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J Korean Dysphagia Soc 2022; 12(2): 115-122

Published online July 30, 2022 https://doi.org/10.34160/jkds.2022.12.2.005

© The Korean Dysphagia Society.

Natural Course of Swallowing Recovery and Associated Factors in Post-Ischemic Stroke Dysphagia

Jin-Woo Suh, M.D.1, Han-Sol Lim, M.D.1, Dong-Kun Kim, M.D.1, Hyun Seung Lee, M.D.1, Yong-Taek Lee, M.D., Ph.D.1, Young Sook Park, M.D., Ph.D.2, Chul-Hyun Park, M.D., Ph.D.1, Kyung-Jae Yoon, M.D., Ph.D.1

1Department of Physical and Rehabilitation Medicine, Kangbuk Samsung Hospital, Sungkyunkwan University School of Medicine, Seoul, 2Department of Physical and Rehabilitation Medicine, Samsung Changwon Hospital, Sungkyunkwan University School of Medicine, Changwon, Korea

Correspondence to:Kyung-Jae Yoon, Department of Physical and Rehabilitation Medicine, Kangbuk Samsung Hospital, Sungkyunkwan University School of Medicine, Seoul 03181, Korea
Tel: +82-2-2001-1784, Fax: +82-2-2001-1284, E-mail: yoon.kjae@gmail.com

Chul-Hyun Park, Department of Physical and Rehabilitation Medicine, Kangbuk Samsung Hospital, Sungkyunkwan University School of Medicine, Seoul 03181, Korea
Tel: +82-2-2001-8487, Fax: +82-2-2001-2176, E-mail: chpark0930@gmail.com

Received: May 20, 2022; Revised: May 20, 2022; Accepted: July 12, 2022

This is an open-access article distributed under the terms of the Creative Commons Attribution Non-Commercial License (https://creativecommons.org/licenses/by-nc/4.0/), which permits unrestricted non-commercial use, distribution, and reproduction in any medium, provided the original work is properly cited.

Objective: To identify factors associated with swallowing recovery in patients with dysphagia after ischemic stroke.
Methods: Patients admitted to Kangbuk Samsung Hospital from 2011 to 2019 for first acute ischemic stroke and dysphagia, as confirmed by a videofluoroscopic swallowing study (VFSS), were enrolled in this retrospective study. Patients whose Dysphagia Outcome and Severity Scale (DOSS) level was <6 as determined by VFSS were monitored in a dysphagia clinic and additional VFSS was performed periodically until one year after stroke. Follow-up was discontinued when the DOSS level reached 6 or 7. The main study outcomes were full recovery and tube removal rate. Cox regression analysis was used to identify prognostic factors of dysphagia. The Kaplan-Meier method was used to generate curves of the proportions of patients that achieved full recovery.
Results: One hundred and thirteen patients were enrolled. Multivariate analysis showed that only initial DOSS was significantly associated with swallowing recovery (13.0% for non-oral feeding vs. 35.6 % for a modified diet).
Conclusion: Initial swallowing status (as determined by VFSS findings) is strongly associated with swallowing recovery in post-ischemic stroke patients. Assessments of dysphagia are important for predicting dysphagia recovery and planning management strategies.

Keywords: Dysphagia, Recovery, Stroke

Post stroke dysphagia (PSD) is an important complication associated with mortality, morbidity and quality of life due to malnutrition, dehydration and aspiration pneumonia. Many PSD patients recover spontaneously within 2 weeks, but 11-50% still suffer from dysphagia at 6 months after onset1-3. Patients with dysphagia are more likely to develop pneumonia 3 times and patients with confirmed aspirations 11 times4. Pneumonia after ischemic stroke are associated with mortality, longer hospita-lization and higher disability at discharge5. There are some studies about prognostic factor of dysphagia after stroke3,6,7. These study showed that dysphagia symptom, aspiration and oral transit delay on video fluoroscopic swallowing study (VFSS), bihemispheric infarct, brainstem infarct, dysarthria, intubation, high NIHSS score were significant predictors of persistent dysphagia. However, they have mostly analyzed the associated factor of dysphagia in the early stage of stroke for over 3-6 months. Persistent dysphagia is crucial for preventing aspiration pneumonia and mortality and predicting prognosis of patients, but few study evaluated prognosis of dysphagia over long time, especially using video fluoroscopic swallowing study (VFSS)8.

The object of this study was to investigate swallowing recovery on VFSS in post stroke dysphagia patients for a long time.

This retrospective study was a cohort analysis of all acute ischemic stroke patients admitted to Kangbuk Samsung Hospital from 2011 to 2019. This experiment included the patients 1) who had first acute ischemic stroke, confirmed by magnetic resonance imaging (MRI), 2) who were observed abnormal swallowing ability by VFSS, and 3) who were performed 1st VFSS within 1 month after onset. The swallowing function was assessed by Dysphagia Outcome and Severity Scale (DOSS) that was previously developed dysphagia scale based on measures obtained from VFSS9.(Table 1) DOSS levels 6 and 7 indicated that normal diet was permitted. DOSS level 3-5 indicated that modified diet should be applied, and the DOSS level 1 and 2 meant more severe dysphagia in which non oral feeding was necessary. Exclusion criteria were as follows: 1) other cause of dysphagia such as neurodegenerative disease, motor neuron disease, Guillian Barre syndrome etc., 2) recurrent ischemic stroke within 1 year after 1st ischemic stroke, and 3) pre-existent dysphagia. This study was approved by institutional review board.

Table 1 . Dysphagia outcome and severity scale.

DOSS levelDiet state
Normal diet
Level 7Normal in all situations
Level 6Within functional limits/modified independence
Modified diet
Level 5Mild dysphagia
Level 4Mild-moderate dysphagia
Level 3Moderate dysphagia
Non-oral feeding
Level 2Moderately severe dysphagia
Level 1Severe dysphagia


Patients whose DOSS level was less than 6 in VFSS were monitored in dysphagia clinic and additional VFSS was performed periodically. Follow up was discontinued if DOSS level would be 6 or 7. Swallowing function was assessed long enough until 1 year after stroke. Dysphagia recovery was targeted as outcome and divided into full recovery and tube removal. Full recovery meant DOSS level improved more than 6. Tube removal rate was ratio of patient whose initial DOSS level was less than 2 and last DOSS level recovered more than 3.

1. Statistical analysis

Data were presented as median (Interquantile range). The variables were collected including sex, age at onset, initial and last DOSS, bihemispheric infarcts, infratentorial lesion, and baseline National Institutes of Health Stroke Scale (NIHSS). In addition, hypertension (HTN), diabetes mellitus (DM), dyslipidemia, and atrial fibrillation were collected. We performed a univariate analysis with Cox proportional hazards regression to identify factors that were associated with dysphagia recovery. Covariates with a P-value<0.2 at univariate Cox’s PH regression were included in multivariate Cox’s pH regression to adjust for various confounding variables. Covariates with a P-value<0.05 at multivariate Cox’s PH regression were included in significant predictors.

We used the Kaplan-Meier method to identify log-rank test and generate a curves for the proportion of patients with swallowing recovery. We used significant factors in Kaplan-Meier method. Initial DOSS level was the only significant factor in both full recovery and tube removal. Initial DOSS was dichotomized into more and less than level 2, which might exhibit need for non-oral nutrition or not. All statistical analyses were done with SPSS software version 24.0 (IBM, Armonk, NY, USA).

Among 531 patients, previous stroke (185 subjects), late VFSS (97 subjects) after ischemic stroke, follow up loss (109 subjects), other cause of dysphagia (14 subjects) and hemorrhagic conversion (13 subjects) were excluded. Patients were monitored for 1 year of follow up for dysphagia.(Fig. 1) A total of 113 patients were included for the study and Table 2 shows the characteristics of participants.

Table 2 . Characteristics of patients (n=113).

CharacteristicsValue
Age at onset (year)71.0 (62.5-79.0)
Gender
Male66 (58.4)
Female47 (41.6)
Location
Supratentorial78 (69.0)
Infratentorial35 (31.0)
Lateralization
Hemispheric lesion101 (89.4)
Bihemispheric lesion12 (10.6)
NIHSS8.0 (5.0-13.0)
Comorbidities
Hypertension69 (61.1)
Diabetes mellitus35 (31.0)
Dyslipidemia66 (58.4)
Atrial fibrillation43 (38.1)

Values are presented frequency (%) or median (interquartile range).

NIHSS: National Institutes of health stroke scale.



Figure 1. Flowchart of the study.

Patient’s median age is 71.0 years old (62.5-79.0). They were severely affected by stroke (median NIHSS score : 8.0, Interquantile range : 5.0-13.0).(Table 2)

Median value of initial DOSS level of patients group was 3. In initial VFSS, the number of non-oral feeding group was 54 (47.8%) and 59 patients (52.1%) was in modified diet group. Median value of last DOSS level of post stroke dysphagia patients was 5. Number of non-oral feeding group, modified diet group and normal diet group was 14 (12.4%), 70 (61.9%) and 29 (25.7%) in last VFSS, respectively.(Table 3)

Table 3 . Dysphagia characteristics and time parameters of patients (n=113).

Characteristics and parameterValue
Onset to first VFSS (day)10.0 (6.0-14.0)
Onset to last VFSS (day)31.0 (23.0-58.0)
Initial DOSS (level)3.0 (2.0-5.0)
Non oral feeding group
Level 118 (15.9)
Level 236 (31.9)
Modified diet group
Level 34 (3.5)
Level 44 (3.5)
Level 551 (45.1)
Last DOSS (level)5.0 (3.0-6.0)
Non oral feeding group
Level 16 (5.3)
Level 28 (7.1)
Modified diet group
Level 317 (15.0)
Level 421 (18.6)
Level 532 (28.3)
Normal diet group
Level 621 (18.6)
Level 78 (7.1)

Values are presented frequency (%) or median (interquartile range).

DOSS: dysphagia outcome and severity scale, VFSS: video fluoroscopic swallowing study.



Sex, infratentorial lesion, DM, dyslipidemia, atrial fibrillation, initial DOSS were associated with full recovery of dysphagia in the univariate analysis.(Table 4, P<0.2) In the multivariate analysis by adjusting sex, infratentorial lesion, DM, dyslipidemia, atrial fibrillation, initial DOSS, only initial DOSS was statistically significant factor for full recovery of dysphagia.(Fig. 2A, P-value=0.02)

Table 4 . Cox’s proportional hazard regression for variables for full recovery of dysphagia.

VariablesUnivariates analysisMultivariates analysis*


Hazard ratio (95% CI)P-valueHazard ratio (95% CI)P-value
Age at onset (year)0.984 (0.959-1.010)0.236
Sex0.583 (0.277-1.227)0.155*0.487 (0.213-1.115)0.089
Initial DOSS (level)1.643 (1.254-2.152)<0.001*1.436 (1.058-1.950)0.02**
Baseline NIHSS0.984 (0.927-1.045)0.603
Bihemispheric lesion0.584 (0.138-2.467)0.465
Infratentorial lesion0.513 (0.208-1.267)0.148*0.736 (0.262-2.064)0.560
Hypertension0.93 (0.439-1.970)0.849
Diabetes mellitus1.68 (0.767-3.678)0.195*1.401 (0.598-3.281)0.437
Dyslipidemia2.097 (0.891-4.938)0.09*1.431 (0.559-3.659)0.455
Atrial fibrillation0.334 (0.334-0.970)0.083*0.353 (0.122-1.022)0.055

Multivariate analysis was adjusted for sex, initial DOSS, infratentorial lesion, diabetes mellitus, dyslipidemia, atrial fibrillation.

*Significant factors in univariate analysis (P<0.2).

**Significant factors in multivariate analysis (P<0.05).

NIHSS: National Institutes of health stroke scale, DOSS: dysphagia outcome and severity scale, VFSS: videofluoroscopic swallowing study.



Figure 2. (A) Multivariate cox regression analysis for dysphagia recovery in patients with PSD and (B) Kaplan-Meier plots for dysphagia recovery in patients with PSD depending on initial DOSS level. DOSS: dysphagia outcome and severity scale, PSD: post stroke dysphagia, NIHSS: National Institutes of health stroke scale.

In log rank test, swallowing full recovery was significantly different between non-oral diet and modified diet group (Log rank P=0.001). 13.0% of non-oral feeding group (7 out of 54 patients) improved to normal diet. 35.6% of modified diet group (21 out of 59 patients) were improved to normal diet. Dysphagia was not improved after 115 days in modified diet group, 91 days in non-oral feeding.(Fig. 2B)

Tube removal rate in non-oral feeding group was 75.9% (41 out of 54). Initial DOSS, sex, bihemispheric lesion, infratentorial lesion, DM were associated factor in univariate analysis. In multivariate analysis, initial DOSS was the only statistically significant factor.(Table 5) In DOSS 1, 61.1% (11 out of 18) showed improvement. 83.3% (30 out of 36) patients recovered in DOSS 2 group. DOSS 2 showed recovery until 340 days which is longer than DOSS 1 group (until 213 days).(Fig. 3)

Table 5 . Cox’s proportional hazard regression for variables for tube removal rate of non-oral feeding group.

VariablesUnivariates analysisMultivariates analysis*


Hazard ratio (95% CI)P-valueHazard ratio (95% CI)P-value
Age at onset (year)1.004 (0.980-1.029)0.734
Sex0.549 (0.287-1.048)0.069*0.540 (0.270-1.080)0.082
Initial DOSS (level)2.142 (1.038-4.419)0.039*2.161 (1.030-4.536)0.042**
Baseline NIHSS1.007 (0.963-1.052)0.767
Bihemispheric lesion0.429 (0.125-1.471)0.178*0.874 (0.206-3.706)0.855
Infratentorial lesion0.523 (0.267-1.024)0.059*0.589 (0.265-1.306)0.192
Hypertension0.915 (0.488-1.714)0.781
Diabetes mellitus2.419 (1.226-4.771)0.011*1.732 (0.835-3.594)0.140
Dyslipidemia0.905 (0.483-1.695)0.755
Atrial fibrillation0.949 (0.508-1.771)0.869

Multivariate analysis was adjusted for sex, initial DOSS, infratentorial lesion, diabetes mellitus, dyslipidemia, atrial fibrillation.

*Significant factors in univariate analysis (P<0.2).

**Significant factors in multivariate analysis (P<0.05).

NIHSS: National Institutes of health stroke scale, DOSS: dysphagia outcome and severity scale, VFSS: videofluoroscopic swallowing study.



Figure 3. Kaplan-Meier plots for tube removal rate in patients with PSD depending on initial DOSS level. DOSS: dysphagia outcome and severity scale, PSD: post stroke dysphagia, NIHSS: National Institutes of health stroke scale.

This study was proceded to identify dysphagia recovery using VFSS in post ischemic stroke dysphagia to find associated factors about these outcome and to characterize the clinical course of dysphagia among severity. Especially, we chracterized dysphagia as DOSS, not presence of aspiration, oral transit delay and pharyngeal dysfunction in VFSS. We assumed that DOSS could be a predictor of post stroke dysphagia prognosis among severity of dysphagia. PAS could replace DOSS, but PAS reflected not other dysphagia status, but only severity of aspiration. We used cox proportion hazards regression with some other variables. It included sex, age at onset, baseline NIHSS, bihemispheric infarcts, infratentorial lesion, HTN, DM, dyslipidemia, and atrial fibrillation. Sex, age, bihemispheric infarct, infratentorial lesion, baseline NIHSS have been investigated as prognostic factors of swallowing recovery, but comorbidities mentioned above were not3,6,10. HTN, DM, atrial fibrillation and dyslipidemia were included because they were known as associated factors of post stroke dysphagia and stroke prognosis11-13.

Our study showed that initial DOSS level was significantly associated with full recovery and tube removal rate in post stroke dysphagia. It means that mild dysphagia show more recovery than severe dysphagia patients. Previous studies also revealed that initial dysphagia severity was an important factor for dysphagia recovery8,14. In Lee’s study8, bilateral lesion in MRI including both acute and chronic lesion were another significant prognostic factors. We thought that chronic stroke lesion in MRI could affect dysphagia severity, although patient did not present dysphagia symptom. Our study excluded old stroke lesion which was revealved in brain MRI because of possibility of 2nd ischemic stroke.

Galovic et al.14 found that age, baseline NIHSS, stroke lesion at frontal operculum, initial aspiration sign, initial swallowing impairment were significant prognostic factors. Galovic et al.14 included patient with functional oral intake scale <5, so initial dysphagia status was more severe than that of our study. More higher NIHSS score are predictive of clinically relevant dysphagia15,16. Actually, patients group of Galovic’s study were older (median age: 79) and more severe stroke patients (median NIHSS: 12) than our study. Different patient group’s characteristics might effect associated factors of dysphagia recovery. Other studies assessed initial dysphagia state through clinical dysphagia scale and symptom3,8,14,17. Our study defined dysphagia through only VFSS findings, not clinical symptoms. Because VFSS is golden standard in detecting dysphagia. Actually, clinical findings had relatively lower sensitivity and specificity18. It is advantage of our study that patients of our study represented dysphagia severity, more objectively.

Our study also showed information about natural course of post stroke dysphagia. More severe dysphagia group showed less recovery rate had shorter recovery period in both full recovery and tube removal rate. Similar to natural course of our study group, previous studies showed that initial stroke severity was predictive value of functional recovery in ischemic stroke, similar to our study15,16. Mechanism of ischemic stroke is not perfectly understood. Neuroplasticity, neurogenesis and angiogenseis are thought to be responsible for neurological recovery19. Hamdy et al.’s study20 showed that dysphagia patients who were recovered after transcranial magnetic stimulation had significant change in area of pharyngeal representation in undamaged hemisphere, similar to neuroplasticity. In dysphagia management, neuroplasticity could be also responsible for recovery, and targeted as outcome of management. More severe dysphagia might need more intensive and longer rehabilitation. Also persistent dysphagia group have higher risk of death and aspiration pneumonia, so long term management plan should be needed21. Full recovery and tube removal rate of post-ischemic stroke dysphagia were 24.7% and 75.9% during 1 year after onset of stroke in our study. In previous study, tube removal rate in post ischemic stroke dysphagia were 70%, similar to our study17. In head & neck cancer with operation, swallowing recovery was 76% within 6 weeks22. In post extubation dysphagia, 77% of patients recovered from dysphagia at 6 months23. Many articles studied about improvement of post ischemic stroke dysphagia, not full recovery24. Full recovery of dysphagia is goal of dysphagia management, especially in post stroke dysphagia. It should be studied for many dysphagia patients. Our study was first study of assessing full recovery of post ischemic stroke dysphagia.

This study has some limitations. First, this study had many follow up loss. 109 post stroke dysphagia patient were excluded because they do not proceed additional VFSS. It could be caused by death, consciousness, stroke progression and so on. This could be related to stroke severity and cause of selection bias. Second, we excluded the patients who were not able to carry out VFSS. Severe patients with decreased consciousness, congition, poor physical acitivy were excluded. However, most of previous studies included more severe dysphagia patients that had higher NIHSS score. This study could represent more wide range of dysphagia severity in post ischemic stroke patients. Third, we excluded hemorrhagic stroke. We thought cerebral ischemia and hemorrhagic stroke have different process of dysphagia recovery25.

Further studies should be well-designed to overcome and minimize these limitations.

Based on this and previous studies, we could know that initial dysphagia state of VFSS was important predictive factor abouth dysphagia recovery in not only severe dysphagia but mild to moderate dysphagia patients. We also could predict natural course of dysphagia among severity of dysphagia. In other words, assessment of initial dysphagia status by VFSS are essential for predicting dysphagia recovery and planning long term management strategy. However, more studies will be needed about full recovery of dysphagia.  

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Article

Original Article

J Korean Dysphagia Soc 2022; 12(2): 115-122

Published online July 30, 2022 https://doi.org/10.34160/jkds.2022.12.2.005

Copyright © The Korean Dysphagia Society.

Natural Course of Swallowing Recovery and Associated Factors in Post-Ischemic Stroke Dysphagia

Jin-Woo Suh, M.D.1, Han-Sol Lim, M.D.1, Dong-Kun Kim, M.D.1, Hyun Seung Lee, M.D.1, Yong-Taek Lee, M.D., Ph.D.1, Young Sook Park, M.D., Ph.D.2, Chul-Hyun Park, M.D., Ph.D.1, Kyung-Jae Yoon, M.D., Ph.D.1

1Department of Physical and Rehabilitation Medicine, Kangbuk Samsung Hospital, Sungkyunkwan University School of Medicine, Seoul, 2Department of Physical and Rehabilitation Medicine, Samsung Changwon Hospital, Sungkyunkwan University School of Medicine, Changwon, Korea

Correspondence to:Kyung-Jae Yoon, Department of Physical and Rehabilitation Medicine, Kangbuk Samsung Hospital, Sungkyunkwan University School of Medicine, Seoul 03181, Korea
Tel: +82-2-2001-1784, Fax: +82-2-2001-1284, E-mail: yoon.kjae@gmail.com

Chul-Hyun Park, Department of Physical and Rehabilitation Medicine, Kangbuk Samsung Hospital, Sungkyunkwan University School of Medicine, Seoul 03181, Korea
Tel: +82-2-2001-8487, Fax: +82-2-2001-2176, E-mail: chpark0930@gmail.com

Received: May 20, 2022; Revised: May 20, 2022; Accepted: July 12, 2022

This is an open-access article distributed under the terms of the Creative Commons Attribution Non-Commercial License (https://creativecommons.org/licenses/by-nc/4.0/), which permits unrestricted non-commercial use, distribution, and reproduction in any medium, provided the original work is properly cited.

Abstract

Objective: To identify factors associated with swallowing recovery in patients with dysphagia after ischemic stroke.
Methods: Patients admitted to Kangbuk Samsung Hospital from 2011 to 2019 for first acute ischemic stroke and dysphagia, as confirmed by a videofluoroscopic swallowing study (VFSS), were enrolled in this retrospective study. Patients whose Dysphagia Outcome and Severity Scale (DOSS) level was <6 as determined by VFSS were monitored in a dysphagia clinic and additional VFSS was performed periodically until one year after stroke. Follow-up was discontinued when the DOSS level reached 6 or 7. The main study outcomes were full recovery and tube removal rate. Cox regression analysis was used to identify prognostic factors of dysphagia. The Kaplan-Meier method was used to generate curves of the proportions of patients that achieved full recovery.
Results: One hundred and thirteen patients were enrolled. Multivariate analysis showed that only initial DOSS was significantly associated with swallowing recovery (13.0% for non-oral feeding vs. 35.6 % for a modified diet).
Conclusion: Initial swallowing status (as determined by VFSS findings) is strongly associated with swallowing recovery in post-ischemic stroke patients. Assessments of dysphagia are important for predicting dysphagia recovery and planning management strategies.

Keywords: Dysphagia, Recovery, Stroke

INTRODUCTION

Post stroke dysphagia (PSD) is an important complication associated with mortality, morbidity and quality of life due to malnutrition, dehydration and aspiration pneumonia. Many PSD patients recover spontaneously within 2 weeks, but 11-50% still suffer from dysphagia at 6 months after onset1-3. Patients with dysphagia are more likely to develop pneumonia 3 times and patients with confirmed aspirations 11 times4. Pneumonia after ischemic stroke are associated with mortality, longer hospita-lization and higher disability at discharge5. There are some studies about prognostic factor of dysphagia after stroke3,6,7. These study showed that dysphagia symptom, aspiration and oral transit delay on video fluoroscopic swallowing study (VFSS), bihemispheric infarct, brainstem infarct, dysarthria, intubation, high NIHSS score were significant predictors of persistent dysphagia. However, they have mostly analyzed the associated factor of dysphagia in the early stage of stroke for over 3-6 months. Persistent dysphagia is crucial for preventing aspiration pneumonia and mortality and predicting prognosis of patients, but few study evaluated prognosis of dysphagia over long time, especially using video fluoroscopic swallowing study (VFSS)8.

The object of this study was to investigate swallowing recovery on VFSS in post stroke dysphagia patients for a long time.

MATERIALS AND METHODS

This retrospective study was a cohort analysis of all acute ischemic stroke patients admitted to Kangbuk Samsung Hospital from 2011 to 2019. This experiment included the patients 1) who had first acute ischemic stroke, confirmed by magnetic resonance imaging (MRI), 2) who were observed abnormal swallowing ability by VFSS, and 3) who were performed 1st VFSS within 1 month after onset. The swallowing function was assessed by Dysphagia Outcome and Severity Scale (DOSS) that was previously developed dysphagia scale based on measures obtained from VFSS9.(Table 1) DOSS levels 6 and 7 indicated that normal diet was permitted. DOSS level 3-5 indicated that modified diet should be applied, and the DOSS level 1 and 2 meant more severe dysphagia in which non oral feeding was necessary. Exclusion criteria were as follows: 1) other cause of dysphagia such as neurodegenerative disease, motor neuron disease, Guillian Barre syndrome etc., 2) recurrent ischemic stroke within 1 year after 1st ischemic stroke, and 3) pre-existent dysphagia. This study was approved by institutional review board.

Table 1 . Dysphagia outcome and severity scale.

DOSS levelDiet state
Normal diet
Level 7Normal in all situations
Level 6Within functional limits/modified independence
Modified diet
Level 5Mild dysphagia
Level 4Mild-moderate dysphagia
Level 3Moderate dysphagia
Non-oral feeding
Level 2Moderately severe dysphagia
Level 1Severe dysphagia


Patients whose DOSS level was less than 6 in VFSS were monitored in dysphagia clinic and additional VFSS was performed periodically. Follow up was discontinued if DOSS level would be 6 or 7. Swallowing function was assessed long enough until 1 year after stroke. Dysphagia recovery was targeted as outcome and divided into full recovery and tube removal. Full recovery meant DOSS level improved more than 6. Tube removal rate was ratio of patient whose initial DOSS level was less than 2 and last DOSS level recovered more than 3.

1. Statistical analysis

Data were presented as median (Interquantile range). The variables were collected including sex, age at onset, initial and last DOSS, bihemispheric infarcts, infratentorial lesion, and baseline National Institutes of Health Stroke Scale (NIHSS). In addition, hypertension (HTN), diabetes mellitus (DM), dyslipidemia, and atrial fibrillation were collected. We performed a univariate analysis with Cox proportional hazards regression to identify factors that were associated with dysphagia recovery. Covariates with a P-value<0.2 at univariate Cox’s PH regression were included in multivariate Cox’s pH regression to adjust for various confounding variables. Covariates with a P-value<0.05 at multivariate Cox’s PH regression were included in significant predictors.

We used the Kaplan-Meier method to identify log-rank test and generate a curves for the proportion of patients with swallowing recovery. We used significant factors in Kaplan-Meier method. Initial DOSS level was the only significant factor in both full recovery and tube removal. Initial DOSS was dichotomized into more and less than level 2, which might exhibit need for non-oral nutrition or not. All statistical analyses were done with SPSS software version 24.0 (IBM, Armonk, NY, USA).

RESULTS

Among 531 patients, previous stroke (185 subjects), late VFSS (97 subjects) after ischemic stroke, follow up loss (109 subjects), other cause of dysphagia (14 subjects) and hemorrhagic conversion (13 subjects) were excluded. Patients were monitored for 1 year of follow up for dysphagia.(Fig. 1) A total of 113 patients were included for the study and Table 2 shows the characteristics of participants.

Table 2 . Characteristics of patients (n=113).

CharacteristicsValue
Age at onset (year)71.0 (62.5-79.0)
Gender
Male66 (58.4)
Female47 (41.6)
Location
Supratentorial78 (69.0)
Infratentorial35 (31.0)
Lateralization
Hemispheric lesion101 (89.4)
Bihemispheric lesion12 (10.6)
NIHSS8.0 (5.0-13.0)
Comorbidities
Hypertension69 (61.1)
Diabetes mellitus35 (31.0)
Dyslipidemia66 (58.4)
Atrial fibrillation43 (38.1)

Values are presented frequency (%) or median (interquartile range).

NIHSS: National Institutes of health stroke scale.



Figure 1. Flowchart of the study.

Patient’s median age is 71.0 years old (62.5-79.0). They were severely affected by stroke (median NIHSS score : 8.0, Interquantile range : 5.0-13.0).(Table 2)

Median value of initial DOSS level of patients group was 3. In initial VFSS, the number of non-oral feeding group was 54 (47.8%) and 59 patients (52.1%) was in modified diet group. Median value of last DOSS level of post stroke dysphagia patients was 5. Number of non-oral feeding group, modified diet group and normal diet group was 14 (12.4%), 70 (61.9%) and 29 (25.7%) in last VFSS, respectively.(Table 3)

Table 3 . Dysphagia characteristics and time parameters of patients (n=113).

Characteristics and parameterValue
Onset to first VFSS (day)10.0 (6.0-14.0)
Onset to last VFSS (day)31.0 (23.0-58.0)
Initial DOSS (level)3.0 (2.0-5.0)
Non oral feeding group
Level 118 (15.9)
Level 236 (31.9)
Modified diet group
Level 34 (3.5)
Level 44 (3.5)
Level 551 (45.1)
Last DOSS (level)5.0 (3.0-6.0)
Non oral feeding group
Level 16 (5.3)
Level 28 (7.1)
Modified diet group
Level 317 (15.0)
Level 421 (18.6)
Level 532 (28.3)
Normal diet group
Level 621 (18.6)
Level 78 (7.1)

Values are presented frequency (%) or median (interquartile range).

DOSS: dysphagia outcome and severity scale, VFSS: video fluoroscopic swallowing study.



Sex, infratentorial lesion, DM, dyslipidemia, atrial fibrillation, initial DOSS were associated with full recovery of dysphagia in the univariate analysis.(Table 4, P<0.2) In the multivariate analysis by adjusting sex, infratentorial lesion, DM, dyslipidemia, atrial fibrillation, initial DOSS, only initial DOSS was statistically significant factor for full recovery of dysphagia.(Fig. 2A, P-value=0.02)

Table 4 . Cox’s proportional hazard regression for variables for full recovery of dysphagia.

VariablesUnivariates analysisMultivariates analysis*


Hazard ratio (95% CI)P-valueHazard ratio (95% CI)P-value
Age at onset (year)0.984 (0.959-1.010)0.236
Sex0.583 (0.277-1.227)0.155*0.487 (0.213-1.115)0.089
Initial DOSS (level)1.643 (1.254-2.152)<0.001*1.436 (1.058-1.950)0.02**
Baseline NIHSS0.984 (0.927-1.045)0.603
Bihemispheric lesion0.584 (0.138-2.467)0.465
Infratentorial lesion0.513 (0.208-1.267)0.148*0.736 (0.262-2.064)0.560
Hypertension0.93 (0.439-1.970)0.849
Diabetes mellitus1.68 (0.767-3.678)0.195*1.401 (0.598-3.281)0.437
Dyslipidemia2.097 (0.891-4.938)0.09*1.431 (0.559-3.659)0.455
Atrial fibrillation0.334 (0.334-0.970)0.083*0.353 (0.122-1.022)0.055

Multivariate analysis was adjusted for sex, initial DOSS, infratentorial lesion, diabetes mellitus, dyslipidemia, atrial fibrillation.

*Significant factors in univariate analysis (P<0.2).

**Significant factors in multivariate analysis (P<0.05).

NIHSS: National Institutes of health stroke scale, DOSS: dysphagia outcome and severity scale, VFSS: videofluoroscopic swallowing study.



Figure 2. (A) Multivariate cox regression analysis for dysphagia recovery in patients with PSD and (B) Kaplan-Meier plots for dysphagia recovery in patients with PSD depending on initial DOSS level. DOSS: dysphagia outcome and severity scale, PSD: post stroke dysphagia, NIHSS: National Institutes of health stroke scale.

In log rank test, swallowing full recovery was significantly different between non-oral diet and modified diet group (Log rank P=0.001). 13.0% of non-oral feeding group (7 out of 54 patients) improved to normal diet. 35.6% of modified diet group (21 out of 59 patients) were improved to normal diet. Dysphagia was not improved after 115 days in modified diet group, 91 days in non-oral feeding.(Fig. 2B)

Tube removal rate in non-oral feeding group was 75.9% (41 out of 54). Initial DOSS, sex, bihemispheric lesion, infratentorial lesion, DM were associated factor in univariate analysis. In multivariate analysis, initial DOSS was the only statistically significant factor.(Table 5) In DOSS 1, 61.1% (11 out of 18) showed improvement. 83.3% (30 out of 36) patients recovered in DOSS 2 group. DOSS 2 showed recovery until 340 days which is longer than DOSS 1 group (until 213 days).(Fig. 3)

Table 5 . Cox’s proportional hazard regression for variables for tube removal rate of non-oral feeding group.

VariablesUnivariates analysisMultivariates analysis*


Hazard ratio (95% CI)P-valueHazard ratio (95% CI)P-value
Age at onset (year)1.004 (0.980-1.029)0.734
Sex0.549 (0.287-1.048)0.069*0.540 (0.270-1.080)0.082
Initial DOSS (level)2.142 (1.038-4.419)0.039*2.161 (1.030-4.536)0.042**
Baseline NIHSS1.007 (0.963-1.052)0.767
Bihemispheric lesion0.429 (0.125-1.471)0.178*0.874 (0.206-3.706)0.855
Infratentorial lesion0.523 (0.267-1.024)0.059*0.589 (0.265-1.306)0.192
Hypertension0.915 (0.488-1.714)0.781
Diabetes mellitus2.419 (1.226-4.771)0.011*1.732 (0.835-3.594)0.140
Dyslipidemia0.905 (0.483-1.695)0.755
Atrial fibrillation0.949 (0.508-1.771)0.869

Multivariate analysis was adjusted for sex, initial DOSS, infratentorial lesion, diabetes mellitus, dyslipidemia, atrial fibrillation.

*Significant factors in univariate analysis (P<0.2).

**Significant factors in multivariate analysis (P<0.05).

NIHSS: National Institutes of health stroke scale, DOSS: dysphagia outcome and severity scale, VFSS: videofluoroscopic swallowing study.



Figure 3. Kaplan-Meier plots for tube removal rate in patients with PSD depending on initial DOSS level. DOSS: dysphagia outcome and severity scale, PSD: post stroke dysphagia, NIHSS: National Institutes of health stroke scale.

DISCUSSION

This study was proceded to identify dysphagia recovery using VFSS in post ischemic stroke dysphagia to find associated factors about these outcome and to characterize the clinical course of dysphagia among severity. Especially, we chracterized dysphagia as DOSS, not presence of aspiration, oral transit delay and pharyngeal dysfunction in VFSS. We assumed that DOSS could be a predictor of post stroke dysphagia prognosis among severity of dysphagia. PAS could replace DOSS, but PAS reflected not other dysphagia status, but only severity of aspiration. We used cox proportion hazards regression with some other variables. It included sex, age at onset, baseline NIHSS, bihemispheric infarcts, infratentorial lesion, HTN, DM, dyslipidemia, and atrial fibrillation. Sex, age, bihemispheric infarct, infratentorial lesion, baseline NIHSS have been investigated as prognostic factors of swallowing recovery, but comorbidities mentioned above were not3,6,10. HTN, DM, atrial fibrillation and dyslipidemia were included because they were known as associated factors of post stroke dysphagia and stroke prognosis11-13.

Our study showed that initial DOSS level was significantly associated with full recovery and tube removal rate in post stroke dysphagia. It means that mild dysphagia show more recovery than severe dysphagia patients. Previous studies also revealed that initial dysphagia severity was an important factor for dysphagia recovery8,14. In Lee’s study8, bilateral lesion in MRI including both acute and chronic lesion were another significant prognostic factors. We thought that chronic stroke lesion in MRI could affect dysphagia severity, although patient did not present dysphagia symptom. Our study excluded old stroke lesion which was revealved in brain MRI because of possibility of 2nd ischemic stroke.

Galovic et al.14 found that age, baseline NIHSS, stroke lesion at frontal operculum, initial aspiration sign, initial swallowing impairment were significant prognostic factors. Galovic et al.14 included patient with functional oral intake scale <5, so initial dysphagia status was more severe than that of our study. More higher NIHSS score are predictive of clinically relevant dysphagia15,16. Actually, patients group of Galovic’s study were older (median age: 79) and more severe stroke patients (median NIHSS: 12) than our study. Different patient group’s characteristics might effect associated factors of dysphagia recovery. Other studies assessed initial dysphagia state through clinical dysphagia scale and symptom3,8,14,17. Our study defined dysphagia through only VFSS findings, not clinical symptoms. Because VFSS is golden standard in detecting dysphagia. Actually, clinical findings had relatively lower sensitivity and specificity18. It is advantage of our study that patients of our study represented dysphagia severity, more objectively.

Our study also showed information about natural course of post stroke dysphagia. More severe dysphagia group showed less recovery rate had shorter recovery period in both full recovery and tube removal rate. Similar to natural course of our study group, previous studies showed that initial stroke severity was predictive value of functional recovery in ischemic stroke, similar to our study15,16. Mechanism of ischemic stroke is not perfectly understood. Neuroplasticity, neurogenesis and angiogenseis are thought to be responsible for neurological recovery19. Hamdy et al.’s study20 showed that dysphagia patients who were recovered after transcranial magnetic stimulation had significant change in area of pharyngeal representation in undamaged hemisphere, similar to neuroplasticity. In dysphagia management, neuroplasticity could be also responsible for recovery, and targeted as outcome of management. More severe dysphagia might need more intensive and longer rehabilitation. Also persistent dysphagia group have higher risk of death and aspiration pneumonia, so long term management plan should be needed21. Full recovery and tube removal rate of post-ischemic stroke dysphagia were 24.7% and 75.9% during 1 year after onset of stroke in our study. In previous study, tube removal rate in post ischemic stroke dysphagia were 70%, similar to our study17. In head & neck cancer with operation, swallowing recovery was 76% within 6 weeks22. In post extubation dysphagia, 77% of patients recovered from dysphagia at 6 months23. Many articles studied about improvement of post ischemic stroke dysphagia, not full recovery24. Full recovery of dysphagia is goal of dysphagia management, especially in post stroke dysphagia. It should be studied for many dysphagia patients. Our study was first study of assessing full recovery of post ischemic stroke dysphagia.

This study has some limitations. First, this study had many follow up loss. 109 post stroke dysphagia patient were excluded because they do not proceed additional VFSS. It could be caused by death, consciousness, stroke progression and so on. This could be related to stroke severity and cause of selection bias. Second, we excluded the patients who were not able to carry out VFSS. Severe patients with decreased consciousness, congition, poor physical acitivy were excluded. However, most of previous studies included more severe dysphagia patients that had higher NIHSS score. This study could represent more wide range of dysphagia severity in post ischemic stroke patients. Third, we excluded hemorrhagic stroke. We thought cerebral ischemia and hemorrhagic stroke have different process of dysphagia recovery25.

Further studies should be well-designed to overcome and minimize these limitations.

CONCLUSION

Based on this and previous studies, we could know that initial dysphagia state of VFSS was important predictive factor abouth dysphagia recovery in not only severe dysphagia but mild to moderate dysphagia patients. We also could predict natural course of dysphagia among severity of dysphagia. In other words, assessment of initial dysphagia status by VFSS are essential for predicting dysphagia recovery and planning long term management strategy. However, more studies will be needed about full recovery of dysphagia.  

Fig 1.

Figure 1.Flowchart of the study.
Journal of the Korean Dysphagia Society 2022; 12: 115-122https://doi.org/10.34160/jkds.2022.12.2.005

Fig 2.

Figure 2.(A) Multivariate cox regression analysis for dysphagia recovery in patients with PSD and (B) Kaplan-Meier plots for dysphagia recovery in patients with PSD depending on initial DOSS level. DOSS: dysphagia outcome and severity scale, PSD: post stroke dysphagia, NIHSS: National Institutes of health stroke scale.
Journal of the Korean Dysphagia Society 2022; 12: 115-122https://doi.org/10.34160/jkds.2022.12.2.005

Fig 3.

Figure 3.Kaplan-Meier plots for tube removal rate in patients with PSD depending on initial DOSS level. DOSS: dysphagia outcome and severity scale, PSD: post stroke dysphagia, NIHSS: National Institutes of health stroke scale.
Journal of the Korean Dysphagia Society 2022; 12: 115-122https://doi.org/10.34160/jkds.2022.12.2.005

Table 1 . Dysphagia outcome and severity scale.

DOSS levelDiet state
Normal diet
Level 7Normal in all situations
Level 6Within functional limits/modified independence
Modified diet
Level 5Mild dysphagia
Level 4Mild-moderate dysphagia
Level 3Moderate dysphagia
Non-oral feeding
Level 2Moderately severe dysphagia
Level 1Severe dysphagia

Table 2 . Characteristics of patients (n=113).

CharacteristicsValue
Age at onset (year)71.0 (62.5-79.0)
Gender
Male66 (58.4)
Female47 (41.6)
Location
Supratentorial78 (69.0)
Infratentorial35 (31.0)
Lateralization
Hemispheric lesion101 (89.4)
Bihemispheric lesion12 (10.6)
NIHSS8.0 (5.0-13.0)
Comorbidities
Hypertension69 (61.1)
Diabetes mellitus35 (31.0)
Dyslipidemia66 (58.4)
Atrial fibrillation43 (38.1)

Values are presented frequency (%) or median (interquartile range).

NIHSS: National Institutes of health stroke scale.


Table 3 . Dysphagia characteristics and time parameters of patients (n=113).

Characteristics and parameterValue
Onset to first VFSS (day)10.0 (6.0-14.0)
Onset to last VFSS (day)31.0 (23.0-58.0)
Initial DOSS (level)3.0 (2.0-5.0)
Non oral feeding group
Level 118 (15.9)
Level 236 (31.9)
Modified diet group
Level 34 (3.5)
Level 44 (3.5)
Level 551 (45.1)
Last DOSS (level)5.0 (3.0-6.0)
Non oral feeding group
Level 16 (5.3)
Level 28 (7.1)
Modified diet group
Level 317 (15.0)
Level 421 (18.6)
Level 532 (28.3)
Normal diet group
Level 621 (18.6)
Level 78 (7.1)

Values are presented frequency (%) or median (interquartile range).

DOSS: dysphagia outcome and severity scale, VFSS: video fluoroscopic swallowing study.


Table 4 . Cox’s proportional hazard regression for variables for full recovery of dysphagia.

VariablesUnivariates analysisMultivariates analysis*


Hazard ratio (95% CI)P-valueHazard ratio (95% CI)P-value
Age at onset (year)0.984 (0.959-1.010)0.236
Sex0.583 (0.277-1.227)0.155*0.487 (0.213-1.115)0.089
Initial DOSS (level)1.643 (1.254-2.152)<0.001*1.436 (1.058-1.950)0.02**
Baseline NIHSS0.984 (0.927-1.045)0.603
Bihemispheric lesion0.584 (0.138-2.467)0.465
Infratentorial lesion0.513 (0.208-1.267)0.148*0.736 (0.262-2.064)0.560
Hypertension0.93 (0.439-1.970)0.849
Diabetes mellitus1.68 (0.767-3.678)0.195*1.401 (0.598-3.281)0.437
Dyslipidemia2.097 (0.891-4.938)0.09*1.431 (0.559-3.659)0.455
Atrial fibrillation0.334 (0.334-0.970)0.083*0.353 (0.122-1.022)0.055

Multivariate analysis was adjusted for sex, initial DOSS, infratentorial lesion, diabetes mellitus, dyslipidemia, atrial fibrillation.

*Significant factors in univariate analysis (P<0.2).

**Significant factors in multivariate analysis (P<0.05).

NIHSS: National Institutes of health stroke scale, DOSS: dysphagia outcome and severity scale, VFSS: videofluoroscopic swallowing study.


Table 5 . Cox’s proportional hazard regression for variables for tube removal rate of non-oral feeding group.

VariablesUnivariates analysisMultivariates analysis*


Hazard ratio (95% CI)P-valueHazard ratio (95% CI)P-value
Age at onset (year)1.004 (0.980-1.029)0.734
Sex0.549 (0.287-1.048)0.069*0.540 (0.270-1.080)0.082
Initial DOSS (level)2.142 (1.038-4.419)0.039*2.161 (1.030-4.536)0.042**
Baseline NIHSS1.007 (0.963-1.052)0.767
Bihemispheric lesion0.429 (0.125-1.471)0.178*0.874 (0.206-3.706)0.855
Infratentorial lesion0.523 (0.267-1.024)0.059*0.589 (0.265-1.306)0.192
Hypertension0.915 (0.488-1.714)0.781
Diabetes mellitus2.419 (1.226-4.771)0.011*1.732 (0.835-3.594)0.140
Dyslipidemia0.905 (0.483-1.695)0.755
Atrial fibrillation0.949 (0.508-1.771)0.869

Multivariate analysis was adjusted for sex, initial DOSS, infratentorial lesion, diabetes mellitus, dyslipidemia, atrial fibrillation.

*Significant factors in univariate analysis (P<0.2).

**Significant factors in multivariate analysis (P<0.05).

NIHSS: National Institutes of health stroke scale, DOSS: dysphagia outcome and severity scale, VFSS: videofluoroscopic swallowing study.


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