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Håkan Nilsson, MD,1 Olle Ekberg, MD, PhD,2 Rolf Olsson, MD, PhD,2 Bengt Hindfelt, MD, PhD1
Departments of 1Neurology and 2Diagnostic Radiology, University of Lund, Malmö University Hospital, Malmö, Sweden
Abstract. This is a prospective study of 100 consecutive Stroke — Prospective study — Quantitative test — De-
stroke patients. Within 24 h after stroke onset they were glutition.
asked specifically about swallowing complaints and sub-
jected to a clinical examination including neurologic ex-
amination, Mini-Mental test, and Barthel score. Dys-
phagic patients were examined with the repetitive oral Dysphagia is common in various neurologic disorders,
suction swallow test (the ROSS test) for quantitative and particularly in stroke [1–5]. Although swallowing
evaluation of oral and pharyngeal function at 24 h, after dysfunction may have prognostic consequences [1,2,6],
1 week, and after 1 month. At 6 months, the patients there are few longitudinal studies of dysphagia or swal-
were interviewed about persistent dysphagia. Seventy- lowing dysfunction in stroke [2,5,7]. This study was un-
two patients could respond reliably at 24 h after the dertaken with the limited scope of evaluating the preva-
stroke onset and 14 of these complained of dysphagia. lence of symptomatic swallowing dysfunction in the
Non-evaluable patients were either unconscious, aphasic, acute stage of stroke and to correlate dysphagia with
or demented. The presence of dysphagia was not influ- major neurologic deficits. Furthermore, in the stroke pa-
enced by age or other risk factors for stroke. Facial pa- tients complaining of dysphagia, the oral and pharyngeal
resis, but no other clinical findings, were associated with swallow were quantitatively assessed. These patients
dysphagia. Dysphagia 24 h after stroke increased the risk were also followed up prospectively by repeated quanti-
of pneumonia but did not influence the length of hospital tative assessments.
stay, the manner of discharge from hospital, or the mor-
tality. The initial ROSS test, during which the seated Materials and Methods
patient ingests water through a straw, was abnormal in all
dysphagic stroke patients. One-third of the patients were The study participants included 100 consecutive patients (40 females,
unable to perform the test completely. Above all, dys- 60 males), median age 77 yr (range 59–94 yr) with acute ischemic or
hemorrhagic strokes admitted to the stroke unit at the Department of
function was disclosed during forced, repetitive swallow. Internal Medicine in Norrköping. A total of 61 patients underwent a
All phases of the ingestion cycle were prolonged neuroradiologic examination [59 were examined by computerized to-
whereas the suction pressures, bolus volumes, and swal- mography (CT) and 2 by magnetic resonance imaging (MRI)]. All
lowing capacities were low. Abnormalities of quantita- patients were asked about swallowing complaints within 24 hr after
tive swallowing variables decreased with time whereas stroke onset by HN. Patients were considered dysphagic if they re-
ported one or several of the following: (1) they could not eat or drink
the prevalences of swallowing incoordination and abnor- normally, (2) food got stuck in their mouth or throat, (3) they coughed
mal feeding-respiratory pattern became more frequent. during or after swallowing.
After 6 months, 7 patients had persistent dysphagia. Five Neurologic examination was performed by a senior neurologist.
of these were initially non-evaluable because of uncon- Cognitive function was tested by the Mini-Mental test [8]. The severity
sciousness, aphasia, or dementia. of the handicap was estimated according to the Barthel Index (the 20
graded scale) [9] at days 1 and 7 after the stroke. Intravenous drip was
Key words: Deglutition disorders — Dysphagia — given but no patient had a nasogastric tube inserted, nor a gastrostomy.
The food consistency was adjusted by a skilled nurse as needed for the
dysphagic patients. Commonly, purée was recommended for patients
Correspondence to: Håkan Nilsson, M.D., Department of Medicine, with oral dysfunction and thickened liquid patients prone to aspiration.
Vrinnevi Hospital, S-601 82 Norrköping, Sweden No particular swallowing rehabilitation was performed.
H. Nilsson et al.: Dysphagia in Stroke 33
The stroke patients, who on admission complained of dyspha- pertension, previous stroke, diabetes mellitus, smoking,
gia, were examined by the ROSS test, during which the seated patient atrial fibrillation, and other cardiac disease (angina pec-
was instructed to drink 200 ml of water through a straw, previously
described in detail [10]. Assessment was performed during single swal-
toris, myocardial insufficiency, status postmyocardial in-
low and forced, repetitive swallow (‘‘stressed swallow’’) with record- farction, or valvular disorders) did not differ between the
ings of the weight of water remaining in the glass, the suction pressure, dysphagic and nondysphagic patients (Table 1).
the signals from a Doppler probe, and a piezo-electric movement sensor
applied to the neck and a thermodetector in the nostril. The peak Quantitative Assessment of Swallowing
suction pressure, time of suction, bolus volume, time from suction to
swallowing, swallowing capacity, and time for a completed ingestion First Examination Within 24 h after Stroke. The
cycle were recorded. Furthermore, the interactions among suction,
swallowing, and respiration were assessed.
ROSS test was performed in all dysphagic patients ex-
The ROSS test was performed on three occasions: within 24 hr, cept 2 because of technical problems. Quantitative as-
1 week (range 6–8 days), and 1 month (range 24–41 days) after the sessment of single swallow was frequently normal at 24
stroke. Furthermore, after 6 months the patients were interviewed about hr after the stroke. Of the measured parameters, only
any persistent swallowing complaints. The results were compared with suction time and oral pharyngeal transit time were sta-
the findings in a reference group consisting of 53 elderly nondysphagic
subjects (31 females, 22 males, age >70 years, mean age 76 ± 5 yr) in
tistically significantly prolonged (Table 2). However,
a previous study published in Dysphagia [11]. during forced, repetitive swallow suction time, oral pha-
ryngeal transit time, feeding interval, and ingestion cycle
time were significantly prolonged and the bolus volume
Statistical Methods and swallowing capacity were significantly lower com-
pared with the reference group (Table 2).
Values were expressed as median values and interquartile ranges. For
statistical analysis, the Spearman test, the Kruskal-Wallis test, and the Second Examination after 1 Week. During single
Mann-Whitney U-test were used. The Chi-2 test with Yates correction swallow, suction time and oral pharyngeal transit time
was applied for analysis of frequencies. A p value <0.05 was consid-
ered significant. Values were considered abnormal if above 97.5% or
were still significantly abnormal. During forced, repeti-
below 2.5% of the nonparametric normal range of the control group. tive swallow, the bolus volume was now normal. Suction
time, oral pharyngeal transit time, feeding interval and
ingestion cycle time were still significantly abnormal.
The swallowing capacity had improved but was still be-
Results
low normal (Table 2).
Of the one hundred stroke patients, only 72 were able to Third Examination after 1 Month. During single
reliably answer the questions asked (see Methods). Four- swallow, all parameters had improved (Table 2). Suction
teen patients complained of dysphagia and 58 patients pressure was now even above the normal range. The
did not. None of these dysphagic patients needed paren- suction time was still prolonged whereas all other pa-
teral nutrition. Twenty-eight patients could not be evalu- rameters had normalized. Also during forced repetitive
ated at 24 h after the stroke because of either uncon- swallow, abnormally high suction pressure was seen.
sciousness (n 4 14, 8 females), aphasia (n 4 9, 5 fe- The bolus volume was normal but the suction time, oral
males), or dementia (n 4 5, 3 females) that had pharyngeal transit time, feeding interval, and ingestion
developed during the acute stroke. Most unconscious pa- cycle time were still significantly prolonged. The swal-
tients had intravenous drip. No patients had a nasogastric lowing capacity was about twice the value in the first
tube. examination but still below that of the reference group
Ninety-five patients suffered from cerebral hemi- (Table 2).
spheric stroke diagnosed clinically and frequently con- During analysis of frequencies, all patients had at
firmed by CT (n 4 59) or MRI (n 4 2) examinations. least one abnormal variable in the ROSS test performed
Forty-six patients had left-sided pareses, 38 had right- within 24 h (Table 3). On reexamination, 1 week after
sided pareses, and 11 were aphasic or had cognitive im- stroke onset 2 patients had normal results and when ex-
pairments. Five patients had brainstem strokes (Table 1). amined 1 month after the stroke, all patients had im-
Of the various neurologic deficits evaluated, only proved. Three of 4 patients who initially could not per-
central facial paresis was significantly more prevalent form the ROSS test could now be examined. Six out of
among the dysphagic patients [11/14 (79%) vs. 22/58 7 patients had ceased coughing while eating or drinking.
(38%) in the nondysphagic patients; p < 0.05]. In those Despite complaints of dysphagia and coughing dimin-
patients who could respond to the initial interview, the ished with time, the ROSS test revealed several abnormal
clinical deficits did not differ significantly between the findings in 10 (83%) patients (Table 3). The most fre-
dysphagic and nondysphagic patients (Table 1). quent abnormal findings were polyphasic laryngeal
Risk factors for stroke such as male gender, hy- movements, seen in 8 (67%) patients compared with 4
34 H. Nilsson et al.: Dysphagia in Stroke
Table 1. Clinical and prognostic findings in 100 consecutive acute stroke patientsa
p value
Dysphagic Nondysphagic Non-evaluable (Kruskal-
patients patients patients Wallis
n 4 14 n 4 58 n 4 28 test)
(33%) patients on the first examination. Respiration dur- non-evaluable patients compared with the other groups
ing swallowing was seen in 8 (67%) patients compared (Table 1), but similar in dysphagic and nondysphagic
with 5 (42%) patients on the first examination. Prolonged patients. Sixty-four patients returned home. Twenty-one
feeding interval and decreased swallowing capacity were patients were discharged to nursing homes or other com-
also frequent. munity-based facilities, and 15 patients died during their
The whole group of patients spent a median time stay in the hospital. Most unconscious patients died with-
of 13 days (6–28 days) in the acute ward and rehabilita- out regaining consciousness. No patient died from chok-
tion unit combined. The time spent in hospital did not ing.
correlate with age, and no significant differences were
found between the nonevaluable patients and patients Follow-Up after 6 Months. Six months after the
with and without dysphagia (Table 1). The Barthel index stroke, the dysphagic patients were interviewed about
at day 1 correlated with the time spent in the hospital (rs swallowing complaints. At this time, 1 patient had died
4 −0.53, p < 0.001) and with age (rs 4 −0.23, p < 0.05). from renal cancer and 2 of 13 patients had persistent
The Barthel Index was significantly lower in the non- swallowing complaints.
evaluable patients but did not differ between the dys- Among the non-evaluable patients, 18 of 28
phagic and nondysphagic patients. There was a low in- (64%) had died—12 of 14 primarily unconscious pa-
cidence of pneumonia in all groups of patients, though tients, 2 of 9 aphasic patients, and 4 of 5 demented pa-
significantly more frequent in dysphagic patients com- tients. Ten patients were still alive and were interviewed
pared with nondysphagic patients [2/14 (14%) dysphagic about swallowing complaints. However, because of per-
patients, 0/58 nondysphagic patients, p < 0.05]. sistent aphasia or severe cognitive deficits, the questions
Early outcomes were significantly poorer for the were sometimes answered by relatives or caregivers.
H. Nilsson et al.: Dysphagia in Stroke 35
Examinations
1 2 3 Reference values
Single swallow
Suction pressure (mmHg) 83 (23–145) 89 (23–145) 124 (107–164)** 78 (65–105)
Bolus volume (ml) 20 (4–36) 19 (6–32) 29 (17–36) 23 (20–26)
Suction time (secs) 1.72 (1.59–6.23)*** 1.71 (1.35–2.45)** 1.55 (1.36–1.76)** 1.11 (0.52–1.39)
Oral pharyngeal transit time (secs) 1.25 (0.43–6.05)* 0.80 (0.61–1.42)** 0.64 (0.48–1.02) 0.55 (0.30–0.73)
Time to respiration (secs) 1.38 (0.59–6.15) 0.83 (0.34–1.63) 0.48 (0.02–0.94) 0.71 (0.25–0.98)
Forced, repetitive swallow
Suction pressure (mmHg) 74 (0–172) 147 (0–213) 153 (103–233)* 97 (85–127)
Bolus volume (ml) 9 (0–15)* 15 (0–20) 17 (12–20) 18 (15–21)
Suction time (secs) 2.81 (0.63–NA)* 0.93 (0.76–NA)** 0.86 (0.67–1.05)* 0.71 (0.52–0.85)
Oral pharyngeal transit time (secs) 2.15 (0.30–NA)*** 0.32 (0.22–NA)** 0.45 (0.23–0.96)** 0.19 (0.12–0.37)
Feeding interval (secs) 1.29 (0.51–NA)*** 1.18 (0.36–NA)*** 0.86 (0.45–1.00)*** 0.27 (0.19–0.33)
Ingestion cycle time (secs) 4.77 (1.38–NA)*** 2.79 (1.30–NA)*** 2.06 (1.25–3.36)** 1.26 (0.92–1.48)
Swallowing capacity (ml/sec) 4.3 (0–9.8)*** 5.8 (0–14.7)** 9.1 (4.2–16.5)* 14.8 (13.0–17.1)
Twelve patients [5 females, age 77 (70–81) yrs] were examined on three occasions, within 24 h (examination 1), after 1 week (examination 2), and
after 1 month (examination 3). Reference values in 53 elderly non-dysphagic subjects (see methods).
Values are expressed by median and interquartile range.
NA 4 not assessable.
*p < 0.05; **p < 0.01; ***p < 0.001 compared with the reference value.
Among these 10 patients, 5 were dysphagic (all but 5 With respect to major neurologic symptoms and
initially aphasic patients). No patient had a nasogastric signs, neither hemiparesis nor the affected side correlated
tube, a gastrostomy, or parenteral nutrition at this time. with subjective dysphagia, as previously reported [7,24]
(Table 1). However, a central facial paresis was signifi-
cantly correlated with dysphagia, confirming the findings
Discussion in previous studies [2,7] (Table 1). The impact of a facial
paresis on the ability to perform the ROSS test has not
Dysphagia is defined as ‘‘difficulty in swallowing’’ [12]. been specifically addressed in earlier studies. It may be
In this study, the patient’s estimation of his or her ability argued that the deviations in the ROSS tests may primar-
to swallow was the single criterion for separating dys- ily be due to a facial paresis. However, if facial paresis
phagic from nondysphagic patients. Such self-estimation was the crucial determinator for the outcome of the
is unreliable and certainly does not exclude swallowing ROSS test results, this should primarily have influenced
dysfunction, as indicated by various other measures the oral function, providing low suction pressures and
[13,14]. In this study, only 14 of 72 (19%) patients com- low bolus volumes. On the contrary, the bolus volumes
plained of dysphagia. This is half the figure reported in were normal in most examinations. Furthermore, the suc-
previous studies on quantitative swallowing in stroke pa- tion pressures were initially within normal limits and
tients [1,2,4,5] and underlines the fact that swallowing later increased to even supranormal levels. Conse-
dysfunction is frequently subclinical [14]. quently, a facial paresis cannot be considered of major
In this study, more than two-thirds of the patients importance for the results in the test.
suffered their first symptomatic stroke. This was equally Dysphagia with frequent aspiration is associated
common among the dysphagic and nondysphagic pa- with increased risk for subsequent pneumonia [6,7,25,
tients. It has been stated that a unilateral cerebral lesion 26]. However, in this study, the frequency of pneumonia
may be associated with dysphagia [15]. In dysphagic was low, possibly reflecting the fact that most patients
stroke patients, computerized tomography of the brain suffered minor strokes, indicated by the short stay in the
frequently shows unilateral lesions [16–19]. However, hospital, and that no patient needed a nasogastric tube.
by the more sensitive MRI, lesions in the nonsymptom- The presence of dysphagia did not correlate with
atic hemisphere may frequently be revealed [18,20–22]. the Barthel indices at days 1 or 7, the length of stay in the
Consequently, the issue about the locations of lesions hospital, or the final outcome (Table 1). Numerous pre-
that may cause dysphagia is still unsettled [17–20,23]. vious studies have shown divergent results with respect
As the number of patients examined by MRI were few, to these variables. Dysphagia after stroke has been asso-
we cannot add any evidence on this particular point. ciated with lower Barthel indices [3,5,7,27], a longer stay
36 H. Nilsson et al.: Dysphagia in Stroke
Table 3. The frequency of abnormal swallowing in the ROSS test date the quantitative data, as the important issue is the
improvement over time, in which case the patients are
Examinations
their own controls.
1 2 3 The suction time and the oral pharyngeal transit
time were prolonged during single swallow, whereas
Single swallow
Low suction pressure (<35 mmHg) 3 3 0 other parameters were initially normal (Table 2). The
High suction pressure (>145 mmHg) 3 3 3 suction time was prolonged without an increase in bolus
Low bolus volume (<9.0 ml) 5 4 0 volume, indicating oral incoordination or weakness. The
Prolonged suction time (>2.5 sec) 3 3 0 oral pharyngeal transit time reflects the pharyngeal tran-
Prolonged oral pharyngeal transit time (>1.5 sec) 4 2 0
Abnormal time to respiration (not measurable sit of bolus, i.e., probably one of the most fundamental
or >2.4 sec) 3 2 1 variables for describing a safe swallow [30]. After 1
Forced, repetitive swallow month, the suction time was still prolonged and the suc-
Inability to perform the test 4 3 1 tion pressure had increased to supranormal levels, pos-
Low suction pressure (<42 mmHg) 5 4 1
High suction pressure (>243 mmHg) 1 2 2
sibly as a means of compensation [31]. The oral pharyn-
Low bolus volume (<9.3 ml) 7 5 1 geal transit time normalized with time.
Prolonged suction time (<1.5 sec) 6 4 1 More profoundly, abnormal results were seen
Prolonged oral pharyngeal transit time (>0.5 sec) 9 5 5 during forced repetitive swallow. The median suction
Prolonged ingestion cycle time (>2.6 sec) 7 6 4
pressure was normal at 24 h after the stroke despite the
Prolonged feeding interval (>0.8 sec) 6 8 6
Low swallowing capacity (<7.6 ml/sec) 7 7 6 fact that several patients could not generate the suction
Coughing (9% in the reference group) 7 5 1 pressure needed during this type of swallowing. The me-
Polyphasic laryngeal movements (34% in the dian suction pressure increased to supranormal levels at
reference group) 4 5 8 the 1 month examination in the same way as during
Respiration during swallowing (28% in the
reference group) 5 6 8
single swallow. It should be noted that we measured peak
Normal examination 0 2 2 suction pressure and not the area under the pressure
curve. The bolus volume was about half of the reference
Twelve dysphagic patients with acute stroke were examined on three
value initially but normalized thereafter. All other quan-
occasions; within 24 h (examination 1), after 1 week (examination 2),
and after 1 month (examination 3) after the stroke onset. titative parameters were abnormal when examined
within 24 h after the stroke and remained so at 1 month,
in the hospital [27,28], a lower long-term functional abil- though there were definite trends towards normalization.
ity [2], and increased risk of death [1,6]. The discrepan- Forced, repetitive swallow (stressed swallowing)
cies in results are probably explained by variable exclu- showed more pronounced and persistent deviations than
sion and inclusion criteria. When dysphagia is accompa- was seen during single swallow (Table 2). Thus, the
nied by decreased wakefulness or dementia, these factors forced, repetitive swallow seems to increase the sensi-
have to be taken into consideration when analyzing a tivity of detecting swallowing dysfunction in stroke pa-
possible correlation between dysphagia and the general tients. It may be argued that forced, repetitive swallow is
outcome. In a previous multivariate analysis of 15 pos- not a physiologic way of swallowing. However, as there
sible predictors of death and dependence at 3 months are numerous stressing factors in ‘‘normal’’ swallowing
after stroke, swallowing disturbances were found to be such as surrounding noise, people talking, time scarcity,
unimportant [29]. this way of testing may not be ‘‘nonphysiological.’’ The
The outcome may also be assessed by measuring optimal feeding situation is rare for most patients, and
the frequency of referrals to nursing homes or other com- ‘‘stressing’’ factors have to be considered and dealt with
munity-based facilities after the hospital stay. However, during a meal.
such referrals are substantially influenced by social en- The results in the ROSS test revealed that pha-
vironment and other factors not directly associated with ryngeal functions (coughing, polyphasic laryngeal move-
the stroke lesion in itself. ments, respiration during swallowing, and increased oral
The quantitative data on swallowing should be pharyngeal transit time) were more disturbed than oral
interpreted with some caution as no matched control functions (suction pressure, bolus volume, multiple swal-
group of nondysphagic patients was included, nor a con- lows to clear the oral cavity) in the initial examination
trol group of healthy elderly subjects truly matched with (Table 2). This probably indicates differences in the in-
respect to age, gender, or medication. Instead, the com- nervation complexity of the oral and pharyngeal cavities
parisons were made, regarding an elderly reference by central nervous structures. Most quantitative swallow-
group [11], on the age of the dysphagic stroke patients. ing parameters improved with time. However, some
However, the lack of a control group should not invali- swallowing abnormalities, such as polyphasic laryngeal
H. Nilsson et al.: Dysphagia in Stroke 37
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