Stroke
CLINICAL TRIAL
Effect of Intermittent Oro-Esophageal Tube
Feeding in Bulbar Palsy After Ischemic Stroke:
A Randomized Controlled Study
Hongji Zeng , MMed; Weijia Zhao, MMed; Junfa Wu, MD; Jihong Wei, MD; Heping Li, MD; Liugen Wang, MMed; Xi Zeng , MD
BACKGROUND: Nasogastric tube feeding (NG) has been widely used in patients with bulbar palsy after ischemic stroke but is
associated with a significant risk of complications including malnutrition and pneumonia. Intermittent oro-esophageal tube
feeding (IOE) can help alleviate these concerns. This study explored the clinical effect of IOE versus NG on nutritional status,
swallowing function, stroke-associated pneumonia, and depression in patients with bulbar palsy after ischemic stroke.
METHODS: This randomized controlled study included 148 patients with bulbar palsy after ischemic stroke who underwent
routine treatment and swallowing rehabilitation training in the Department of Rehabilitation Medicine between July 2017
and July 2019 in China. The participants were randomly divided into the IOE group (n=74) and NG group (n=74) with IOE
and NG as nutritional supports, respectively. The primary outcome was nutritional status including (1) body mass index (kg/
m2), (2) serum ALB (albumin, g/L), and (3) PA (prealbumin, mg/L). The secondary outcomes were (1) swallowing function
including (i) Functional Oral Intake Scale (FOIS) and (ii) Penetration-Aspiration Scale, (2) pneumonia, (3) depression, and
(4) adverse events. Statistical analyses for continuous outcomes were performed using t test, Mann-Whitney U test and
Wilcoxon signed-rank test and categorical variables using χ2 test. SPSS 21.0 was used for all analysis.
RESULTS: There were no significant baseline differences between the 2 groups. After the treatment, the IOE group demonstrated
significantly better results compared with the NG group in ALB ([32.71±0.94] versus [32.28±0.81] g/L; P=0.003), PA
([278.15±13.81] versus [270.31±15.08] mg/L; P=0.001], body mass index ([19.77±1.03] versus [19.41±0.98] kg/m2;
P=0.002], FOIS (P<0.001), Penetration-Aspiration Scale (P<0.001), stroke-associated pneumonia ([1, 4.05%] versus [26,
35.14%]; P<0.001), depression ([1, 1.35%] versus [44, 59.46%]; P<0.001) and overall less adverse events (reflux, fever,
discomfort in the throat; P<0.001).
CONCLUSIONS: In patients with dysphagia with bulbar palsy after ischemic stroke who received routine treatment and swallowing
rehabilitation training, IOE is safer and more conducive to the improvement of nutritional status, swallowing function, strokeassociated pneumonia, and depression than NG.
REGISTRATION: URL: https://www.chictr.org.cn; Unique identifier: ChiCTR-INC-17011741.
GRAPHIC ABSTRACT: A graphic abstract is available for this article.
Key Words: dysphagia ◼ ischemic stroke ◼ prealbumin ◼ stroke ◼ stroke rehabilitation
I
schemic stroke, a clinical syndrome caused by stenosis or occlusion of cerebral feeding arteries for various
reasons, leads to localized cerebral ischemia, hypoxic
necrosis of brain tissue, and corresponding neurological
deficits. Characterized by its high prevalence, mortality,
disability, and recurrence rate, it constitutes a significant
threat to human health and life safety.1 Dysphagia is a
potential and frequent complication following ischemic
Correspondence to: Xi Zeng, MD, Department of Rehabilitation Medicine, The First Affiliated Hospital of Zhengzhou University, Zhengzhou 450000, China. Email
zenghongjiclv@foxmail.com
Supplemental Material is available at https://www.ahajournals.org/doi/suppl/10.1161/STROKEAHA.123.046122.
For Sources of Funding and Disclosures, see page 1149.
© 2024 American Heart Association, Inc.
Stroke is available at www.ahajournals.org/journal/str
1142 May 2024
Stroke. 2024;55:1142–1150. DOI: 10.1161/STROKEAHA.123.046122
Zeng et al
IOE in Patients With Bulbar Palsy After Stroke
Nonstandard Abbreviations and Acronyms
ALB
FOIS
IOE
NG
PA
PAS
albumin
Functional Oral Intake Scale
Intermittent Oro-esophageal Tube
Feeding
Nasogastric Tube Feeding
prealbumin
Penetration-Aspiration Scale
METHODS
The data that support the findings of this study are available
from the corresponding author upon reasonable request.
Trial Design
stroke, affecting approximately 30% of the patients.
If not promptly treated, it can lead to various problems,
including aspiration pneumonia, hypoproteinemia, dehydration, electrolyte imbalances, and malnutrition. In
severe cases, it may even result in fatal consequences
due to suffocation.3 Based on the lesion, dysphagia following ischemic stroke can be categorized into bulbar
and pseudobulbar palsy, with the former predominantly
affecting the medulla oblongata of the brainstem.4 In
addition to dysphagia, the patients with bulbar palsy after
ischemic stroke typically present with symptoms such as
hoarseness, and dysarthria.5
Unfortunately, corresponding treatment continues
to be a challenge.6 Due to the prevailing dysphagia in
these patients, nutrition support is generally required to
mitigate the risk of malnutrition and associated complications.7 However, parenteral nutrition has limitations in
providing adequate nutrients and may increase the incidence of bacterial infections and diarrhea.8 Therefore,
enteral nutrition is preferred and recommended in clinical practice.9 Currently, nasogastric tube feeding (NG)
is commonly adopted in Asia, whereas percutaneous
endoscopic gastrostomy is frequently utilized in western
countries.10 Nevertheless, NG exhibits poor compliance
and is significantly associated with various complications
including aspiration pneumonia and reflux,11 while gastrostomy may result in vomiting, diarrhea, and leakage.12
Therefore, it holds practical significance to explore a safe
and efficient enteral nutrition approach for such patients.
Intermittent oro-esophageal tube feeding (IOE), an
emerging enteral nutrition approach, has garnered considerable attention. Its distinguishing feature lies in the
insertion via mouth instead of the nasal cavity, intermittently delivering food to the upper esophagus rather than
the stomach.13 During feeding, positive pressure from
the oral cavity and negative pressure from the stomach
propel the food into stomach.14 Furthermore, the tube is
promptly removed after each feeding, thereby not affecting the contraction of gastroesophageal sphincter.13
Consequently, it has the potential to deliver a relatively
large amount of nutrients. Based on this, we speculate
that IOE may improve various conditions in patients with
bulbar palsy after ischemic stroke. Therefore, the current study aimed to conduct a randomized controlled trial
2
Stroke. 2024;55:1142–1150. DOI: 10.1161/STROKEAHA.123.046122
This randomized controlled study included patients with dysphagia with bulbar palsy, after ischemic stroke, who were
treated in the Department of Rehabilitation Medicine from July
2017 to July 2019. The study lasted 15 days for each participant. Patients were divided randomly into IOE and NG groups,
with 74 patients in each group. Both the groups underwent routine treatment and swallowing rehabilitation training. Moreover,
enteral nutrition support was given to the IOE group and NG
group through IOE and NG, respectively.
Participants
Inclusion Criteria
The inclusion criteria were as follows: (1) Meeting the diagnostic criteria of ischemic stroke,15 confirmed by imaging materials,
with stroke occurring in the medulla oblongata, and diagnosed
with bulbar palsy. (2) The upper esophageal sphincter did
not open or opened ineffectively, with food residue or aspiration, as revealed by the Videofluoroscopic Swallow Study and
diagnosed with dysphagia. (3) Aged >18 years. (4) First-time
stroke. (5) Enteral nutritional support was required and feasible.
(6) Steady vital signs without severe cognitive impairment or
aphasia, patient able to cooperate with the assessment. (7)
Transferred or admitted to the Department of Rehabilitation
Medicine within 15 days of onset.
Exclusion Criteria
The exclusion criteria were as follows: (1) Bulbar palsy caused
by other diseases such as neurodegenerative diseases.
(2) Pseudobulbar palsy. (3) Simultaneously suffering from
other neurological diseases. (4) Tracheostomized patient. (5)
Simultaneously suffering from liver kidney failure, tumors, or
hematologic diseases. (6) Dysphagia caused by other diseases.
(7) Pregnant females.
Shedding Criteria
The shedding criteria were as follows: (1) Intolerance or poor
compliance with the intervention. (2) Severe deterioration of the
patient’s condition, such as severe infections. (3) Changes in
treatment required, including the nutritional support approach.
(4) Voluntary withdrawal.
Settings and Locations
After obtaining ethical approval, we published a brief introduction both online and in the institutions. Patients of interest
could contact us for detailed information. Patients could only
participate in the study if they met the selection criteria, and
no patients or the public were involved in the design, conduct,
reporting, or dissemination of the study plans. The study was
May 2024 1143
Clinical Trial
to explore the effect of IOE versus NG in patients with
bulbar palsy after ischemic stroke who received routine
treatment and swallowing rehabilitation training, specifically, nutritional status, swallowing function, strokeassociated pneumonia, and depression.
Zeng et al
Clinical Trial
conducted in the Department of Rehabilitation Medicine of 3
hospitals in China.
Intervention
In addition to routine treatment, both groups were provided
with swallowing rehabilitation training, including direct, indirect, and compensatory training. During treatment, both groups
received enteral nutrition support through IOE or NG, respectively. It is worth mentioning that some patients with ischemic
stroke do not require hospitalization for enteral nutrition support. However, owing to the refund regulations of China’s public
medical insurance, hospitalization is necessary for patients to
be eligible to receive a refund. Consequently, patients (not limited to the diseases in this study) tended to choose hospitalization, which unexpectedly facilitated this study.
Routine Treatment and Swallowing Rehabilitation Training
Both groups received routine treatment including health
education, guidance, risk factor control, and corresponding
medication therapy for secondary prevention. The patients
diagnosed with pneumonia underwent corresponding treatment. Swallowing rehabilitation training was conducted for all
the patients as follows:
(1)Direct training: Use of homemade lotus root powder
(paste) to conduct oral intake training once a day, 5
days per week.
(2)Indirect training: Utilizing the Mendelsohn maneuver
and Shaker maneuver, 30 minute per session, BID, 5
days per week.
(3)Compensatory training: Techniques such as head rotation swallow maneuver and dry swallow maneuver, 5
minute per session, 5× a day, 5 days per week.
Enteral Nutrition Support Approach
The IOE group was provided with the intermittent oroesophageal tube for nutritional support (Figure S1).9 The
tube was 40 cm long with an inner diameter of 5.4 mm,
made of silicone material. There were side holes at the head
and connectors at the end for the syringe connection. When
needed, the tube head was slowly and gently inserted into
the esophagus via the mouth. Then the tube placement test
was conducted as follows: (1) The outer end of the tube
was placed in water, and the presence of bubble exhalation
indicated that the tube may have entered the airway. (2) The
outer end of the tube was rotated, and the strong resistance
from the patients indicated that the tube might be coiled
inside the mouth. If the patient exhibited severe coughing
during rotation, the tube might have been misplaced in the
trachea. An initial feeding of 200 mL per meal was given,
with an increase of 50 mL per meal until reaching the usual
meal volume (≈500–800 mL), 4 to 6 times a day, alternating
between food and water.
Upon admission, the NG group received nutritional support with the nasogastric tube. After the tube was inserted
into the stomach through the nasal cavity. A gastric fluid pH
test was conducted to confirm successful insertion. Once
placement was confirmed, the tube was properly secured on
both sides of the nasal wing and cheek. Feeding was administered according to nasogastric tube care guidelines,16 with
each feeding not exceeding 200 mL and an interval >2 hours
between feedings.
1144 May 2024
IOE in Patients With Bulbar Palsy After Stroke
The nutrition standards for the 2 groups were the same,
with a daily intake of 25 to 35 kcal/kg and protein intake of
0.8 to 1.2 g/kg, which were adjusted according to the patient’s
condition by professional nutritionists.17 In addition, the actual
feeding amount was adjusted based on the patient’s appetite
and willingness, but we tried our best to avoid malnutrition in
the patients.
Baseline Assessment
According to relevant studies and our clinical experience,
patients’ nutritional status and swallowing function generally
improved after 2-week treatment. Hence, this study lasted 15
days for each patient. Nutritional status, swallowing function,
stroke-associated pneumonia, and depression in the 2 groups
were assessed at admission and after treatment. Demographic
information and disease conditions were assessed at baseline.
Primary Outcome
Nutritional Status
Based on previous studies on patients with dysphagia with
stroke,18 nutritional status was assessed in this study, including
body mass index (kg/m2), serum ALB (albumin, g/L), and PA
(prealbumin, mg/L).
Secondary Outcomes
Swallowing Function
The Functional Oral Intake Scale (FOIS) was used to assess
swallowing function.19 FOIS indirectly determined swallowing
function and was divided into 7 levels, with higher levels indicating better swallowing function. The Penetration-Aspiration
Scale (PAS) was also included in this assessment. PAS is typically based on videofluoroscopic swallow study to evaluate the
extent to which food or liquid enters the airway during swallowing.20 The scale is categorized into different levels based on
observations to determine the degree and type of dysphagia,
which is commonly used to assess the safety of oral intake.
It consists of 8 levels, ranging from 1 to 8, with higher levels
indicating lower swallowing function.
Stroke-Associated Pneumonia
The diagnostic criteria for stroke-associated pneumonia were
as follows:21 new or progressive infiltrative pulmonary lesions
identified through computer tomography, after stroke, along
with the presence of ≥2 of the following clinical symptoms: (1)
fever (≥38 °C); (2) newly developed cough and sputum production with purulent secretions; (3) findings of rales and signs of
pulmonary consolidation; (4) peripheral blood leukocyte count
≥10×109/L or ≤4×109/L.
Depression
The Patient Health Questionnaire-9 was used to assess
depression.22 A score of 0 to 4 indicated no depression (negative), while a score >4 indicated potential depression (positive).
Adverse Events
Adverse events were systematically assessed and analyzed
to ensure accurate reporting and proper interpretation of the
results. Specifically, adverse events were identified through
regular monitoring and reporting by both the participants and
Stroke. 2024;55:1142–1150. DOI: 10.1161/STROKEAHA.123.046122
Zeng et al
Sample Size
Based on the literature review, it was assumed that all subindicators of nutritional status (primary outcome) would exhibit
significant changes. The maximum target sample size was
achieved when the expected sample size was estimated using
ALB. The PASS 2008 software was used to calculate the sample size. In this case,23 M1=33.37, M2=32.95, S=0.87, α=0.05,
(1–β)=80%, it was calculated the following:
N1=N2= \frac[{2 \times (Z_{\alpha/2} + Z_{\beta})^2
\times S^2}][{(M1 - M2)^2}]≈67
To assume a 10% dropout rate, the estimated sample size
for this study was calculated as 67×110%, which was ≈74.
Randomization
After enrollment, all patients were first numbered in a database and then randomly divided into IOE and NG groups. The
procedure was programmed in the data center. A computergenerated block was then used for randomization. Random
assignment was conducted by an independent staff member.
All information regarding the randomization was not disclosed
until the end of the study. The random list was kept strictly confidential from unnecessary personnel.
Blinding and Details
All researchers were required to maintain an isolated status from the participants beyond the necessary contact and
strictly kept research-related information confidential throughout the study. In addition, all data collection and assessments
were conducted by professional staff who were unaware
of the study design, study content, and group allocation and
were not involved in the intervention to ensure objectivity and
independence. All the medical personnel responsible for the
interventions received detailed training to ensure their understanding and proper implementation. Specifically, the assessment was conducted by a professional rehabilitation physician
and a professional rehabilitation therapist. The intervention was
implemented by the primary physician in charge, and a designated professional speech and swallowing therapist. The
grouping information is marked by the principal investigator on
the patient’s bedside information card and changed daily, and
only the research personnel involved in the intervention can
understand.
The data collectors were trained to ensure they understood the importance of data integrity. The principal investigator of the study regularly supervised the intervention process
to ensure compliance with the protocol, and checked the data
to identify and record any instances of missing data promptly.
Only complete cases were enrolled in the final analysis. Details
Stroke. 2024;55:1142–1150. DOI: 10.1161/STROKEAHA.123.046122
regarding missing variables would be reported, and a sensitivity
analysis would be conducted to assess the potential influence
on this study.
Ethics Approval
The study was conducted in accordance with the Declaration
of Helsinki and approved by the Ethics Committee of the First
Affiliated Hospital of Zhengzhou University (2017-KY-0629).
Written informed consent was obtained from each patient and
family member before enrollment in the study.
Statistical Analysis
After passing the test of normality, continuous data in this study
were presented as mean and SD (x̄ ± s), and the differences
were analyzed using the t test because all data exhibited homogeneity of variance. Continuous data with a skewed distribution
were expressed as (x̄ ± s), and the ranked data were listed in the
tables, all of which were analyzed using the Mann-Whitney U test
and Wilcoxon signed-rank test. Categorical data were expressed
as the number of cases and frequency (n [%]), while tests were
performed to analyze the differences. Statistical significance was
set at P<0.05, and SPSS 21.0 was used for all analysis.
RESULT
Baseline Data
Totally, 328 patients with bulbar palsy, after ischemic
stroke were sequentially screened for eligibility from July
2017 to May 2019. Finally, 148 patients met our inclusion criteria and were randomly assigned to the IOE and
NG groups. A flowchart was shown in Figure. No dropouts occurred during the study.
There were no statistically significant differences
(P>0.05) between the 2 groups in terms of basic characteristics, as shown in Table 1.
Nutritional Status
At admission, there were no significant differences in
the nutritional status between the 2 groups (P>0.05).
After treatment, all groups showed significant improvement except for body mass index in the NG group, while
there were significant differences in body mass index,
ALB, and PA between the 2 groups (P<0.05), as shown
in Table 2.
Swallowing Function
At admission, there were no significant differences in the
FOIS or PAS scores between the 2 groups (P>0.05). After
treatment, both groups improved significantly in FOIS
and PAS scores, while there were significant differences
in between the 2 groups (P<0.05), as shown in Tables 3
and 4. Moreover, there were no cases with deterioration of
dysphagia. Generally, the IOE group exhibited better appetite, compliance, and willingness to eat than the NG group.
May 2024 1145
Clinical Trial
the study team. Participants were instructed to report any
untoward medical occurrences or side effects related to the
intervention, and these reports were documented in detail. The
study team also conducted periodic assessments to detect
any potential adverse events and analyze the pathogenesis.
Once an adverse event was identified, it was classified and
graded according to the Common Terminology Criteria for
Adverse Events to ensure consistency and comparability
across different studies.
IOE in Patients With Bulbar Palsy After Stroke
IOE in Patients With Bulbar Palsy After Stroke
Clinical Trial
Zeng et al
Figure. Flowchart.
IOE indicates intermittent oro-esophageal tube feeding; and NG, nasogastric tube feeding.
Stroke-Associated Pneumonia and Depression
Adverse Events
At admission, there were no significant differences in
stroke-associated pneumonia (positive/negative) or
depression (positive/negative) between the 2 groups
(P>0.05). After treatment, both groups showed significant improvement in stroke-associated pneumonia,
although there were significant differences in between
the 2 groups (P<0.05). In addition, there were 8 new
cases of pneumonia in the NG group. After treatment, the
IOE group showed a significant improvement in depression, whereas deterioration (insignificant, P>0.05) was
observed in the NG group. No new cases of depression
were observed in the IOE group, whereas there were 12
new cases of depression-positive (6 turned negative) in
the NG group, as shown in Table 5.
Both the groups reported adverse events related to
the intervention. No grade III or more severe adverse
events were observed in either group. Additionally, patients using IOE reported a significantly lower
(P<0.05) occurrence of reflux, throat discomfort, and
fever (Table S1).
1146 May 2024
DISCUSSION
In general, this study supported the superiority of IOE
over NG, which was consistent with the previous research
applying IOE to various neurological disorders.24 Patients
with bulbar palsy after ischemic stroke typically experience severe dysphagia, resulting in a rapid decrease in
Stroke. 2024;55:1142–1150. DOI: 10.1161/STROKEAHA.123.046122
Zeng et al
Table 1.
IOE in Patients With Bulbar Palsy After Stroke
Basic Characteristics
Table 2.
The NG
group (n=74)
Male
51 (68.92)
42 (56.76)
Female
23 (31.08)
32 (43.24)
Age, y; x̄ ± s
56.32±5.42
54.83±6.32
0.126
10.26±3.17
10.98±2.47
0.125
Sex, n (%)
Course of disease, d; x̄ ± s
P
value
0.126
Smoking, n (%)
0.150
Yes
56 (75.68)
48 (64.86)
No
18 (24.32)
26 (35.14)
Yes
65 (87.84)
57 (77.03)
No
9 (12.16)
17 (22.97)
Suffering
47 (63.51)
41 (55.41)
Not suffering
27 (36.49)
33 (44.59)
Suffering
68 (91.89)
61 (82.43)
Not suffering
6(8.11)
13 (17.57)
Yes
21 (28.38)
29 (39.19)
No
53 (71.62)
45 (60.81)
Left
28 (37.84)
37 (50.00)
Right
38 (51.35)
33 (44.59)
Both
8 (10.81)
4 (5.41)
7 (9.46)
11 (14.86)
Alcohol intake, n (%)
0.083
Type II diabetes, n (%)
ALB (g/L)
PA (mg/L)
The NG group (n=74)
At admission
19.29±1.03
31.87±1.03
264.19±17.21
After treatment
19.41±0.98
32.28±0.81
270.31±15.08
P value
0.489
0.007**
0.028*
At admission
19.36±0.95
32.05±1.27
259.81±15.33
After treatment
19.77±1.03
32.71±0.94
278.15±13.81
P value
<0.013*
<0.001***
<0.001***
P (between groups
after treatment)
0.002**
0.003**
0.001**
The IOE group (n=74)
ALB indicates albumin; BMI, body mass index; IOE, intermittent oroesophageal tube feeding; NG, nasogastric tube feeding; and PA, prealbumin.
*P<0.05, **P<0.01, ***P<0.001.
0.085
Atrial fibrillation, n (%)
0.215
Multiple ischemic lesions, n (%)
0.314
In the cerebellum
13 (17.57)
8 (10.81)
0.239
National Institutes of Health
Stroke Scale (points, x̄ ± s)
17.18±3.12
16.79±2.54
0.406
I
47 (63.51)
53 (72.60)
II
27 (36.49)
21 (28.38)
4
7 (9.46)
2 (2.70)
5
9 (12.16)
16 (21.62)
6
38 (51.35)
41 (55.41)
7
17 (23.01)
13 (17.57)
FOIS level, n (%)
0.295
PAS level, n (%)
0.518
3 (4.05)
its invasiveness. Therefore, exploring new enteral nutrition approaches is of practical significance.
Nutritional Status
0.164
Stroke side, n (%)
8
BMI (kg/m2)
0.417
Hypertension, n (%)
In the brainstem
Group
2 (2.70)
All the data were based on the medical record. Smoking Yes: within 3 y before
the onset of stroke, smoking at least 1 cigarette per week. Alcohol intake Yes:
within 3 y before the onset of stroke, drinking alcohol at least once per month.
FOIS indicates Functional Oral Intake Scale; IOE, intermittent oro-esophageal
tube feeding; NG, nasogastric tube feeding; and PAS, Penetration-Aspiration
Scale.
intake, continuous weight loss, and severe deficiency of
vitamins and minerals.25 This can easily result in malnutrition. In Western countries, percutaneous endoscopic
gastrostomy is the primary choice for addressing this
issue. However, it is not widely used in Asia because of
Stroke. 2024;55:1142–1150. DOI: 10.1161/STROKEAHA.123.046122
This study demonstrated that, compared with NG, IOE
can improve the nutritional status of patients. Although
we set the same nutritional standards as the guidelines
for all patients, the actual intake of the patients was
influenced by various factors. In clinical practice, patients
using IOE showed greater appetite and higher compliance, with a significantly higher daily intake than patients
using NG. In addition, to reduce reflux, a single feeding
amount for patients using NG was not recommended
to exceed 200 mL.16 In contrast, IOE did not affect the
function of the lower esophageal sphincter and posed a
minimal risk of reflux. Therefore, it facilitated relatively
adequate feeding amount.9,10 Moreover, IOE was aligning more with the physiological pattern of normal eating
than NG. This is manifested specifically as IOE being
inserted orally rather than through the nasal cavity, with
longer intervals between feedings compared with NG,
Table 3.
Comparison of FOIS
FOIS level (n)
Group
I
II
III
IV
V
VI
VII
At admission
53
21
0
0
0
0
0
After treatment
30
16
19
7
2
0
0
At admission
47
27
0
0
0
0
0
After treatment
4
7
40
15
4
3
1
P (between groups after
treatment)
<0.001***
P value
The NG group (n=74)
<0.001***
The IOE group (n=74)
<0.001***
FOIS indicates Functional Oral Intake Scale; IOE, intermittent oro-esophageal
tube feeding; NG, nasogastric tube feeding; and PAS, Penetration-Aspiration
Scale.
***P<0.001.
May 2024 1147
Clinical Trial
The IOE
group (n=74)
Item
Comparison of Nutritional Status
Zeng et al
IOE in Patients With Bulbar Palsy After Stroke
Clinical Trial
Table 4. Comparison of PAS
PAS level (n)
Group
1
2
3
4
5
6
7
8
P value
The NG group (n=74)
At admission
0
0
0
2
16
41
13
2
After treatment
0
1
6
19
37
9
2
0
<0.001***
The IOE group (n=74)
At admission
0
0
0
7
9
38
17
3
After treatment
1
14
20
29
8
2
0
0
P (between groups
after treatment)
<0.001***
<0.001***
IOE indicates intermittent oro-esophageal tube feeding; NG, nasogastric tube
feeding; and PAS, Penetration-Aspiration Scale.
***P<0.001.
and without the need for indwelling within the patient’s
body.13 Based on this, IOE posed less negative impact
on the digestive systems and contributed to improved
digestion and absorption. In addition, previous studies
have indicated that prolonged placement of a feeding
tube can stimulate the body, resulting in inflammation
and low-grade fever, which subsequently decreases the
activity of various digestive enzymes, ultimately affecting
digestive function.26 These findings partially support our
results.
Swallowing Function
The improvement in swallowing function observed in
both groups can primarily be attributed to the recovery
of the patients’ health condition and their participation
in swallowing rehabilitation training. As the treatment
progressed, the brain and nervous system underwent
a process of neuroplasticity, which involved the reorganization and repair of neural connections, resulting
in limited functional recovery. Swallowing rehabilitation training also contributed to the enhancement of
coordination among relevant nerves and muscles, as
well as the improvement of muscle strength and range
of motion.9 However, the significant difference was
observed between the 2 groups. A potential mechanism
might be that during tube insertion, IOE could stimulate
the base of the tongue, which enhanced tongue tension by triggering the swallowing reflex. This strengthened upward movement of the larynx, promoting the
restoration of coordinated swallowing movements.27
Moreover, the bending of the tube also stimulated the
pharyngeal wall, affecting the pharyngeal branch of the
vagus nerve and triggering the pharyngeal reflexes.26
By simulating the normal swallowing process, each
insertion of the IOE tube provided physiological training for the swallowing-related muscles, which helped
promote the recovery of oral and pharyngeal motor
function in patients. Furthermore, prompt removal of
the tube after feeding can prevent interference with
rehabilitation training and nasal blockage, thus allowing patients to breathe comfortably.
In contrast, the NG maintained the nasopharynx and
upper esophageal sphincter in an extended open state,
leading to heightened resistance during palate elevation during swallowing and a delayed pharyngeal reflex.
It also interfered with the movement of the tongue.28
Consequently, this can result in the potential development of disuse atrophy in the swallowing function.13
Additionally, IOE allowed the esophagus to function and
hence may contribute to the improvement of dysphagia.
However, as there is limited research on dysphagia in
the esophageal phase, further exploration is needed to
fully understand the mechanisms involved. Some scholars have also proposed a vicious cycle in which malnutrition caused by dysphagia can further worsen the
patient’s swallowing impairment.29 Under this circumstance, IOE can not only improve the nutritional status,
but also enhance swallowing function through complex
neural feedback mechanisms. Therefore, IOE serves
as both the nutrition support mode and the swallowing
function training.
Stroke-Associated Pneumonia and Depression
*P<0.05, ***P<0.001.
The prevalence of pneumonia in patients with stroke
with indwelling gastric tubes was reported as 35%.30
According to previous study, the main cause of aspiration pneumonia in patients with stroke with dysphagia
was the repeated entry of bacteria-infected secretions
or ingested food into the airway.31 NG affected the
contraction function of the patient’s cardia and caused
persistent foreign body sensation in the posterior pharyngeal wall. This increased the risk of both refluxaspiration and swallowing-aspiration, leading to an
elevated incidence of pneumonia.32 Furthermore, NG
can also cause irritation and damage to the mucous
membranes of the throat and trachea, making them
more susceptible to infection and inflammation, further
1148 May 2024
Stroke. 2024;55:1142–1150. DOI: 10.1161/STROKEAHA.123.046122
Table 5. Comparison of Stroke-Associated Pneumonia and
Depression (n, %)
Group
At admission
After
treatment
P (withingroup)
Stroke-associated pneumonia (positive)
The IOE group (n=74)
46 (62.16)
3 (4.05)
<0.001***
The NG group (n=74)
39(52.70)
26(35.14)
<0.031*
P (between-group)
0.245
<0.001***
Depression (positive)
The IOE group (n=74)
31(41.89)
1(1.35)
<0.001***
The NG group (n=74)
38(51.35)
44(59.46)
<0.321
P (between-group)
0.249
<0.001***
Zeng et al
Strengths and Weakness
This is the first study to explore the effect of IOE in
patients with dysphagia with bulbar palsy after ischemic stroke. We conducted a detailed investigation of
patients’ basic information, and the outcomes covered
several aspects. However, this study has some limitations. First, although we calculated the sample size, it
was a small-scale study. Second, despite conducting
a multicenter study, the participating hospitals were all
concentrated in central China, which may have led to a
lack of sample representativeness. In addition, we were
unable to successfully complete the follow-up work,
which indicated that this study could only illustrate the
short-term effects of IOE. Subsequent large-scale, multicenter cohort studies should be conducted to address
these issues.
Conclusions
IOE is safer and more effective than NG in improving
nutritional status, swallowing function, stroke-associated
pneumonia, and depression in patients with dysphagia
with bulbar palsy after ischemic stroke undergoing routine treatment and swallowing rehabilitation training.
ARTICLE INFORMATION
Received December 6, 2023; final revision received February 22, 2024; accepted
February 28, 2024.
Affiliations
School of Public Health, Zhengzhou University, China (H.Z., W.Z.). Department
of Rehabilitation Medicine, Huashan Hospital Fudan University, Shanghai, China
(Junfa Wu). National Center for Neurological Disorders, Shanghai, China (Junfa
Stroke. 2024;55:1142–1150. DOI: 10.1161/STROKEAHA.123.046122
Wu). Mianyang Central Hospital, China (Jihong Wei). Department of Rehabilitation Medicine, The First Affiliated Hospital of Zhengzhou University, China (H.L.,
L.W., X.Z.). NHC Key Laboratory of Prevention and treatment of Cerebrovascular
Diseases, Zhengzhou, China (X.Z.)
Sources of Funding
This work was supported by the Non-Profit Central Research Institute Fund of the
Chinese Academy of Medical Sciences (2020-PT310-01).
Disclosures
None.
Supplemental Material
Figure S1
Table S1
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increasing the risk of aspiration. Conversely, IOE caused
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