Keywords: Deglutition - Deglutition Disorders - Stroke - Outcome Assessment, Health Care
Palavras-chave: Deglutição - Transtornos de Deglutição - Acidente Vascular Cerebral - Avaliação de
Resultados em Cuidados de Saúde
INTRODUCTION
Dysphagia is common in post-stroke individuals[1 ] and contributes to worse long-term outcomes, including functional dependence[2 ],[3 ],[4 ],[5 ], institutionalization[2 ],[4 ],[5 ],[6 ],[7 ] and increased mortality[2 ],[3 ],[4 ],[5 ],[6 ],[7 ],[8 ],[9 ]. Some studies with stroke individuals have demonstrated that the presence of dysphagia
is associated with age[2 ],[5 ],[6 ],[7 ],[8 ],[10 ], female sex[2 ],[5 ],[6 ], stroke severity[2 ],[4 ],[5 ],[7 ],[8 ],[11 ], hemorrhagic stroke[6 ],[8 ], lesion in the left hemisphere[9 ], stroke involving total anterior circulation[6 ], stroke with involvement of the middle cerebral artery[8 ], brain stem lesion[10 ], prior stroke[5 ],[9 ],[12 ], hypertension[2 ],[5 ], diabetes[10 ] and atrial fibrillation[2 ],[6 ],[8 ]. However, the factors associated with dysphagia in stroke individuals are not well
established[5 ],[12 ].
In Brazil, the frequency of dysphagia in individuals with stroke is high compared
to developed countries[13 ]. Nevertheless, only two Brazilian studies were conducted prospectively with a large
sample of stroke individuals to identify the factors associated with dysphagia and
the impact of dysphagia on this population[9 ],[14 ]. In addition, these studies have explored few risk factors and did not report blinded
assessments of outcomes.
Knowledge about factors associated with dysphagia and the impact of dysphagia on outcomes
is important for stroke teams because it can provide information on what to expect
in the assessment and prognosis of these individuals, and therefore may contribute
to the planning of early preventive measures.
Thus, the aims of this study were to investigate the factors associated with dysphagia
and to assess the impact of dysphagia on sub-acute clinical outcomes in stroke individuals
in a large cohort prospectively and with blinded assessments of outcomes.
METHODS
Design of the study
To investigate the frequency of dysphagia and its associated factors, we performed
a cross-sectional study, and to assess the impact of dysphagia on outcomes, we conducted
a cohort study.
Subjects
All consecutive eligible individuals admitted to the emergency unit of a tertiary
academic Brazilian hospital were approached and gave consent. Eligible individuals
were those that met the following criteria: age ≥18 years and had a medical diagnosis
of any stroke event confirmed by CT scan and/or MRI findings. Individuals with a transient
ischemic attack, subarachnoid hemorrhage, cerebral venous thrombosis, hemorrhagic
stroke with secondary cause, non-acute stroke (>10 days after last seen normal), or
those who did not consent were excluded. This study was approved by the Ethics Committee
of our institution. Individuals that were discharged from hospital before swallowing
assessment or those that were not able to be assessed due to clinical conditions were
also excluded.
Data source
Demographic and clinical information
All individuals were initially screened by research coordinators as part of the admitting
process with an institution-specific stroke registry. The data were collected prospectively
as per standard of care and included age, sex, premorbid functional status, potential
risk factors for stroke, admission/discharge dates, stroke details, tube feeding,
overall function, and in-hospital death.
Stroke characteristics
The neuroimaging analysis was performed by neurovascular neurologists blinded to dysphagia
diagnosis. The software used for analysis was Weasis v2.03. Exams were classified
according to stroke type and hemisphere injured. Ischemic strokes were classified
into “lacunar”, “cerebellar”, “cortical” and “watershed” and according to cerebral
vascular territories in anterior circulation - media and anterior cerebral arteries,
posterior circulation - vertebral arteries, basilar, and posterior cerebral. Stroke
characteristics were analyzed independently and the same individual may have been
classified into more than one topography, according to the lesion location. All individuals
were also classified according to Bamford classification (total anterior circulation
syndrome - TACS; partial anterior circulation syndrome - PACS; lacunar syndrome -
LACS; posterior circulation syndrome - POCS)[15 ].
Swallowing assessment
Swallowing was evaluated by speech language pathologists (SLP) at the bedside using
the Volume-Viscosity Swallow Test (V-VST)[16 ]. We mixed 100 mL of water with three measures of a xanthan-based thickener to make
the pudding consistency, and with one measure to make the nectar consistency. We used
increasing volumes of 5-, 10-, and 20-mL boluses in a progression of increasing difficulty
as proposed in the V-VST, and the presence of dysphagia was determined according to
the test results. Any sign or symptom of swallowing impairment (oral residue, reduced
efficiency of labial seal, fractional swallow, and pharyngeal residue) or any sign
of unsafe swallowing (cough, change in voice quality and decrease in oxygen saturation
≥3%) was considered dysphagia.
Outcomes
Individuals were assessed for functional status during an outpatient clinic visit
three months after stroke onset by raters blinded to dysphagia diagnosis during acute
hospital stay. Data from individuals that died were obtained from hospital records.
Functional outcomes were functional disability, assessed using the modified Rankin
scale[17 ] (mRS; 0-2: no functional dependence; 3-6: functional dependence or death), functional
dependence, assessed using the Barthel Index[17 ] and Functional Independence Measure (FIM)[18 ], and use of tube feeding. Individuals were also asked if they had received any rehabilitation
since their stroke onset. Individuals who could not attend their outpatient clinic
appointment were contacted by phone for details to inform the mRS score, the use of
tube feeding and rehabilitation.
Data analysis
Clinical and demographic information were summarized descriptively using frequencies,
percentages, means, standardized deviations (SD), medians and interquartile ranges
(IQ). Data from individuals with and without dysphagia were compared using the t-test
or Mann-Whitney test for continuous variables and chi-square or Fisher’s exact test
for categorical variables. Multivariate logistic regression was applied using a backward
stepwise method to identify the factors associated with dysphagia and to determine
if dysphagia was an independent predictor of death and or of functional dependence
at three months post-stroke. All variables that presented a statistically significant
difference in the univariate analysis and were potential associated factors for dysphagia
and for functional dependence or death were included in the multivariate logistic
regression model. We used the threshold of 0.05 for statistical significance for all
analyses. Statistical analyses were performed using the software SPSS version 20.
RESULTS
A total of 831 individuals with suspected stroke were admitted to hospital between
April 2015 and September 2016. Of these, 305 individuals were included based on inclusion
and exclusion criteria ([Figure 1 ]). The mean age of individuals was 63.6±13.3 years, 168 (55.1%) were male, 285 (93.4%)
had an ischemic stroke, median National Institutes of Health Stroke Scale (NIHSS)
score at admission was 74-13 , and 18 (5.9%) individuals died within three months after stroke. The mean time from
stroke to swallowing assessment was 4.2±4.1 days.
Figure 1 Flowchart of the study.
Factors associated with dysphagia
One hundred and thirty-eight (45.2%) individuals had dysphagia, 54.7% of which had
only safety impairments, 9.4% had only efficacy impairments, and 35.9% had both safety
and efficacy impairments. Cough was the most frequent sign of impaired safe swallow
(47.3%) and reduced efficiency of labial seal was the most frequent sign of impaired
efficacy (41.8%). Dysphagic individuals were older (65.8±13.3 vs. 61.9±13.0 years;
p=0.010) and had higher stroke severity at hospital admission (95-17 vs. 53-10 ; p<0.001) than comparable individuals without dysphagia. They were also more likely
to have obstructive sleep apnea (OSA) (12.3 vs. 3%; p=0.002) and TACS (18.8 vs. 9.6%;
p=0.019) and less likely to have LACS (21.7% vs. 36.5%; p=0.005) than individuals
without dysphagia ([Table 1 ]). In the multivariate analysis, age (OR=1.02; 95%CI 1.00-1.04; p=0.017), medical
history of OSA (OR=5.13; 95%CI 1.74-15.15; p=0.003), and stroke severity at hospital
admission (OR=1.10; 95%CI 1.06-1.15; p<0.001) were independently associated with dysphagia
([Table 2 ]).
Table 1
Baseline characteristics of patients with and without dysphagia.
General n=305
Dysphagia
Yes n=138
No n=167
p-value
Age (years), mean±SD
63.6±13.3
65.8±13.3
61.9±13.0
0.010*
Male sex
168 (55.1%)
77 (55.8%)
91 (54.5%)
0.819
Pre-event functional dependence
17 (5.6%)
10 (7.2%)
7 (4.2%)
0.252
Prior stroke
91 (29.8%)
43 (31.2%)
48 (28.7%)
0.646
Hypertension
232 (76.1%)
98 (71.0%)
134 (80.2%)
0.060
Diabetes
99 (32.5%)
47 (34.1%)
52 (31.1%)
0.588
Dyslipidemia
107 (35.1%)
46 (33.3%)
61 (36.5%)
0.561
Obstructive sleep apnea
22 (7.2%)
17 (12.3%)
5 (3.0%)
0.002*
Atrial fibrillation
58 (19.0%)
28 (20.3%)
30 (18.0%)
0.606
Cardiac insufficiency
37 (12.1%)
21 (15.2%)
16 (9.6%)
0.133
Obesity
66 (22.5%)
31 (23.0%)
35 (22.2%)
0.841
Smoking in the past year
82 (30.0%)
44 (34.4%)
40 (26.3%)
0.143
Alcoholism in the past year
119 (42.8%)
50 (39.4%)
69 (45.7%)
0.288
GCS at admission, median [IQ]
15 [14-15]
15 [14-15]
15 [14-15]
0.144
NIHSS at admission, median [IQ]
7 [4-13]
9 [5-17]
5 [3-10]
<0.001*
Thrombolysis or thrombectomy
92 (30.2%)
47 (34.1%)
45 (26.9%)
0.178
Thrombolysis
82 (26.9%)
42 (51.2%)
40 (48.8%)
0.180
Thrombectomy
37 (12.1%)
20 (54.1%)
17 (45.9%)
0.290
Hemorrhagic stroke
20 (6.6%)
11 (8.0%)
9 (5.4%)
0.365
Right hemisphere
137 (52.7%)
64 (55.2%)
73 (50.7%)
0.472
Bamford TACS
42 (13.8%)
26 (18.8%)
16 (9.6%)
0.019*
Bamford PACS
131 (43.0%)
61 (44.2%)
70 (41.9%)
0.688
Bamford LACS
91 (29.8%)
30 (21.7%)
61 (36.5%)
0.005*
Bamford POCS
40 (13.1%)
20 (14.5%)
20 (12.0%)
0.517
Anterior circulation
263 (86.2%)
118 (85.5%)
145 (86.8%)
0.739
Watershed
13 (4.6%)
5 (3.9%)
8 (5.1%)
0.651
Cerebellum
18 (6.3%)
6 (4.7%)
12 (7.6%)
0.322
Cortical
125 (43.9%)
57 (44.9%)
68 (43.0%)
0.755
Lacuna
80 (26.2%)
31 (22.5%)
49 (29.3%)
0.174
*statistically significant; GCS: Glasgow Coma Scale; NIHSS: National Institutes of
Health Stroke Scale; IQ: interquartile range; SD: standardized deviation; TACS: total anterior circulation
syndrome; PACS: partial anterior circulation syndrome; LACS: lacunar syndrome; POCS:
Posterior circulation syndrome.
Table 2
Multivariate analysis of dysphagia predictors.
OR
95%CI
p-value
Step 1
Age
1.02
1.00-1.04
0.021
Stroke severity
1.09
1.04-1.14
<0.001
Obstructive sleep apnea
5.51
1.84-16.49
0.002
TACS
1.00
0.45-2.20
0.986
LACS
0.66
0.37-1.17
0.157
Step 2
Age
1.02
1.00-1.04
0.021
Stroke severity
1.09
1.05-1.14
<0.001
Obstructive sleep apnea
5.50
1.84-16.48
0.002
LACS
0.66
0.37-1.16
0.151
Step 3
Age
1.02
1.00-1.04
0.017
Stroke severity
1.10
1.06-1.14
<0.001
Obstructive sleep apnea
5.13
1.73-15.14
0.003
OR: Odds Ratio ; 95%CI: 95% confidence interval; TACS: total anterior circulation syndrome; LACS:
lacunar syndrome.
Outcomes
Dysphagic individuals had longer length of hospital stay (10.0±10.2 vs. 6.7±7.8 days;
p=0.001), used tube feeding during hospitalization (65.1 vs. 18%), had functional
dependence at discharge (mRS 3-6: 54.3 vs. 22.8%), did rehabilitation (58.2% vs. 31.8%),
and used tube feeding (15.5 vs. 0.9%) within three months more often (p<0.001 for
all comparisons) than individuals without dysphagia ([Table 3 ]). They also were more likely to die (9.4 vs. 3%; p=0.010) and were more functionally
dependent (Barthel: 71.1±33.1 vs. 91.0±16.9; FIM: 92.3±35.1 vs. 114.4±19.8; p<0.001)
at three months ([Figure 2 ]). Presence of dysphagia (OR=3.78; 95%CI 2.16-6.61; p<0.001) and stroke severity
as measure by the NIHSS scale (OR=1.05; 95%CI 1.00-1.09; p=0.024) were independently
associated with death and functional dependence at three months ([Table 4 ]).
Figure 2 Modified Rankin Scale score (0 to 6; 0=no symptoms, 6=dead) at three months post-stroke
in individuals with and without dysphagia diagnosed in the acute phase.
Table 3
Outcomes of patients with and without dysphagia.
General (n=305)
Dysphagia
Yes (n=138)
No (n=167)
p-value
Length of stay (days), mean±SD
8.2±9.0
10.0±10.2
6.7±7.8
0.001
Use of tube feeding in hospital
107 (40.4%)
82 (65.1%)
25 (18.0%)
<0.001
mRS score at discharge
0-2
151 (53.0%)
41 (32.3%)
110 (69.6%)
<0.001
3-6
134 (47.0%)
86 (67.7%)
48 (30.4%)
In-hospital death
3 (1.0%)
2 (1.4%)
1 (0.6%)
0.454
mRS score at 3 months
0-2
192 (63.0%)
63 (45.7%)
129 (77.2%)
<0.001
3-6
113 (37.0%)
75 (54.3%)
38 (22.8%)
Barthel at 3 months, mean±SD
82.4±27.0
71.1±33.1
91.0±16.9
<0.001
FIM at 3 months, mean±SD
104.9±29.5
92.3±35.1
114.4±19.8
<0.001
Death within 3 months
18 (5.9%)
13 (9.4%)
5 (3.0%)
0.018
Rehabilitation within 3 months
88 (43.8%)
53 (58.2%)
35 (31.8%)
<0.001
SLP therapy
22 (12.0%)
14 (18.2%)
8 (7.5%)
0.029
Physiotherapy
66 (35.9%)
35 (46.1%)
31 (28.7%)
0.016
Use of tube feeding within 3 months
14 (7.4%)
13 (15.5%)
1 (0.9%)
<0.001
SD: standard deviation; mRS: modified Rankin Scale; FIM: functional Independence Measure;
SLP: speech and language pathology.
Table 4
Multivariate analysis for predictors of functional dependence or death at three months.
OR
95%CI
p-value
Step 1
Age
1.01
0.99-1.04
0.181
Stroke severity
1.04
0.99-1.09
0.157
TACS
1.29
0.55-3.00
0.555
LACS
0.69
0.35-1.35
0.279
Dysphagia
3.52
2.00-6.20
<0.001
Step 2
Age
1.01
0.99-1.04
0.169
Stroke severity
1.04
1.00-1.09
0.072
LACS
0.67
0.35-1.31
0.243
Dysphagia
3.53
2.00-6.20
<0.001
Step 3
Age
1.01
0.99-1.04
0.153
Stroke severity
1.05
1.01-1.10
0.022
Dysphagia
3.60
2.05-6.32
<0.001
Step 4
Stroke severity
1.05
1.01-1.09
0.024
Dysphagia
3.78
2.16-6.61
<0.001
TACS: total anterior circulation syndrome; LACS: lacunar syndrome.
DISCUSSION
The frequency of dysphagia identified in our study is consistent with two recent cohort
studies[14 ],[15 ], one of them in Brazil[14 ]. However, it was lower than the frequency of dysphagia estimated in a systematic
review of Brazil [13], probably because we did not include severely affected individuals
who could not be evaluated in the first days after the stroke.
The results of our study confirm the association of dysphagia with age and stroke
severity reported in the literature[5 ],[11 ],[14 ],[19 ],[20 ],[21 ]. Thus, among the many factors associated with dysphagia in stroke individuals, age
and stroke severity are strong risk factors for dysphagia. Therefore, older individuals
and those with more severe strokes should be monitored more carefully due to the risk
of developing dysphagia and its associated complications.
An important finding in our study was the association between OSA and dysphagia. OSA
is an important risk factor for stroke[22 ],[23 ],[24 ], being common in this population. It is also associated with changes in swallowing[25 ],[26 ],[27 ],[28 ]. However, to date, no study has investigated whether individuals with stroke and
OSA are at greater risk of developing dysphagia than individuals with stroke without
OSA. In our study, OSA was an independent risk factor for dysphagia, so these individuals
are more likely to develop dysphagia after a stroke. Thus, all stroke patients with
OSA should be assessed for orofacial muscles and swallowing, as they have more chances
to have dysphagia compared to stroke individuals without OSA.
Our study also confirmed that dysphagia in stroke patients in Brazil has an important
impact on length of stay, mortality, and outcomes[9 ],[14 ]. This highlights the importance of promoting adequate management strategies for
dysphagia in Brazilian guidelines to avoid poor outcomes in this population.
Thus, this study provides important epidemiological data for stroke care in Brazil
to help identify individuals at risk for dysphagia and to demonstrate the impact of
dysphagia on this population. This highlights the importance of promoting better management
strategies for these individuals to prevent poor outcomes. These strategies include
screening for early detection of dysphagia and referring individuals who do not have
it for evaluation by speech therapists.
There are some limitations in this study. Data about risk factors for stroke were
collected from the medical history reported by the individual or his or hers caregiver.
However, the presence of risk factors such as OSA was considered only if the diagnosis
was confirmed or if the person was taking medication for the condition. We did not
evaluate more severe stroke individuals because we only assessed individuals in the
first few days after hospital admission, and severe patients could not be assessed
at that time. Despite this, we could identify a high rate of dysphagia and associations
with poor outcomes.
Despite these limitations, our study was performed prospectively and consecutively,
with a large cohort of stroke individuals, and all individuals were assessed in a
standardized way by SLP. The outcomes were assessed blindly for dysphagia diagnosis,
which contributes to the reliability of the observed results.
This study confirms that dysphagia is frequent in post-stroke individuals and is a
strong predictor of death or functional dependence. Stroke teams should be alert for
increased risk of dysphagia in the elderly or those with OSA. Brazilian health managers
should be aware of the need to implement strategies for early detection and management
of dysphagia to avoid poor outcomes.
