Clinical Nutrition xxx (xxxx) xxx

Contents lists available at ScienceDirect

Clinical Nutrition
journal homepage: http://www.elsevier.com/locate/clnu

Original article

Dysphagia and tube feeding after stroke are associated with poorer
functional and mortality outcomes
Juli Thomaz Souza a, *, Priscila Watson Ribeiro b, Se

rgio Alberto Rupp de Paiva a,
Suzana Erico Tanni a, Marcos Ferreira Minicucci a, Leonardo Anto ^ nio Mamede Zornoff a,
a
Bertha Furlan Polegato , Silme
ia Garcia Zanati Bazan , Gabriel Pinheiro Modolo b,
a

Rodrigo Bazan , Paula Schmidt Azevedo a

b

a
Department of Internal Medicine, Sao Paulo State University (Unesp), Medical School, Botucatu, Brazil
b
Department of Neurology, Psychology and Psychiatry, Sao Paulo State University (Unesp), Medical School, Botucatu, Brazil

a r t i c l e i n f o s u m m a r y

Article history: Background & aims: Stroke is the leading cause of disability in adult life. Oropharyngeal dysphagia occurs
Received 25 October 2018 in 65e90% of patients, and its identification in the acute phase of stroke can prevent complications. The
Accepted 27 November 2019 aim of this study was to verify whether oropharyngeal dysphagia during stroke hospitalization is
associated with functional capacity, as assessed by the modified Rankin Scale (mRs), and mortality 90
Keywords: days after stroke.
Stroke
Materials and methods: A prospective cohort study evaluating 201 patients hospitalized in the Stroke
Oropharyngeal dysphagia
Unit was carried out. Dysphagia was evaluated during hospitalization using both a specific protocol to
Tube feeding
Disability
evaluate swallowing biomechanics and the Functional Oral Intake Scale (FOIS), in which FOIS 1e3 reflects
tube feeding, 4e5 reflects oral feeding requiring food consistency changes, and 6e7 reflects oral feeding
with no changes in food consistency. An mRs
3 at 90 days after discharge was considered disability. The
data were adjusted for the National Institute of Health Stroke Scale score, sex, age, stroke-associated
pneumonia, type of stroke, and presence of thrombolysis. The significance level was set at 5%.
Results: Of the 201 patients evaluated, 42.8% (86) who had dysphagia were older, had a higher severity of
stroke, and pneumonia rate. A FOIS score of 6e7 was a protective factor against disability (mRs
3) (OR:
0.17; CI: 0.005e0.56; p ¼ 0.004), and tube feeding use at hospital discharge increased the risk of mRs
3
(OR: 14.97; CI: 2.68e83.65; p ¼ 0.002) and mortality (OR: 9.79; CI: 2.21e43.4; p ¼ 0.003) within 90 days
after stroke. Pneumonia was the leading cause of death, however dysphagia and tube feeding at
discharge were associated with death from any cause.
Conclusion: Dysphagia or tube feeding use at discharge are markers of poor prognosis after the first
stroke. Our data suggest the importance of early evaluation of dysphagia and closely monitoring the tube
fed patients following stroke.
© 2019 Elsevier Ltd and European Society for Clinical Nutrition and Metabolism. All rights reserved.

1. Introduction
Stroke is an important health problem that directly interferes
with the morbimortality and quality of life of the individual.
Currently, stroke is the main cause of incapacity in the adult pop-
ulation, with approximately two-thirds of those affected presenting
incomplete recuperation of functionality after the event [1,2].
Defined as a sudden neurological dysfunction of vascular origin
with a rapidly evolving disturbance of cerebral function lasting
* Corresponding author.
E-mail address: jtsouz@yahoo.com.br (J.T. Souza).
more than 24 h, stroke can have an ischemic origin (80% of cases) or
a hemorrhagic origin [2,3].
Among the alterations observed, oropharyngeal dysphagia oc-
curs in 65e90% of patients and is associated with elevated morbi-
mortality along with alterations in pulmonary function, aspiration
risk, nutrition, hydration and quality of life [4,5]. However, in many
patients, dysphagia recovery occurs spontaneously in the first
weeks after ictus, and approximately 11e50% of stroke patients
may present oropharyngeal dysphagia up to six months after the
neurological injury, which increases the risk of pneumonia ac-
cording to Martino et al. [6].

https://doi.org/10.1016/j.clnu.2019.11.042
0261-5614/© 2019 Elsevier Ltd and European Society for Clinical Nutrition and Metabolism. All rights reserved.

Please cite this article as: Souza JT et al., Dysphagia and tube feeding after stroke are associated with poorer functional and mortality outcomes,
Clinical Nutrition, https://doi.org/10.1016/j.clnu.2019.11.042
2 J.T. Souza et al. / Clinical Nutrition xxx (xxxx) xxx
To prevent clinical and nutritional complications in the short
and long term and to reduce the impact of this disturbance on other
aspects of neurological rehabilitation, guidelines were developed
[7,8]. Early identification of dysphagia in the acute phase of stroke is
crucial for defining nutritional therapy, which can range from the
necessity to thicken liquids up to necessity for nasogastric tube
feeding. The aim of enteral tube feeding is to prevent dysphagia-
related complications such as aspiration pneumonia and to avoid
malnutrition resulting from inadequate nutrient intake. The most
recent guidelines for clinical nutrition in neurology show that
enteral tube feeding is indicated in the first 72 h after stroke in
cases of severe dysphagia when the condition is maintained for
more than 7 days [1,7].
Although the importance of dysphagia in the context of stroke is
known, little is understood about the influence of this alteration on
functional capacity and mortality post stroke. This study aimed to
verify the association of oropharyngeal dysphagia identified during
hospitalization for stroke with functional capacity evaluated by the
Modified Rankin Scale (mRs) as well as by mortality 90 days after
the event.
2. Materials and methods
2.1. Design and population
This study was a prospective observational study in which 201
patients were included; patients of both sexes were at least 18 years
old, hospitalized at the Stroke Unit of the Hospital of Clinics at the
UNESP Botucatu Medical School between April 2014 and November
2017, and diagnosed with stroke proven by clinical evaluation and
neuroimaging exams. Patients with other neurological diagnoses,
previous stroke, previous disability, use of pacemakers and metallic
prostheses, clinical instability/ICU admission, or pregnancy
(women) and those who did not agree to participate in the study
were excluded.
The unit is considered a level III stroke emergency center, with
capacity for 10 monitored beds, the presence of a neurologist/
neurosurgeon and thrombolysis monitoring 24 h per day, 7 days
per week, and a full multiprofessional team (physiotherapist, nurse,
dietitian, speech therapist, psychologist, pharmacist, occupational
therapist and social worker). This unit is a highly specialized
referred stroke center (tertiary care) that focuses on the acute
phase of stroke, etiological investigation, complication prevention
and rehabilitation.
The study was approved by the Research Ethics Committee of
the institution, and all patients signed the informed consent form.
2.2. Clinical and neurological evaluation
Clinical and neurological evaluations were performed by the
medical team at the time of hospital admission and consisted of
anamnesis, neuroimaging tests (computed tomography and/or
magnetic resonance), the stroke diagnosis was confirmed by the
presence of acute neurological deficit lasting more than 24 h and/or
ischemic or hemorrhagic lesion present in neuroimaging, previous
history of diseases was obtained from medical records and appli-
cation of the National Institute of Health Stroke Scale (NIHSS) for
stroke prognosis and severity. The NIHSS comprises 11 items from
neurological tests for evaluating the effect of acute stroke on the
level of consciousness, language, negligence, loss of visual field,
ocular movements, muscular strength, ataxia, dysarthria and
sensitivity loss. Deficits are classified as light (NIHSS<5), moderate
(NIHSS 5e17), severe (NIHSS 18e22) and very severe (NIHSS>22)
[3,9,10].
Please cite this article as: Souza JT et al., Dysphagia and tube feeding after stroke are associated with poorer functional and mortality outcomes,
Clinical Nutrition, https://doi.org/10.1016/j.clnu.2019.11.042
For the diagnosis of stroke-associated pneumonia, the param-
eters described by Smith et al. were utilized [11]. To verify the
occurrence of mortality we utilized death certificate in medical
records.
2.3. Evaluation of dysphagia
For dysphagia assessment, clinical signs suggestive of laryngeal
penetration or laryngotracheal aspiration were assessed by a
trained speech therapist specializing in dysphagia after stroke. The
criteria used were based on parameters in protocols found in the
instrument created by Silva in 2004 for the evaluation of dysphagia
in patients after stroke. Silva's protocol has been used in a Brazilian
population and features criteria similar to those of the Volume-
Viscosity Swallow Test (V-VST) protocol of Pere Clave
[12e14].
Initially, the integrity and functionality of the oral structures
involved in saliva swallowing and voluntary coughing were iden-
tified. Pasty, solid and liquid consistencies (four categories for liquid
foods: normal/thin, thicker liquid, nectar/honey, and paste/creamy;
and two categories for solid foods: solid and soft solid or pure
e)
were offered in volumes of 3 ml, 5 ml and ad libitum [15]. The
evolution of the food consistency and volume offered was deter-
mined by the performance of the patient. Performance during food
swallowing was observed in the oral and pharyngeal phases, with
the identification of clinical signs suggestive of laryngeal penetra-
tion or aspiration (coughing before, during or after swallowing;
“wet” vocal quality; and alterations in cervical auscultation), and
the presence or absence of dysphagia was noted based on alter-
ations in at least one of these described aspects.
The Functional Oral Intake Scale (FOIS), composed of seven
levels ranging from 1 to 7, is designed to grade oral ingestion [16].
To analyze the FOIS results, patients were grouped according to
FOIS scale score (FOIS 1e3: use of an alternative route for feeding;
4e5: oral feeding with a necessity for the modification of food
consistency; and 6e7: no modifications in food consistency).
The swallowing evaluation was performed in the first 48 h after
admission and repeated on the day of hospital discharge.
2.4. Nutritional evaluation and management
The nutritional evaluation was accomplished in the first 48 h
after hospital admission. Body weight, expressed in kg, was
measured on a Relaxmedic Your Way digital balance, with the pa-
tient barefoot and wearing only hospital pajamas. Height,
expressed in meters, was determined via a stadiometer with gra-
dations of 0.5 cm present on a Balmak 111 professional mechanical
balance.
Patients who were unable to get up from the hospital bed had
their weight and height estimated via measurement of the arm
circumference and knee height and by the formula of Chumlea and
Blackburn [17e20]. Body mass index (BMI) was calculated by the
equation described by Quetelet (BMI ¼ weight/height [2]) and
classified using the parameters of the World Health Organization
for adults and the criteria of the Pan American Health Organization
for the elderly [21e23].
Arm circumference (AC) measurement was performed using an
inelastic and inextensible measuring tape with values shown in
centimeters. For the measurement of triceps skinfold thickness
(TST), a Lange®-branded adipometer (Cambridge Scientific In-
dustries, Cambridge, Maryland, England) was used, with a constant
pressure of 10 g/mm2 on the contact surface, an accuracy of 1 mm
and a scale of 0e65 mm [24]. The value recorded was the mean of
three consecutive measurements. The arm muscle area (AMA) was
calculated using the formula AMA (cm2) ¼ [AC - (p x TST) [2]/4p],
and to adjust for the bone area and obtain the muscle area of the
 J.T. Souza et al. / Clinical Nutrition xxx (xxxx) xxx
arm without including the bone, 10 cm2 was subtracted for men
and 6.5 cm2 was subtracted for women [25].
The Nutritional Risk Screening 2002 was administered to all
patients at admission to assess the presence of undernutrition and
the risk of developing undernutrition during hospitalization [26].
All patients on tube feeding were evaluated by a dietitian, and
energy-protein calculations were performed according to the
nutrition guidelines for patients in critical care units [27]. All pa-
tients received dietary orientation at discharge following institu-
tional protocol in which we used (Simple weight-based predictive
equations e 27 a 30 kcal/kg/day and 1.2e1.5 g of protein/kg/day)
and all patients were referred to a specialized outpatient care unit.
2.5. Evaluation of functional capacity
Functional capacity was evaluated by the medical team in the
ambulatory follow-up unit 90 days after hospital discharge via the
mRs, in which patients are scored based on functional capacity:
patients with a score of 0 or 1 were considered independent with
zero or few sequelae, those with a score of 2 or 3 were those having
some sequelae but, by means of adaptations, were able to perform
previous activities and walk without aid, those with a score of 4 or 5
could not walk without aid and may have been bedridden, but did
not require a 24-hour caretaker, and a score of 6 indicated death
[7,10,28].
Patients with an mRs
3 were defined as having functional
disability.
2.6. Statistical analysis
Variables that were normally distributed are expressed as the
means ± standard deviations, whereas those that did not show a
normal distribution are expressed as the medians and 25th and
75th percentiles.
To verify the differences between the characteristics of patients
with and without dysphagia, patients with mRs<3 and
3, sur-
viving and not surviving patients Student's t test was used for
normally distributed data. For non-normally distributed data, the
ManneWhitney test was used for continuous variables, and the
chi-squared test was used for categorical variables, and the same
analysis was performed.
To verify whether the FOIS score and nasoenteral tube feeding
use at discharge are associated with the mRs Score and mortality 90
days after hospital discharge, a multivariate logistic regression
model was applied using dummy variables with FOIS score 1e3 as
the reference category. The FOIS variable was adjusted for stroke
severity (NIHSS score), sex, age, presence of stroke-associated
pneumonia, stroke type and presence of thrombolysis. Another
multivariate logistic regression model was performed for nasoen-
teral tube feeding use at discharge, adjusted by the same variables.
We selected this procedure because of collinearity between both
variables FOIS score and tube feeding use at discharge. The signif-
icance level was set at 5%.
Stata/SE v13 software was used to perform statistical analysis.
3. Results
During the study period, 1120 patients were admitted to the
Stroke Unit. Of these, 941 had a confirmed diagnosis of ischemic or
hemorrhagic stroke. Of these patients, 201 were included in the
study. The flowchart of patient recruitment and inclusion is shown
in Fig. 1.
During hospitalization, dysphagia was present in 42.8% (86) of
the individuals, and the analysis of the groups with and without
dysphagia revealed a significant difference in age, NIHSS score,
Please cite this article as: Souza JT et al., Dysphagia and tube feeding after stroke are associated with poorer functional and mortality outcomes,
Clinical Nutrition, https://doi.org/10.1016/j.clnu.2019.11.042
3
mortality and stroke-associated pneumonia. The general charac-
teristics of the population with or without dysphagia are shown in
Table 1.
Regarding the patients' nutritional status, there was no differ-
ence in the NRS 2002 score, BMI or arm muscle area between pa-
tients with mRs<3 and mRs
3, and there were no differences in
anthropometric measurements, but we found a higher percentage
of patients with nutritional risk in the group who died 90 days after
stroke. The results of these analyses are shown in Tables 2 and 3.
Of all patients evaluated those who had dysphagia upon hospital
admission, a FOIS score of 1e3 or 4e5 and nasoenteral tube feeding
use at admission and at discharge presented a statistically signifi-
cant incidence rate of mRs
3 at 90 days after stroke. Those with a
FOIS score of 6e7 during hospitalization presented a mRs<3 at 90
days after hospital discharge (Table 2).
Regarding the association between the FOIS score during hos-
pitalization, feeding tube use at discharge and mRs
3 at 90 days
after stroke, a FOIS score of 6e7 was found to be a protective factor
reducing the risk of disability (mRs
3) (OR: 0.17; 95% CI:
0.05e0.56; p ¼ 0.004). Furthermore, tube feeding use at hospital
discharge increased the risk of a mRs
3 over the same period (OR:
14.97; 95% CI: 2.68e83.65; p ¼ 0.002) (Table 4).
Regarding the association between the FOIS score during hos-
pitalization, tube feeding use at discharge with mortality 90 days
after stroke, the logistic regression model adjusted by stroke
severity (NIHSS score), sex, age, presence of stroke-associated
pneumonia, stroke type and presence of thrombolysis showed
that tube feeding use at hospital discharge increased the risk of
mortality 90 days after the cerebrovascular event (OR: 9.79; 95% CI:
2.21e43.44; p ¼ 0.003) (Table 4).
Considering the causes of death, we observed that 59% died
from pneumonia, all of them presented with dysphagia and 90%
had tube feeding at discharge. From patients who died from other
causes, 86% presented with dysphagia and 57% had tube feeding at
discharge.
KaplaneMeier survival analysis was performed to evaluate pa-
tient survival 90 days after stroke according to the FOIS score
(Fig. 2), and another curve was constructed to assess patient sur-
vival according to the presence or absence of dysphagia (Fig. 3). The
mean survival of patients separated by the FOIS score was: FOIS
1e3 (72.5 days), FOIS 4e5 (84.1 days) and FOIS 6e7 (89.3 days). The
mean survival of patients without dysphagia was 89.3 days and
with dysphagia was 78.2 days.
4. Discussion
The principal objective of this study was to verify the association
of oropharyngeal dysphagia, identified in the acute phase of stroke,
with functional capacity evaluated by the mRs and mortality 90
days after stroke. From our results, we observed that the presence
of dysphagia and nasoenteral tube feeding use during hospitaliza-
tion are associated with functional disability and mortality after
hospital discharge.
Our study showed that individuals with dysphagia were older
than those without dysphagia. It is known that aging is directly
related to the decline in swallowing functionality, thus affecting
anatomical, muscular and sensory structures. Advanced age may
favor the appearance of alterations in swallowing biomechanics in
healthy seniors, accompanied by a decrease in tactile, thermal,
gustatory and olfactory perception; reduction of flexibility in
neuromuscular control; decline in muscular strength; and
decreased rate of movements [29e31]. Similar to the age, the
severity of stroke (mean NIHSS score of 10) was greater in patients
with dysphagia.
4 J.T. Souza et al. / Clinical Nutrition xxx (xxxx) xxx

Fig. 1. Flowchart of patient inclusion between April 2014 and November 2017.

Table 1
General characteristics of patients with and without dysphagia during hospitalization for stroke and the mRs score at 90 days after stroke (n ¼ 201).

Variables Without dysphagia (n ¼ 115) With dysphagia (n ¼ 86) p

Male sex, N (%) 66 (57.4) 44 (51.2) 0.460

Age (years) 67 (54e75) 70.5 (62e79) 0.013
NIHSS 3 (1e6) 10 (5e16) <0.001
Ischemic Stroke, N (%) 109 (94.8) 77 (89.5) 0.260
Hemorrhagic Stroke, N (%) 6 (5.2) 9 (10.5) 0.260
Thrombolysis, N (%) 15 (13) 17 (20) 0.110
Mortality, N (%) 1 (0.87) 17 (19.8) <0.001
Length of stay (days) 6 (4e8) 7 (4e10.2) 0.110
Stroke-Associated Pneumonia, N (%) 3 (2.61) 17 (19.77) <0.001
NRS 2002
3 17 (14.8) 20 (23.2) 0.177
Body mass index (kg/m2) 26.8 ± 4.4 27.2 ± 5.4 0.613
Arm muscle area (cm2) 38.5 (31.5e46.8) 39.9 (31.3e46.9) 0.849
mRs
3 12 (10.4) 46 (53.5) <0.001

mRs: Modified Rankin Scale; NIHSS: National Institutes of Health Stroke Scale; NRS 2002: Nutritional Risk Screening.

Table 2
Dysphagia, FOIS score, feeding tube use and nutritional assessment of patients during hospitalization stratified by the mRs score at 90 days after stroke (n ¼ 201).

Variables mRs<3 (n ¼ 143) mRs
3 (n ¼ 58) p

Male sex, N (%) 83 (58.0) 27 (46.5) 0.185

Age (years) 68 (57.0e74.0) 74 (65.2e79.2) 0.002
NIHSS 3 (2e6) 13 (7.7e18.0) <0.001
Length of stay (days) 6 (4e8) 8 (5e11.2) 0.001
Stroke-Associated Pneumonia, N (%) 5 (3.5) 15 (25.9) <0.001
Dysphagia at admission, N (%) 40 (27.9) 46 (79.3) <0.001
FOIS, N (%) <0.001
1-3 14 (9.8) 28 (48.3)
4-5 26 (18.2) 21 (36.2)
6-7 103 (72.0) 9 (15.5)
Tube feeding at discharge, N (%) 2 (1.40) 22 (37.9) <0.001
Body mass index (kg/m2) 26.9 (24.4e29.4) 26.6 (24.4e31.2) 0.554
Arm muscle area (cm2) 38.4 (31.4e46.4) 40.9 (31.4e47.8) 0.755
NRS 2002
3 22 (15.4) 15 (25.9) 0.125

FOIS: Functional Oral Intake Scale; mRs: Modified Rankin Scale; NIHSS: National Institutes of Health Stroke Scale; NRS 2002: Nutritional Risk Screening.

When the patients were compared by stratification into 2 majority of individuals with mRs
3 presented an indicator of
groups (mRs<3, without functional disability; and mRs
3, with swallowing disorder: a) a score of 1e3 or 4e5 on the FOIS scale
functional disability) at 90 days after hospital discharge, analysis or b) dysphagia upon admission or necessity for tube feeding at
of the characteristics during hospitalization revealed that the admission or discharge. In addition, most patients with mRs<3

Please cite this article as: Souza JT et al., Dysphagia and tube feeding after stroke are associated with poorer functional and mortality outcomes,
Clinical Nutrition, https://doi.org/10.1016/j.clnu.2019.11.042
 J.T. Souza et al. / Clinical Nutrition xxx (xxxx) xxx 5

Table 3
Dysphagia, FOIS score, feeding tube use and nutritional assessment of patients during hospitalization stratified by mortality at 90 days after stroke (n ¼ 201).

Variables Surviving patients (n ¼ 183) Non surviving patients (n ¼ 18) p

Male sex, N (%) 102 (55.7) 8 (44.4) 0.503

Age (years) 68 (59e76) 77 (66.7e81) 0.010
NIHSS 4 (2e8) 19.5 (13.2e22.2) <0.001
Length of stay (days) 6 (4e9) 8.5 (3.7e12.2) 0.311
Stroke-Associated Pneumonia, N (%) 9 (4.9) 11 (61.1) <0.001
Dysphagia at admission, N (%) 69 (37.71) 17 (94.44) <0.001
FOIS, N (%) <0.001
1-3 30 (16.4) 12 (66.7)
4-5 42 (22.9) 5 (27.8)
6-7 111 (60.6) 1 (5.6)
Tube feeding at discharge, N (%) 11 (6.01) 13 (72.2) <0.001
Body mass index (kg/m2) 26.9 ± 4.6 27.6 ± 6.9 0.513
Arm muscle area (cm2) 38.8 (31.5e46.8) 40.4 (25.3e47.6) 0.832
NRS 2002
3 25 (13.7) 12 (66.7) <0.001

FOIS: Functional Oral Intake Scale; mRs: Modified Rankin Scale; NRS 2002: Nutritional Risk Screening.

Table 4
Association of FOIS score during hospitalization and tube feeding use at discharge with mRs
3 and mortality at 90 days after stroke (n ¼ 201).

mRs
3 Mortality
Variables
Simple LR Simple LR

OR CI p OR CI p

FOIS 4-5 0.404 0.17e0.96 0.039 0.298 0.09e0.93 0.038

FOIS 6-7 0.044 0.02e0.11 <0.001 0.022 0.00e0.18 <0.001
Tube feeding at discharge 14.48 2.92e71.79 0.001 19.088 4.19e87.00 <0.001

Multiple LR Multiple LR

OR CI p OR CI p

FOIS 4-5 0.49 0.17e1.39 0.181 0.61 0.14e2.64 0.507

FOIS 6-7 0.17 0.05e0.56 0.004 0.23 0.02e2.59 0.234
Tube feeding at discharge 14.97 2.68e83.65 0.002 9.79 2.21e43.44 0.003

FOIS: Functional Oral Intake Scale; mRs: Modified Rankin Scale; LR: Logistic regression.

Fig. 2. Survival of patients stratified by the FOIS score after stroke.

Fig. 3. Survival of patients with and without dysphagia after stroke.

after 90 days presented a FOIS score of 6e7 at hospital
admission.
Upon verifying the patients with an mRs
3 after 90 days, we
found that a FOIS score of 6e7 was a protective factor against severity and type, age, sex, thrombolysis or the presence of stroke-
functional disability. Similarly, the need for tube feeding use at associated pneumonia. The identification of dysphagia, adequacy of
discharge was associated with an mRs
3 independent of stroke food consistency, feeding route and rehabilitation after stroke have

Please cite this article as: Souza JT et al., Dysphagia and tube feeding after stroke are associated with poorer functional and mortality outcomes,
Clinical Nutrition, https://doi.org/10.1016/j.clnu.2019.11.042
6 J.T. Souza et al. / Clinical Nutrition xxx (xxxx) xxx
the objective of promoting the safety and efficacy of nutritional
therapy [6,32,33].
Considering that alterations in food consistency as well as
inadequate administration of an enteral diet can lead to an insuf-
ficient energy-protein supply, the patient is exposed to the risk of
malnutrition and to the complications related to a nutritional status
that impairs the post stroke rehabilitation process. Furthermore,
disease severity is associated with the appearance of complications
after ictus and can lead an individual to worse functional outcomes
[34].
Although indication for an alternative feeding route to ensure
the safety and efficacy of oral feeding in patients with dysphagia is
demonstrated in the literature and indicated in the treatment
guidelines for poststroke patients, and despite its unquestioned
importance in the treatment of diseases that prevent oral feeding,
the use of feeding tubes is a predictor of complications and reho-
spitalizations in stroke patients [7,35].
Some studies have discussed the possibility that nasoenteral
feeding tube use may elevate the risk of aspiration due to its
oropharyngeal localization, lead to the accumulation of secretions
in the hypopharynx, diminish the coughing reflex and its ability to
protect airways, and thus also neutralize gastric juice, causing
intragastric pH elevation and enabling consequent bacterial colo-
nization in the pharynx from the migration of stomach bacteria
through the tube [36]. Another aspect for consideration is that
adequate guidance to caretakers and the presence of a team
specializing in nursing care constitute decisive factors for avoiding
unfavorable outcomes in this population [7,36,37].
In our study, tube feeding use at hospital discharge increased
the risk of mRs
3 and mortality 90 days after stroke, independent
of the confounding factors already cited. Although patients were
referred for specialized outpatient care after discharge, it is not
known exactly which specific aspects in the use of an alternative in-
home feeding pathway lead an individual to present worse out-
comes than individuals with an indication for an exclusively oral
diet. We may presume that the factors involved in this phenome-
non are diverse and include the ease of contracting infections, in-
efficiency of food intake, reduction of aerodigestive tract sensitivity
with consequent risk of saliva aspiration, and psychosocial aspects
[38]. Indeed, pneumonia was a frequent cause of mortality, how-
ever dysphagia at admission and tube feeding at discharge were
related to death from pneumonia or other causes.
Furthermore, there are no data in the literature demonstrating
that patients on in-home nasoenteral tube feeding receive
adequate energy, protein and micronutrient supplies. This point is
important in the discussion, given that patients with a feeding tube
face an increased risk of functional disability independent of stroke
severity; thus, it is crucial to direct greater attention to this
population.
In this context, we observed that the early identification of
dysphagia, the assessment of swallowing performance evolution
by qualified professionals and the use of specific instruments are
indispensable in the treatment of these patients. In addition, we
verified that a simple, inexpensive and feasible bedside meth-
oddthe FOIS scaledcan aid the entire healthcare team in
attending to dysphagia in patients during hospitalization for
stroke.
5. Conclusion
Dysphagia or tube feeding use at discharge are markers of poor
prognosis after the first stroke. Our data suggest the importance of
early evaluation of dysphagia and closely monitoring the tube fed
patients following stroke.
Please cite this article as: Souza JT et al., Dysphagia and tube feeding after stroke are associated with poorer functional and mortality outcomes,
Clinical Nutrition, https://doi.org/10.1016/j.clnu.2019.11.042
Conflict of Interest
None.
CRediT authorship contribution statement
Juli Thomaz Souza: Data curation, Investigation, Formal anal-
ysis, Writing - original draft, Visualization. Priscila Watson
Ribeiro: Data curation, Investigation, Writing - original draft.

rgio Alberto Rupp de Paiva: Methodology, Formal analysis,
Se
Writing - review & editing. Suzana Erico Tanni: Formal analysis,
Writing - review & editing. Marcos Ferreira Minicucci: Writing -
review & editing. Leonardo Anto ^ nio Mamede Zornoff: Writing -
review & editing. Bertha Furlan Polegato: Writing - review &

ia Garcia Zanati Bazan: Writing - review & editing.
editing. Silme
Gabriel Pinheiro Modolo: Data curation. Rodrigo Bazan: Super-
vision, Writing - review & editing. Paula Schmidt Azevedo:
Conceptualization, Methodology, Formal analysis, Supervision,
Writing - review & editing.
Acknowledgments
This work was supported in part by the Fundaça ~o de Amparo a
Pesquisa do Estado de Sa~o Paulo (FAPESP) [scholarship 2016/11119-
07] and the Coordenaça ~o de Aperfeiçoamento de Pessoal de Nível
Superior - Brasil (CAPES) [Finance Code 001].
References
[1] Scherbakov N, Haehling S, Anker SD, Dirnagl U, Doehner W. Stroke induced
Sarcopenia: muscle wasting and disability after stroke. Int J Cardiol 2013;170:
89e94. https://doi.org/10.1016/j.ijcard.2013.10.031.
[2] Silva RA, de Melo LP, Dantas AATSG, Carmo Eul
alio M, Campos TF. Evolution of
cognitive and functional after Stroke: follow-up study. Braz J Health 2014;2:
104e14.
[3] Itaquy RB, Favero SR, Ribeiro MC, Barea LM, Almeida ST, Mancopes R.
Dysphagia and cerebrovascular accident: relationship between severity de-
gree and level of neurological impairment. J Soc Bras Fonoaudiol 2011;23:
385e9. https://doi.org/10.1590/S2179-64912011000400016.
[4] Schelp AO, Cola PC, Gatto AR, Silva RG, Carvalho LR. Incidence of oropharyn-
geal dysphagia associated with stroke in a regional hospital in S~ ao Paulo State
- Brazil. Arq Neuropsiquiatr 2004;62:503e6. S0004-282X2004000300023.
[5] Cohen DL, Roffe C, Beavan J, Blackett B, Fairfield CA, Hamdy S, et al. Post-stroke
dysphagia: a review and design considerations for future trials. Int J Stroke Off J
Int Stroke Soc 2016;11:399e411. https://doi.org/10.1177/1747493016639057.
[6] Martino R, Foley N, Bhogal S, Diamant N, Speechley M, Teasell R. Dysphagia
after stroke: incidence, diagnosis, and pulmonary complications. Stroke
2005;36:2756e63. https://doi.org/10.1161/01.STR.0000190056.76543.eb.
[7] Burgos R, Breto
n I, Cereda E, Desport JC, Dziewas R, Genton L, et al. ESPEN
guideline clinical nutrition in neurology. Clin Nutr Edinb Scotl 2018;37:
354e96. https://doi.org/10.1016/j.clnu.2017.09.003.
[8] Winstein CJ, Stein J, Arena R, Bates B, Cherney LR, Cramer SC, et al. Guidelines
for adult stroke rehabilitation and recovery: a guideline for healthcare pro-
fessionals from the American heart association/American stroke association.
Stroke 2016;47:98e169. https://doi.org/10.1161/STR.0000000000000098.
[9] Rolim CLRC. Evaluation of the effectiveness of hospital treatment of acute
stroke in National Health System: use of mortality as indicator of perfor-
mance. Available in: https://www.arca.fiocruz.br/handle/icict/2405.
[10] Caneda MA, Fernandes JG, de Almeida AG, Mugnol FE. Reliability of neuro-
logical assessment scales in patients with stroke. Arq Neuropsiquiatr 2006;64:
690e7. https://doi.org/10.1590/S0004-282X2006000400034.
[11] Smith CJ, Kishore AK, Vail A, Chamorro A, Garau J, Hopkins SJ, et al. Diagnosis
of stroke-associated pneumonia: recommendations from the pneumonia in
stroke consensus group. Stroke 2015;46:2335e40. https://doi.org/10.1161/
STROKEAHA.115.009617.
[12] Silva RG. Oropharyngeal dysphagia after stroke. In: Textbook of speech
therapy. 1 ed. Roca: Sa ~o Paulo, SP; 2004.
[13] Ribeiro PW, Cola PC, Gatto AR, da Silva RG, Luvizutto GJ, Braga GP, et al. Rela-
tionship between dysphagia, national Institutes of health stroke scale score, and
predictors of pneumonia after ischemic stroke. J Stroke Cerebrovasc Dis
2015;24:2088e94. https://doi.org/10.1016/j.jstrokecerebrovasdis.2015.05.009.
[14] Clave
P, Arreola V, Romea M, Medina L, Palomera E, Serra-Prat M. Accuracy of
the volume-viscosity swallow test for clinical screening of oropharyngeal
dysphagia and aspiration. Clin Nutr 2008;27:806e15. https://doi.org/10.1016/
j.clnu.2008.06.011.
 J.T. Souza et al. / Clinical Nutrition xxx (xxxx) xxx
[15] Steele CM, Alsanei WA, Ayanikalath S, Barbon CEA, Chen J, Cichero JAY, et al.
The influence of food texture and function: a systematic review. Dysphagia
2015;30:2e26. https://doi.org/10.1007/s00455-014-9578-x.
[16] Crary MA, Mann GDC, Groher ME. Initial psychometric assessment of a
functional oral intake scale for dysphagia in stroke patients. Arch Phys Med
Rehabil 2005;86:1516e20. https://doi.org/10.1016/j.apmr.2004.11.049.
[17] Blackburn GL, Thornton PA. Nutritional assessment of the hospitalized patient.
Med Clin N Am 1979;63:11103e15. https://doi.org/10.1016/S0025-7125(16)
31663-7.
[18] Callaway CW, Chumlea WC, Bouchard C, Himes JH, Lohman TG, Martin AD,
et al. Circumferences. Anthr Stand Ref Man 1988:39e54.
[19] Chumlea WC, Roche AF, Steinbaugh ML. Estimating stature from knee height
for persons 60 to 90 years of age. J Am Geriatr Soc 1985;33:116e20.
[20] Chumlea WC, Guo S, Roche AF, Steinbaugh ML. Prediction of body weight for
the nonambulatory elderly from anthropometry. J Am Diet Assoc 1988;88:
564e8.
[21] Garrow JS, Webster J. Quetelet's index (W/H2) as a measure of fatness. Int J
Obes 1985;9:147e53.
[22] OPAS. Organizacio
n Panamericana de la Salud. Reunio
n del Comite
^ Asesor de
Investigaciones en Salud. Encuestra Multice ^ntrica. Salud Beinestary Enveje-
cimeiento (SABE) en Ame
rica Latina e el Caribe. 2001. Available in: http://
www1.paho.org/Spanish/HDP/HDR/CAIS-01-05.PDF.
[23] WHO. Obesity: preventing and managing the global epidemic. Report of a
WHO consultation. World Health Organ Tech Rep Ser 2000;894:1e253.
[24] Harrison GG, Buskirk EK, Carter JEL, Ohmston JFE, Lohman TG, Pollock ML,
et al. Skinfold thicknesses and measurements technique. In: Lohman TG,
Roche AF, Martorell R, editors. Anthropometric standardizing reference
manual. Champaign. Il: Human Kinetics Books; 1991. p. 55e80.
[25] Frisancho AR. Anthropometric standards for the assessment of growth and
nutritional status. Michigan: The University of Michigan Press; 1990.
p. 48e53.
[26] Kondrup J, Rasmussen HH, Hamberg O, Stanga Z, Ad Hoc ESPEN Working
Group. Nutritional Risk Screening (NRS 2002): a new method based on an
analysis of controlled clinical trials. Clin Nutr 2003;22:321e36. https://
doi.org/10.1016/S0261-5614(02)00214-5.
[27] Singer P, Blaser AR, Berger MM, Alhazzani W, Calder PC, Casaer MP, et al.
ESPEN guideline on clinical nutrition in the intensive care unit. Clin Nutr
2019;38:48e79. https://doi.org/10.1016/j.clnu.2018.08.037.
Please cite this article as: Souza JT et al., Dysphagia and tube feeding after stroke are associated with poorer functional and mortality outcomes,
Clinical Nutrition, https://doi.org/10.1016/j.clnu.2019.11.042
7
[28] Baggio JAO, Santos-Pontelli TEG, Cougo-Pinto PT, Camilo M, Silva NF,
Antunes P, et al. Validation of a structured interview for telephone assessment
of the modified Rankin Scale in Brazilian stroke patients. Cerebrovasc Dis
Basel Switz 2014;38:297e301. https://doi.org/10.1159/000367646.
[29] Gleeson DC. Oropharyngeal swallowing and aging: a review. J Commun Dis-
ord 1999;32:373e95. https://doi.org/10.1016/S0021-9924(99)00017-9.
[30] Logemann JA, Curro FA, Pauloski B, Gensler G. Aging effects on oropharyngeal
swallow and the role of dental care in oropharyngeal dysphagia. Oral Dis
2013;19:733e7. https://doi.org/10.1111/odi.12104.
[31] Liu L, Xiao Y, Zhang W, Yao L, Gao X, Chandan S, et al. Functional changes of
neural circuits in stroke patients with dysphagia: a meta-analysis. J Evid Based
Med 2017;10:189e95. https://doi.org/10.1111/jebm.12242.
[32] Arnold M, Liesirova K, Broeg-Morvay A, Meisterernst J, Schlager M, Mono ML,
et al. Dysphagia in acute stroke: incidence, burden and impact on clinical
outcome. PLoS One 2016;11:e0148424. https://doi.org/10.1371/journal.p
one.0148424.
[33] Ickenstein GW, Ho €hlig C, Prosiegel M, Koch H, Dziewas R, Bodechtel U, et al.
Prediction of outcome in neurogenic oropharyngeal dysphagia within 72
hours of acute stroke. J Stroke Cerebrovasc Dis Off J Natl Stroke Assoc
2012;21:569e76. https://doi.org/10.1016/j.jstrokecerebrovasdis.2011.01.004.
[34] Bannerman E, McDermott K. Dietary and fluid intakes of older adults in care
homes requiring a texture modified diet: the role of snacks. J Am Med Dir
Assoc 2011;12:234e9. https://doi.org/10.1016/j.jamda.2010.06.001.
[35] Kernan WN, Ovbiagele B, Black HR, Bravata DM, Chimowitz MI,
Ezekowitz MD, et al. Guidelines for the prevention of stroke in patients with
stroke and transient ischemic attack: a guideline for healthcare professionals
from the American Heart Association/American Stroke Association. Stroke
2014;45:2160e236. https://doi.org/10.1161/STR.0000000000000024.
[36] Gomes GF, Pisani JC, Macedo ED, Campos AC. The nasogastric feeding tube as a
risk factor for aspiration and aspiration pneumonia. Curr Opin Clin Nutr Metab
Care 2003;6:327e33. https://doi.org/10.1097/01.mco.0000068970.34812.8b.
[37] Wilmskoetter J, Simpson KN, Bonilha HS. Hospital readmissions of stroke
patients with percutaneous endoscopic gastrostomy feeding tubes. J Stroke
Cerebrovasc Dis 2016;25:2535e42. https://doi.org/10.1016/j.jstrokecereb
rovasdis.2016.06.034.
[38] FOOD Trial Collaboration. Poor nutritional status on admission predicts poor
outcomes after stroke: observational data from the FOOD trial. Stroke
2003;34:1450e6. https://doi.org/10.1161/01.STR.0000074037.49197.8C.