30:744–8.
8 Robbins J, Levin RL. Swallowing after unilateral stroke of the cerebral cortex:
preliminary experience. Dysphagia 1988;3:11–17.
9 Sellars C, Campbell AM, Stott DJ, et al. Swallowing abnormalities after acute
stroke: a case control study. Dysphagia 1999;14:212–18.
10 Odderson IR, Keaton JC, McKenna BS. Swallow management in patients on
an acute stroke pathway: quality is cost effective. Arch Phys Med Rehabil
1995;76:1130–3.
11 Wolfe CD, Taub NA, Woodrow J, et al. Does the incidence, severity, or case
fatality of stroke vary in southern England? J Epidemiol Community Health
1993;47:139–43.
12 Logemann JA. Evaluation and treatment of swallowing disorders. 2nd ed.
Austin, TX: Pro, ed, 1983:406.
13 Leder SB. Videofluoroscopic evaluation of aspiration with visual examination
of the gag reflex and velar movement. Dysphagia 1997;12:21–3.
14 DePippo K, Holas M, Reding M, et al. Dysphagia therapy following stroke: a
controlled trial. Neurology 1994;44:1655–60.
15 Perry L, Love CP. Screening for dysphagia and aspiration in acute stroke: a
systematic review. Dysphagia 2001;16:7–18.
16 Lundy DS, Smith C, Colangelo L, et al. Aspiration: cause and implications.
Otolaryngol Head Neck Surg 1999;120:474–8.
17 Smith CH, Logemann JA, Colangelo LA, et al. Incidence and patient
characteristics associated with silent aspiration in the acute care setting.
Dysphagia 1999;14:1–7.
18 Smithard D, O’Neill, Park C, et al. Can bedside assessment reliably exclude
aspiration following acute stroke? Age Ageing 1998;27:99–106.
19 DePippo KL, Holas MA, Reding MJ. Validation of the 3-oz water swallow test
for aspiration following stroke. Arch Neurol 1992;49:1259–61.
20 Splaingard ML, Hutchins B, Sulton LD, et al. Aspiration in rehabilitation
patients: videofluoroscopy vs bedside clinical assessment. Arch Phys Med
Rehabil 1988;69:637–40.
21 Smith HA, Lee SH, O’Neill PA, et al. The combination of bedside swallowing
assessment and oxygen saturation monitoring of swallowing in acute stroke: a
safe and humane screening tool. Age Ageing 2000;29:495–9.
22 Daniels SK, McAdam CP, Brailey K, et al. Clinical assessment of swallowing
and prediction of dysphagia severity. Am J Speech Lang Pathol
1997;6:17–24.
23 McCullough GH, Wertz RT, Rosenbek JC. Sensitivity and specificity of clinical/
bedside examination signs for detecting aspiration in adults subsequent to
stroke. J Commun Disord 2001;34:55–72.
24 Nishiwaki K, Tsuji T, Liu M, et al. Identification of a simple screening tool for
dysphagia in patients with stroke using factor analysis of multiple dysphagia
variables. J Rehabil Med 2005;37:247–51.
25 Horner J, Massey EW. Silent aspiration following stroke. Neurology
1988;38:317–19.
26 Kuhlemeier KV, Yates, Palmer JB. Intra- and interrater variation in the
evaluation of videofluorographic swallowing studies. Dysphagia
1998;13:142–7.
27 Ekberg O, Nylander G, Fork FT, et al. Interobserver variability in
cineradiographic assessment of pharyngeal function during swallow.
Dysphagia 1988;3:46–8.
28 Daniels SK, Brailey K, Foundas AL. Lingual discoordination and dysphagia
following acute stroke: analyses of lesion localization. Dysphagia
1999;14:85–92.
29 Langmore SE, Schatz K, Olsen N. Fiberoptic endoscopic examination of
swallowing safety: a new procedure. Dysphagia 1988;2:216–19.
30 Aviv JE, Murry T, Zschommler A, et al. Flexible endoscopic evaluation of
swallowing with sensory testing: patient characteristics and analysis of safety
in 1,340 consecutive examinations. Ann Otol Rhinol Laryngol
2005;114:173–6.
31 Doggett DL, Turkelson CM, Coates V. Recent developments in diagnosis and
intervention for aspiration and dysphagia in stroke and other neuromuscular
disorders. Curr Atheroscler Rep 2002;4:311–18.
32 Zaidi NH, Smith HA, King SC, et al. Oxygen desaturation on swallowing as a
potential marker of aspiration in acute stroke. Age Ageing 1995;24:267–70.
33 Collins MJ, Bakheit AM. Does pulse oximetry reliably detect aspiration in
dysphagic stroke patients? Stroke 1997;28:1773–5.
34 Sellars C, Dunnet C, Carter R. A preliminary comparison of videofluoroscopy
of swallow and pulse oximetry in the identification of aspiration in dysphagic
patients. Dysphagia 1998;13:82–6.
35 Colodny N. Comparison of dysphagics and nondysphagics on pulse oximetry
during oral feeding. Dysphagia 2000;15:68–73.
36 Miller JL, Watkin KL. Lateral pharyngeal wall motion during swallowing using
real time ultrasound. Dysphagia 1997;12:125–32.
37 Hamlet S, Choi J, Zormeier M, et al. Normal adult swallowing of liquid and
viscous material: scintigraphic data on bolus transit and oropharyngeal
residues. Dysphagia 1996;11:41–7.
38 Hughes TA, Liu, Griffiths H, et al. The repeatability and variability of electrical
impedance tomography indices of pharyngeal transit time in normal adults.
Physiol Meas 1995;16(suppl A):A79–86.
39 Barer DH. The natural history and functional consequences of dysphagia after
hemispheric stroke. J Neurol Neurosurg Psychiatry 1989;52:236–41.
40 Smithard DG, O’Neill PA, England RE, et al. The natural history of dysphagia
following a stroke. Dysphagia 1997;12:188–93.
41 Smithard DG, O’Neill PA, Park C, et al. Complications and outcome after
acute stroke: Does dysphagia matter? Stroke 1996;27:1200–4.
42 James A, Kapur K, Hawthorne AB. Long-term outcome of percutaneous
endoscopic gastrostomy feeding in patients with dysphagic stroke. Age
Ageing 1998;27:671–6.
43 Rehman HU, Knox J. There is a need for a regular review of swallowing ability
in patients after PEG insertion to identify patients with delayed recoveryof
swallowing. Dysphagia 2000;15:48.
44 Hull MA, Rawlings J, Murray FE, et al. Audit of outcome of long-term enteral
nutrition by percutaneous endoscopic gastrostomy. Lancet 1993;341:869–72.
45 Wanklyn P, Cox N, Belfield. Outcome in patients who require a gastrostomy
after stroke. Age Ageing 1995;24:510–14.
46 Holas MA, DePippo KL, Reding MJ. Aspiration and relative risk of medical
complications following stroke. Arch Neurol 1994;51:1051–3.
47 Kidd D, Lawson J, Nesbitt R, et al. The natural history and clinical
consequences of aspiration in acute stroke. QJM 1995;88:409–13.
48 Katzan IL, Cebul RD, Husak SH, et al. The effect of pneumonia on mortality
among patients hospitalized for acute stroke. Neurology 2003;60:620–5.
49 Parker C, Power M, Hamdy S, et al. Awareness of dysphagia by patients
following stroke predicts swallowing performance. Dysphagia
2004;19:28–35.
50 Finegold SM. Aspiration pneumonia. Rev Infect Dis 1991;13(suppl
9):S737–742.
51 Langmore SE, Skarupski KA, Park PS, et al. Predictors of aspiration
pneumonia in nursing home residents. Dysphagia 2002;17:298–307.
52 Davenport RJ, Dennis MS, Wellwood I, et al. Complications after acute stroke.
Stroke 1996;27:415–20.
53 Poor nutritional status on admission predicts poor outcomes after stroke:
observational data from the FOOD trial. Stroke 2003;34:1450–6.
54 Hamdy S, Aziz Q, Rothwell JC, et al. The cortical topography of human
swallowing musculature in health and disease. Nat Med 1996;2:1217–24.
55 Hamdy S, Aziz Q, Rothwell JC, et al. Explaining oropharyngeal dysphagia
after unilateral hemispheric stroke. Lancet 1997;350:686–92.
56 Hamdy S, Aziz Q, Rothwell JC, et al. Recovery of swallowing after dysphagic
stroke relates to functional reorganization in the intact motor cortex.
Gastroenterology 1998;115:1104–12.
57 Bath PM, Bath FJ, Smithard DG. Interventions for dysphagia in acute stroke.
Cochrane Library. Issue 2. Oxford: Update Software, 2000.
58 Cook IJ, Kahrilas PJ. AGA technical review on management of oropharyngeal
dysphagia. Gastroenterology 1999;116:455–78.
59 Bisch EM, Logemann JA, Rademaker AW, et al. Pharyngeal effects of bolus
volume, viscosity, and temperature in patients with dysphagia resulting from
neurologic impairment and in normal subjects. J Speech Hear Res
1994;37:1041–59.
60 Butler SG, Postma GN, Fischer E. Effects of viscosity, taste, and bolus volume
on swallowing apnea duration of normal adults. Otolaryngol Head Neck Surg
2004;131:860–3.
61 Steele CM, Van Lieshout PH. Influence of bolus consistency on lingual
behaviors in sequential swallowing. Dysphagia 2004;19:192–206.
62 Hiss SG, Strauss M, Treole K, et al. Effects of age, gender, bolus volume, bolus
viscosity, and gustation on swallowing apnea onset relative to lingual bolus
propulsion onset in normal adults. J Speech Lang Hear Res 2004;47:572–83.
63 Kendall KA, Leonard RJ, McKenzie SW. Accommodation to changes in bolus
viscosity in normal deglutition: a videofluoroscopic study. Ann Otol Rhinol
Laryngol 2001;110:1059–65.
64 Raut VV, McKee GJ, Johnston BT. Effect of bolus consistency on swallowing–
does altering consistency help? Eur Arch Otorhinolaryngol 2001;258:49–53.
65 Shanahan TK, Logemann JA, Rademaker AW, et al. Chin-down posture effect
on aspiration in dysphagic patients. Arch Phys Med Rehabil 1993;74:736–9.
66 Logemann JA, Kahrilas PJ, Kobara M, et al. The benefit of head rotation on
pharyngoesophageal dysphagia. Arch Phys Med Rehabil 1989;70:767–71.
67 Kahrilas PJ, Logemann JA, Krugler C, et al. Volitional augmentation of upper
esophageal sphincter opening during swallowing. Am J Physiol
1991;260):G450–456.
68 Cogen R, Weinryb J. Aspiration pneumonia in nursing home patients fed via
gastrostomy tubes. Am J Gastroenterol 1989;84:1509–12.
69 Hassett JM, Sunby C, Flint LM, No elimination of aspiration pneumonia in
neurologically disabled patients with feeding gastrostomy. Surg Gynecol
Obstet 1988;167:383–8.
70 Finucane TE, Bynum JP. Use of tube feeding to prevent aspiration pneumonia.
Lancet 1996;348:1421–4.
390 Singh, Hamdy
www.postgradmedj.com
71 Ciocon JO, Silverstone FA, Graver LM, et al. Tube feedings in elderly patients.
Indications, benefits, and complications. Arch Intern Med 1988;148:429–33.
72 Nakajoh K, Nakagawa T, Sekizawa K, et al. Relation between incidence of
pneumonia and protective reflexes in post-stroke patients with oral or tube
feeding. J Intern Med 2000;247:39–42.
73 Dziewas R, Ritter M, Schilling M, et al. Pneumonia in acute stroke patients fed
by nasogastric tube. J Neurol Neurosurg Psychiatry 2004;75:852–6.
74 Langmore SE, Terpenning MS, Schork A, et al. Predictors of aspiration
pneumonia: how important is dysphagia? Dysphagia 1998;13:69–81.
75 Norton B, Homer-Ward M, Donnelly MT, et al. A randomised prospective
comparison of percutaneous endoscopic gastrostomy and nasogastric tube
feeding after acute dysphagic stroke. BMJ 1996;312:13–16.
76 Park RH, Allison MC, Lang J, et al. Randomised comparison of percutaneous
endoscopic gastrostomy and nasogastric tube feeding in patients with
persisting neurological dysphagia. BMJ 1992;304:1406–9.
77 Dennis MS, Lewis SC, Warlow C. Effect of timing and method of enteral tube
feeding for dysphagic stroke patients (FOOD): a multicentre randomised
controlled trial. Lancet 2005;365:764–72.
78 Dennis MS, Lewis SC, Warlow C. Routine oral nutritional supplementation for
stroke patients in hospital (FOOD): a multicentre randomised controlled trial.
Lancet 2005;365:755–63.
79 Shaker R, Easterling C, Kern M, et al. Rehabilitation of swallowing by exercise
in tube-fed patients with pharyngeal dysphagia secondary to abnormal UES
opening. Gastroenterology 2002;122:1314–21.
80 Lazarra G, Lazarus C, Logemann JA. Impact of thermal stimulation on the
triggering of the swallow reflex. Dysphagia 1986;1:73–7.
81 Fraser C, Power M, Hamdy S, et al. Driving plasticity in human adult motor
cortex is associated with improved motor function after brain injury. Neuron
2002;34:831–40.
82 Perez I, Smithard DG, Davies H, et al. Pharmacological treatment of
dysphagia in stroke. Dysphagia 1998;13:12–16.
83 Arai T, Yasuda Y, Takaya T, et al. ACE inhibitors and symptomless dysphagia.
Lancet 1998;352:115–16.
84 Crary MA, Carnaby GDM, Groher ME, et al. Functional benefits of dysphagia
therapy using adjunctive sEMG biofeedback. Dysphagia 2004;19:160–4.
85 Huckabee ML, Cannito MP. Outcomes of swallowing rehabilitation in chronic
brainstem dysphagia: a retrospective evaluation. Dysphagia
1999;14:93–109.
ANSWERS
1. (A), (C), (D) are true. Royal College of Physician guidelines
reiterate that all stroke patients need screening for dysphagia.
Studies based on more objective instrumental assessments of
dysphagia have suggested an incidence of up to 50% after
stroke. 2. (C) is true. Most dysphagic patients will not
volunteer problems with swallowing but ‘‘silent aspirator’’
shows that the clinician cannot detect signs of aspiration at
the bedside. (B) and (D) would be true of non-dysphagic
patients. 3. (A), (C), and (D) are true. FEES is likely to
become more widely available as an alternative to video-
fluoroscopy. Training is required and commonly it is the
nurses, doctors, and speech and language therapists that take
on the role. 4. (A) Described by Shaker et al and (D) act on
upper oesophageal sphincter opening to facilitate bolus flow
through the pharynx. 5. (B) is the only true answer. There is
insufficient evidence for enteral feeding reducing pneumonia
and recovery of swallowing can take place months after a
stroke. The recent FOOD trial suggested no clear benefit of
gastrostomy ahead of nasogastric feeding in the short term. 6.
All of the answers are true.
Dysphagia in stroke patients 391
www.postgradmedj.com