Dysphagia and tube feeding after stroke are associated with poorer functional and mortality outcomes

Dysphagia and tube feeding after stroke are associated with poorer functional and mortality outcomes

Clinical Nutrition xxx (xxxx) xxx Contents lists available at ScienceDirect Clinical Nutrition journal homepage: http://www.elsevier.com/locate/clnu...

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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 rgio Alberto Rupp de Paiva a, Juli Thomaz Souza a, *, Priscila Watson Ribeiro b, Se ^ nio Mamede Zornoff a, Suzana Erico Tanni a, Marcos Ferreira Minicucci a, Leonardo Anto a a ia Garcia Zanati Bazan , Gabriel Pinheiro Modolo b, Bertha Furlan Polegato , Silme b Rodrigo Bazan , Paula Schmidt Azevedo a a b

Department of Internal Medicine, Sao Paulo State University (Unesp), Medical School, Botucatu, Brazil 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: Received 25 October 2018 Accepted 27 November 2019

Background & aims: Stroke is the leading cause of disability in adult life. Oropharyngeal dysphagia occurs in 65e90% of patients, and its identification in the acute phase of stroke can prevent complications. The 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 days after stroke. Materials and methods: A prospective cohort study evaluating 201 patients hospitalized in the Stroke Unit was carried out. Dysphagia was evaluated during hospitalization using both a specific protocol to 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 mRs3 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 (mRs3) (OR: 0.17; CI: 0.005e0.56; p ¼ 0.004), and tube feeding use at hospital discharge increased the risk of mRs3 (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.

Keywords: Stroke Oropharyngeal dysphagia Tube feeding Disability

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 population, 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: [email protected] (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 occurs in 65e90% of patients and is associated with elevated morbimortality 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 according 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

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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 dysphagiarelated 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 application 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].

For the diagnosis of stroke-associated pneumonia, the parameters 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 [12e14]. Viscosity Swallow Test (V-VST) protocol of Pere Clave Initially, the integrity and functionality of the oral structures involved in saliva swallowing and voluntary coughing were identified. Pasty, solid and liquid consistencies (four categories for liquid foods: normal/thin, thicker liquid, nectar/honey, and paste/creamy; e) and two categories for solid foods: solid and soft solid or pure were offered in volumes of 3 ml, 5 ml and ad libitum [15]. The evolution of the food consistency and volume offered was determined 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 penetration 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 alterations 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 patient barefoot and wearing only hospital pajamas. Height, expressed in meters, was determined via a stadiometer with gradations 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 Industries, 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

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

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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 patients received dietary orientation at discharge following institutional 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 mRs3 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, surviving 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 nasoenteral 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 significance 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,

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mortality and stroke-associated pneumonia. The general characteristics of the population with or without dysphagia are shown in Table 1. Regarding the patients' nutritional status, there was no difference in the NRS 2002 score, BMI or arm muscle area between patients with mRs<3 and mRs3, 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 significant incidence rate of mRs3 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 hospitalization, feeding tube use at discharge and mRs3 at 90 days after stroke, a FOIS score of 6e7 was found to be a protective factor reducing the risk of disability (mRs3) (OR: 0.17; 95% CI: 0.05e0.56; p ¼ 0.004). Furthermore, tube feeding use at hospital discharge increased the risk of a mRs3 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 hospitalization, 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 patient survival 90 days after stroke according to the FOIS score (Fig. 2), and another curve was constructed to assess patient survival 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 hospitalization 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.

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

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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 (%) Age (years) NIHSS Ischemic Stroke, N (%) Hemorrhagic Stroke, N (%) Thrombolysis, N (%) Mortality, N (%) Length of stay (days) Stroke-Associated Pneumonia, N (%) NRS 2002  3 Body mass index (kg/m2) Arm muscle area (cm2) mRs3

66 (57.4) 67 (54e75) 3 (1e6) 109 (94.8) 6 (5.2) 15 (13) 1 (0.87) 6 (4e8) 3 (2.61) 17 (14.8) 26.8 ± 4.4 38.5 (31.5e46.8) 12 (10.4)

44 (51.2) 70.5 (62e79) 10 (5e16) 77 (89.5) 9 (10.5) 17 (20) 17 (19.8) 7 (4e10.2) 17 (19.77) 20 (23.2) 27.2 ± 5.4 39.9 (31.3e46.9) 46 (53.5)

0.460 0.013 <0.001 0.260 0.260 0.110 <0.001 0.110 <0.001 0.177 0.613 0.849 <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)

mRs3 (n ¼ 58)

p

Male sex, N (%) Age (years) NIHSS Length of stay (days) Stroke-Associated Pneumonia, N (%) Dysphagia at admission, N (%) FOIS, N (%) 1-3 4-5 6-7 Tube feeding at discharge, N (%) Body mass index (kg/m2) Arm muscle area (cm2) NRS 2002  3

83 (58.0) 68 (57.0e74.0) 3 (2e6) 6 (4e8) 5 (3.5) 40 (27.9)

27 (46.5) 74 (65.2e79.2) 13 (7.7e18.0) 8 (5e11.2) 15 (25.9) 46 (79.3)

0.185 0.002 <0.001 0.001 <0.001 <0.001 <0.001

14 (9.8) 26 (18.2) 103 (72.0) 2 (1.40) 26.9 (24.4e29.4) 38.4 (31.4e46.4) 22 (15.4)

28 (48.3) 21 (36.2) 9 (15.5) 22 (37.9) 26.6 (24.4e31.2) 40.9 (31.4e47.8) 15 (25.9)

<0.001 0.554 0.755 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 groups (mRs<3, without functional disability; and mRs3, with functional disability) at 90 days after hospital discharge, analysis of the characteristics during hospitalization revealed that the

majority of individuals with mRs3 presented an indicator of swallowing disorder: a) a score of 1e3 or 4e5 on the FOIS scale or b) dysphagia upon admission or necessity for tube feeding at 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

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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 (%) Age (years) NIHSS Length of stay (days) Stroke-Associated Pneumonia, N (%) Dysphagia at admission, N (%) FOIS, N (%) 1-3 4-5 6-7 Tube feeding at discharge, N (%) Body mass index (kg/m2) Arm muscle area (cm2) NRS 2002  3

102 (55.7) 68 (59e76) 4 (2e8) 6 (4e9) 9 (4.9) 69 (37.71)

8 (44.4) 77 (66.7e81) 19.5 (13.2e22.2) 8.5 (3.7e12.2) 11 (61.1) 17 (94.44)

0.503 0.010 <0.001 0.311 <0.001 <0.001 <0.001

30 (16.4) 42 (22.9) 111 (60.6) 11 (6.01) 26.9 ± 4.6 38.8 (31.5e46.8) 25 (13.7)

12 (66.7) 5 (27.8) 1 (5.6) 13 (72.2) 27.6 ± 6.9 40.4 (25.3e47.6) 12 (66.7)

<0.001 0.513 0.832 <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 mRs3 and mortality at 90 days after stroke (n ¼ 201). Variables

FOIS 4-5 FOIS 6-7 Tube feeding at discharge

mRs3

Mortality

Simple LR

Simple LR

OR

CI

p

OR

CI

p

0.404 0.044 14.48

0.17e0.96 0.02e0.11 2.92e71.79

0.039 <0.001 0.001

0.298 0.022 19.088

0.09e0.93 0.00e0.18 4.19e87.00

0.038 <0.001 <0.001

Multiple LR

FOIS 4-5 FOIS 6-7 Tube feeding at discharge

Multiple LR

OR

CI

p

OR

CI

p

0.49 0.17 14.97

0.17e1.39 0.05e0.56 2.68e83.65

0.181 0.004 0.002

0.61 0.23 9.79

0.14e2.64 0.02e2.59 2.21e43.44

0.507 0.234 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.

after 90 days presented a FOIS score of 6e7 at hospital admission. Upon verifying the patients with an mRs3 after 90 days, we found that a FOIS score of 6e7 was a protective factor against functional disability. Similarly, the need for tube feeding use at discharge was associated with an mRs3 independent of stroke

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

severity and type, age, sex, thrombolysis or the presence of strokeassociated pneumonia. The identification of dysphagia, adequacy of 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

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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 insufficient 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 rehospitalizations 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 colonization 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 mRs3 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 inhome feeding pathway lead an individual to present worse outcomes than individuals with an indication for an exclusively oral diet. We may presume that the factors involved in this phenomenon are diverse and include the ease of contracting infections, inefficiency 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, however 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 methoddthe 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.

Conflict of Interest None. CRediT authorship contribution statement Juli Thomaz Souza: Data curation, Investigation, Formal analysis, 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 ^ nio Mamede Zornoff: Writing review & editing. Leonardo Anto review & editing. Bertha Furlan Polegato: Writing - review & ia Garcia Zanati Bazan: Writing - review & editing. editing. Silme Gabriel Pinheiro Modolo: Data curation. Rodrigo Bazan: Supervision, Writing - review & editing. Paula Schmidt Azevedo: Conceptualization, Methodology, Formal analysis, Supervision, Writing - review & editing. Acknowledgments ~o de Amparo a  This work was supported in part by the Fundaça ~o Paulo (FAPESP) [scholarship 2016/11119Pesquisa do Estado de Sa ~o de Aperfeiçoamento de Pessoal de Nível 07] and the Coordenaça 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 degree 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 oropharyngeal 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. n I, Cereda E, Desport JC, Dziewas R, Genton L, et al. ESPEN [7] Burgos R, Breto 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 professionals 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 performance. Available in: https://www.arca.fiocruz.br/handle/icict/2405. [10] Caneda MA, Fernandes JG, de Almeida AG, Mugnol FE. Reliability of neurological 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 ~o Paulo, SP; 2004. therapy. 1 ed. Roca: Sa [13] Ribeiro PW, Cola PC, Gatto AR, da Silva RG, Luvizutto GJ, Braga GP, et al. Relationship 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.  P, Arreola V, Romea M, Medina L, Palomera E, Serra-Prat M. Accuracy of [14] Clave 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.

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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