brain
sciences
Article
Exploring the Influence of Dysphagia and Tracheostomy on
Pneumonia in Patients with Stroke: A Retrospective
Cohort Study
Yong Dai 1,2 , Jia Qiao 2 , Qiu-Ping Ye 2 , Xin-Ya Li 1 , Jia-Hui Hu 1 and Zu-Lin Dou 1,2, *
Citation: Dai, Y.; Qiao, J.; Ye, Q.-P.; Li,
X.-Y.; Hu, J.-H.; Dou, Z.-L. Exploring
the Influence of Dysphagia and
Tracheostomy on Pneumonia in
Patients with Stroke: A Retrospective
Cohort Study. Brain Sci. 2022, 12,
1664. https://doi.org/10.3390/
brainsci12121664
Academic Editors: Simona Lattanzi
and Yvonne Teuschl
Received: 20 October 2022
Accepted: 28 November 2022
Published: 3 December 2022
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Copyright: © 2022 by the authors.
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4.0/).
Brain Sci. 2022, 12, 1664. https://doi.org/10.3390/brainsci12121664
1 Clinical Medical College of Acupuncture-Moxibustion and Rehabilitation, Guangzhou University of Chinese
Medicine, Guangzhou 510006, China
2 Department of Rehabilitation Medicine, the Third Affiliated Hospital of Sun Yat-sen University,
Guangzhou 510630, China
* Correspondence: douzulin@mail.sysu.edu.cn; Tel.: +86-189-22102718
Abstract: Background: Pneumonia is common in patients with tracheostomy and dysphagia. How-
ever, the influence of dysphagia and tracheostomy on pneumonia in patients with stroke remains
unclear. The aim of this study was to explore the risk factors related to pneumonia, and the associ-
ation between dysphagia, tracheostomy and pneumonia in patients with stroke was investigated.
Methods: Patients with stroke who experienced tracheostomy and dysphagia were included and
divided into two groups based on record of pneumonia at discharge. Clinical manifestations and
physical examination were used to diagnose pneumonia, whereas clinical swallowing examination,
and videofluoroscopy swallowing studies (VFSS) were used to evaluate swallowing function. Results:
There were significant differences between the pneumonia group and the no pneumonia group in
total tracheostomy time (6.3 ± 5.9 vs. 4.3 ± 1.7 months, p = 0.003), number of instances of ventilator
support (0.41 ± 0.49 vs. 0.18 ± 0.38, p = 0.007), PAS score (5.2 ± 1.92 vs. 4.3 ± 1.79, p = 0.039),
impaired or absent cough reflex (76.4 vs. 55.6%, p = 0.035), oropharyngeal phase dysfunction (60.6
vs. 40.8%, p = 0.047), length of hospital stay (36.0 ± 7.2 vs. 30.5 ± 11.7 days, p = 0.025) and direct
medical costs (15,702.21 ± 14,244.61 vs. 10,923.99 ± 7250.14 United States dollar [USD], p = 0.042).
Multivariate logistic regression showed that the total tracheostomy time (95% confidence interval
[CI], 1.966–12.922, p = 0.001), impaired or absent cough reflex (95% CI, 0.084–0.695, p = 0.008), and
oropharyngeal phase dysfunction (95% CI, 1.087–8.148, p = 0.034) were risk factors for pneumonia.
Spearman’s correlation analysis demonstrated that PAS scores were significantly correlated with
cough reflex dysfunction (r = 0.277, p = 0.03), oropharyngeal phase dysfunction (r = 0.318, p < 0.01)
and total tracheostomy time (r = 0.178, p = 0.045). The oropharyngeal phase dysfunction was sig-
nificantly correlated with cough reflex (r = 0.549, p < 0.001) and UES opening (r = 0.643, p < 0.01).
Conclusions: Tracheostomy and dysphagia increased the risk of pneumonia in patients with stroke.
Total tracheostomy time, duration of ventilator support, degree of penetration and aspiration, and
oropharyngeal phase dysfunction are risk factors. Given this, we also found that there may be a
correlation between tracheostomy and dysphagia.
Keywords: tracheostomy; stroke; pneumonia; dysphagia; retrospective study
1. Introduction
Stroke is the second leading cause of death and the third leading cause of disability
worldwide, and the burden of this disease is rapidly increasing in low- and middle-income
countries [1,2]. Tracheostomy is a vital rescue intervention for patients with stroke who
have reduced airway protection reflexes, and thus high risk of aspiration and/or depressed
consciousness [3]. It is a surgical procedure that involves cutting into the trachea and
inserting a tube into the opening. These artificial airways provide direct, unobstructed
lower respiratory tract access to maximize ventilation, expedite oxygen entry, and facilitate
https://www.mdpi.com/journal/brainsci
Brain Sci. 2022, 12, 1664 2 of 12

secretion management [4]. Despite its benefits, tracheostomy often co-exists with dyspha-
gia (11% to 93%) [5,6], and is associated with adverse medical outcomes, most notably
increased risk of pneumonia and malnutrition [7]. In addition, patients with dysphagia
and pneumonia are more likely to develop worse functional outcomes, higher mortality,
and increased readmissions and institutionalization [8].
Previously, aspiration after tracheostomy has been reported in 50–87% of patients [9],
and the subglottic secretions above the endotracheal cuff are associated with bacteria
colonization of lower respiratory tract, resulting in pneumonia [10]. There are several
posited explanations for why pneumonia occurs in patients with tracheostomy and dys-
phagia, including decreases in the strength of sensory input, disuse atrophy of laryngeal
structures, and reduced subglottic air pressure [11]; however, this risk does not appear to
be widely recognized [12] as the relationship between tracheostomy and pneumonia is
controversial, and inflated endotracheal tube cuffs to prevent aspiration of water into the
lung have been reported [8]. Currently, the risks factors related to pneumonia in patients
with dysphagia and tracheostomy remains unclear [13,14], and the relationships among
tracheostomy, dysphagia and pneumonia in patients with stroke have not been well de-
scribed [15,16]. Therefore, the current study aimed to explore the influence of dysphagia
and tracheostomy on pneumonia in patients with stroke, and to clarify possible association
between dysphagia, tracheostomy and pneumonia.

2. Materials and Methods

2.1. Study Design and Subjects
This was a retrospective study; the data were extracted from the cohort database of
the Third Affiliated Hospital of Sun Yat-sen University from January 2010 to June 2022.
Stroke patients who had undergone tracheostomy were identified, and detailed clinical
information was collated, including medical records, auxiliary examinations, and treatment
processes. A standardized identified data collection form was used to collect data from the
medical records. Collected data included: demographic details (age, sex); stroke type; stroke
location; comorbidities (coronary heart disease, hypertension, diabetes, hyperlipidemia);
personal history (smoking and drinking); videofluoroscopy swallowing study (VFSS)
assessment results, including the penetration–aspiration scale (PAS), upper esophageal
sphincter (UES) opening, cough reflex, and swallowing phase; total tracheostomy time
(the duration of tracheal cannula), number of instances of ventilator support, hospital
length of stay, and direct medical costs. Dysphagia was confirmed by specifically-trained
speech–language therapists specializing in post-stroke dysphagia based on swallowing
screening, detailed clinical swallowing evaluation, and VFSS examination. Ethical approval
was obtained from the ethical committees of the Third Affiliated Hospital of Sun Yat-sen
University (02-351-01).

2.2. Inclusion and Exclusion Criteria

The inclusion criteria were age > 18 years; stroke was diagnosed and confirmed by
computed tomography and/or magnetic resonance imaging of the brain, performed at the
acute stage in all patients (hemorrhagic or ischemic stroke, such as subdural hematoma, sub-
arachnoid hemorrhage, intracerebral hemorrhage, and ischemia); tracheostomy performed
after stroke; swallowing function evaluation by speech language therapists at admission
to the rehabilitation department; and pneumonia diagnosed during hospitalization af-
ter tracheostomy. The exclusion criteria were incomplete case information; neurological
diseases other than stroke (e.g., brain tumor, Parkinson’s disease, neuromyelitis optica);
pre-existing diseases causing dysphagia (e.g., structural abnormalities of the mouth or
throat, esophageal cancer); diagnosis of pneumonia at admission; high-risk diseases such as
chronic obstructive pulmonary disease, lung transplantation, immune system dysfunction,
respiratory disease; severe cognitive impairment, including delirium, dementia, coma, veg-
etative state; and other surgeries such as neck surgery, lung transplantation, thoracotomy,
chemotherapy for nasopharyngeal cancer, and tongue cancer.
Brain Sci. 2022, 12, 1664 3 of 12

2.3. Evaluation Methods

2.3.1. Pneumonia Diagnosis
Pneumonia is identified using a combination of imaging, clinical and laboratory
criteria. In the current study, the diagnostic criteria for pneumonia were as follows: (A) The
relevant clinical characteristics of pneumonia: new onset of cough or exacerbation of
symptoms of existing respiratory diseases, with or without purulent sputum, chest pain,
dyspnea, or hemoptysis; fever; evidence of pulmonary consolidation and/or moist rales;
Peripheral white blood cell count (WBC) > 10 × 109 /L or <4 × 109 /L, with or without a left
shift. (B) The chest radiograph showing new patchy infiltrates, ground-glass opacities, or
interstitial changes, lobar or segmental consolidation, with or without pleural effusion [17].
Clinical diagnosis was established if a patient satisfied criterion B and any one condition of
criterion A. Patients with tuberculosis, pulmonary tumor, non-infectious interstitial lung
disease, pulmonary edema, atelectasis, pulmonary embolism, pulmonary eosinophilia, and
pulmonary vasculitis were excluded [18].

2.3.2. Swallowing Function Evaluation

All tracheostomy patients underwent clinical swallowing evaluations at admission to
the rehabilitation department. Typical components included dysphagia specific anamnesis,
dysphagia screening and examination, and instrumental examination methods [19]. The
underlying diseases, comorbidities, drug history, previous diagnosis and therapeutic trials
and dysphagia specific issues were also evaluated [20], and, in particular, there was a
specific need to ask about the occurrence of pneumonia.
The volume–viscosity swallow test (V-VST) was used to detect patients’ signs of
impaired safety and efficacy of swallow [21]. Patients start the test with a 5 mL medium
bolus, followed by 10 and 20 mL, then perform with low viscosity boluses following the
same volumetric approach, and finally complete the test with high viscosity boluses. The
V-VST should be ended if any safety impairment with high viscosity happened [22]. If
the V-VST is positive, tracheostomized patients whose neurological and vital signs were
stable undertook the VFSS examination at admission to the rehabilitation department with
specifically trained speech-language therapists [23]. The first record was included in the
analysis. The PAS score, UES opening, cough reflex, and swallowing phase dysfunction
obtained from VFSS were adopted. Videofluoroscopy was performed using a fluoroscopy
unit (Siemens ICONOS R200, Siemens AG, Erlangen, Germany, 2005) with an image rate
of 30 pulses/second. The procedure was performed according to the modified Logemann
protocol [24].
PAS is an 8-point scale used to evaluate the severity of penetration and aspiration. The
higher the score, the more severe the penetration and aspiration symptoms [25]. Complete
airway protection was given a PAS score of 1, while the impermanent entry of the bolus into
the laryngeal vestibule (above the vocal folds) was given a score of 2. If the bolus was not
cleared from the laryngeal vestibule the score was 3–5 according to the depth and amount.
Scores of 6–8 were given in the case of aspiration, when the bolus crossed the vocal folds
into the trachea. In cases with multiple sub-swallows in one swallowing trial, swallowing
safety was recorded based on the worst score obtained on the PAS. Swallowing dysfunction
in the oral, pharyngeal, and esophageal phases were recorded. The definitions of the
different phases are shown in Table 1 [26]. Different measures were analyzed using Image J
open-source software (National Institutes of Health, Bethesda, Maryland) by specifically
trained speech-language therapists with more than two years of work experience. During
the analysis, the video was played at a speed of 30 frames/s and played back frame-by-
frame; each video image was rated in duplicate by two trained raters, and any discrepancies
across ratings were resolved through consensus with a third experienced rater [27].
Brain Sci. 2022, 12, 1664 4 of 12

Table 1. Operational definitions of different phases of swallowing.

Phases of
Operational Definitions Start Point Endpoint
Swallowing
Before the swallowing
reaction begins, the food
Oral preparatory
is chewed and formed The bolus was processed in the oral cavity
phase
into a bolus in the oral
cavity
The head of the bolus
The tongue voluntary reaches the
The passage of food
Oral propulsive presses the collected intersection of the
bolus from the oral cavity
phase bolus against the mandibular ramus
to the pharynx
palate and the base of the
tongue
The bolus from the Bolus passing the
The upper esophageal
Pharyngeal phase pharynx to the esophagus ramus of the
sphincter relaxation
entrance mandible
The bolus goes down the
The upper esophageal The bolus into the
Esophageal phase esophagus and into the
sphincter relaxation stomach
stomach

2.4. Statistical Analysis

Continuous variables were tested for normality using the Kolmogorov–Smirnov test.
The Student’s t-test was used for continuous data and Fisher’s exact test for categorical
data. Differences between groups were determined using Pearson’s chi-squared test (χ2) or
Fisher’s exact test (as appropriate). PAS was analyzed using the Wilcoxon rank sum test in
the prespecified subgroup analysis. Risk factors for pneumonia were investigated using
multivariate logistic regression. The correlation between PAS, UES opening, impaired
or absent cough reflex, oropharyngeal phase dysfunction, total tracheostomy time, and
number of instances of ventilator support was analyzed using the Spearman correlation
analysis. All comparisons were two-tailed. The statistical significance level was set at
p < 0.05. All statistical analyses were performed using IBM SPSS Statistics for Windows,
version 23 (IBM Corp., Armonk, NY, USA, 2015).

3. Results
A total of 555 patients with tracheostomy after stroke were screened, of which 180 pa-
tients diagnosed with dysphagia were included in the analysis of risk factors for pneumonia,
including 140 patients in the pneumonia group and 40 in the no pneumonia group. In
this study, dysphagia was diagnosed based on swallowing function assessment, including
clinical symptoms, FOIS, V-VST, or VFSS. To further explore the relationship between
dysphagia and pneumonia, only 116 patients who underwent VFSS were included in the
subgroup analysis (Figure 1).

3.1. The Influence of Tracheostomy on Pneumonia

Among 180 patients with dysphagia, 140 were in the pneumonia group, and 40 were
in the no pneumonia group. There were no significant differences in terms of sex, age,
stroke type, stroke location, feeding behavior, and history of disease between the two
groups (p > 0.05) (Table 2). However, the comparative analysis demonstrated that the total
tracheostomy time for patients in the pneumonia group (6.3 ± 5.9 months) was significantly
longer than for patients in the no pneumonia group (4.3 ± 1.7 months) (p = 0.037). A signif-
icant difference was found in the number of instances of ventilator support between the
pneumonia (0.41 ± 0.49) and the no pneumonia groups (0.18 ± 0.38) (p = 0.007). In addition,
a longer length of hospital stays and higher direct medical costs during hospitalization
were observed in the pneumonia group (36.0 ± 7.2 days; 15,702.21 ± 14,244.61 USD, re-
Brain Sci. 2022, 12, 1664 5 of 12

Brain Sci. 2022, 12, x FOR PEER REVIEW  5  of  13 

  than in the no pneumonia group (30.5 ± 11.7 days; 10,923.99 ± 7250.14 USD,
spectively)
respectively) (p = 0.025; p = 0.042, respectively).

. 
Figure 1. The flow chart of the study design.
Figure 1. The flow chart of the study design. 
Table 2. Clinical characters of tracheostomy patients with dysphagia after stroke.
3.1. The Influence of Tracheostomy on Pneumonia 
Pneumonia Group No Pneumonia
Among 180 patients with dysphagia, 140 were in the pneumonia group, and 40 were 
Variables p-Value
(n = 140) Group (n = 40)
in the no pneumonia group. There were no significant differences in terms of sex, age, 
Male,
stroke  type,  n (%)
stroke  100 (71.5)and  history  of 31
location,  feeding  behavior,  (77.5) between 0.447
disease  the  two 
Age (year), mean (SD) 54.0 (15.7) 54.8 (14.2)
groups (p > 0.05) (Table 2). However, the comparative analysis demonstrated that the total  0.341
Stroke type, n (%)
tracheostomy  time for  patients in  the  pneumonia 
Hemorrhagic 52 (37.1) group  (6.3 ± 5.9  months)  was  signifi‐
12 (30)
cantly longer than for patients in the no pneumonia group (4.3 ± 1.7 months) (p = 0.037).  0.405
Ischemic 89 (62.9) 28 (70)
A significant difference was found in the number of instances of ventilator support be‐
Stroke site, n (%)
0.995
Supratentorial 78 (55.7) 22 (55)
tween the pneumonia (0.41 ± 0.49) and the no pneumonia groups (0.18 ± 0.38) (p = 0.007). 
Infratentorial 35 (25) 10 (25)
In addition, a longer length of hospital stays and higher direct medical costs during hos‐
Other 27 (19.3) 8 (20)
pitalization were observed in the pneumonia group (36.0 ± 7.2 days; 15702.21 ± 14244.61 
Feeding behavior, n (%)
USD, respectively) than in the no pneumonia group (30.5 ± 11.7 days; 10923.99 ±7250.14 
Oral feeding 27 (19.3) 9 (22.5) 0.654
USD, respectively) (p = 0.025; p = 0.042, respectively). 
Gastric tube feeding 64 (45.7)   15 (37.5) 0.356
Intermittent intubation feeding 17 (12.2) 7 (17.5) 0.379
Partial oral feeding 32 (22.8) 9 (22.5)
Table 2. Clinical characters of tracheostomy patients with dysphagia after stroke.  0.962
History of disease, n (%)
Coronary Heart Disease Pneumonia group (n = 
16 (11.4) No pneumonia group 
5 (12.5) 0.852
Variables.  p‐Value 
Hypertension 85 (60.7)
140)  26 (65.0)
(n = 40)  0.623
Diabetes
Male, n (%)  33 (23.5)
100(71.5)  10 (25.0)
31(77.5)  0.852
0.447 
Hyperlipidemia 11 (7.8) 5 (12.5) 0.363
Age (year), mean (SD) 
Smoker, n (%) 54.0(15.7) 
21 (15.0) 54.8(14.2) 
4 (10.0) 0.584
0.341 
Stroke type, n (%) 
Drinker, n (%)  
15 (10.7)  
3 (7.5) 0.765
 
Total tracheostomy
Hemorrhagic times (month) 6.3 ± 5.9
52(37.1)  4.3 ± 1.7
12(30)  0.037 *
Number of Ischemic 
instances of ventilator 0.41 (0.493) 0.18 (0.385) 0.405 
0.007 *
89(62.9)  28(70) 
support, mean (SD)  
Stroke site, n (%) 
Length of hospital stay (day)
 
36.0 ± 7.2
 
30.5 ± 11.7 0.025 *
0.995 
Supratentorial 
Direct medical costs (USD) 78(55.7) 
15,702.21 ± 14,244.61 22(55) 
10,923.99 ± 7250.14 0.042  *
Infratentorial 
Note: SD, standard 35(25) 
deviation; USD, United States Dollar; * p < 0.05. 10(25) 
 
Other    27(19.3)  8(20) 
Feeding behavior, n (%)       
Oral feeding  27(19.3)  9(22.5)  0.654 
Brain Sci. 2022, 12, 1664 6 of 12

3.2. Subgroup Analysis of the Influence of Dysphagia on Pneumonia

Finally, 89 and 27 patients in the pneumonia and no pneumonia group, respectively,
were included to explore the relationship between dysphagia and pneumonia. A signif-
icant difference in PAS scores was found between the pneumonia (5.2 ± 1.92) and the
no pneumonia group (4.3 ± 1.79) (p = 0.039) (Table 3). Impaired/absent cough reflex
was more common in the pneumonia (76.4%) compared with the no pneumonia group
(55.6%) (p = 0.035) (Table 3). However, no difference was found between the groups in UES
opening (Table 3). Furthermore, there were statistical differences in oropharyngeal phase
dysfunction between the pneumonia and no pneumonia subgroups (p = 0.047), however,
no differences were found for other phases of swallowing (Table 4). The post hoc testing of
differences in the phase of swallowing between groups are showed in Table 5.

Table 3. Analysis of swallowing function on pneumonia.

Pneumonia No Pneumonia
Group Group p-Value Effect
Variables 95% CI
Size
n = 89 n = 27
PAS, mean (SD)
5.2 (1.92) 4.3 (1.79) 0.039 *
UES opening, n (%)
0.503 0.458 0.024 to 0.893
Complete
59 (66.3) 16 (59.3) 0.124 −0.24 to 0.489
Not complete
30 (33.7) 11 (40.7)
Cough reflex, n (%)
0.035 *
Present
21 (23.6) 12 (44.4) 0.399 0.028 to 0.770
Dysfunction
68 (76.4) 15 (55.6)
(impaired/absent)
Note: SD, standard deviation; UES, Upper Esophageal Sphincter; PAS, Penetration-Aspiration Scale; * p < 0.05.
95% CI, 95% Confidence Interval.

Table 4. Differences in the phase of swallowing between groups.

Pneumonia No Pneumonia
Effect
The Phase of Swallowing, n (%) Group Group p Value 95% CI
Size
(n = 89) (n = 27)
Oral phase 8 (8.9) 3 (11.1) 0.742 0.061 −0.303 to 0.425
Pharyngeal phase 18 (20.2) 9 (33.3) 0.158 0.264 −0.102 to 0.631
Esophageal phase 0 0
Oral + Pharyngeal phase (Oropharyngeal) 54 (60.6) 10 (37.1) 0.031 * 0.408 0.037 to 0.780
Pharyngeal + Esophageal phase 4 (4.5) 2 (7.4) 0.918 0.019 −0.344 to 0.383
Oral + Pharyngeal + Esophageal phase 5 (5.7) 3 (11.1) 0.580 0.102 −0.261 to 0.467
Note: * p < 0.05. 95% CI, 95% Confidence Interval.

Table 5. Post hoc testing between groups.

The Phase of Swallowing, Pneumonia Group No Pneumonia Group

n (Adjusted Residual) (n = 89) (n = 27)
Oral phase 8 (−0.3) 3 (0.3)
Pharyngeal phase 18 (−1.4) 9 (1.4)
Esophageal phase 0 0
Oral + Pharyngeal phase (Oropharyngeal) 54 (2.2) * 10 (−2.2)
Pharyngeal + Esophageal phase 4 (−0.6) 2 (0.6)
Oral + Pharyngeal + Esophageal phase 5 (−1) 3 (1)
Note: Adjusted residuals appear in parentheses to the right of observed frequencies. * The difference is statistically
significant.

3.3. The Risk Factors of Pneumonia

There were significant differences in total tracheostomy time, number of instances of
ventilator support, PAS score, cough reflex, and oropharyngeal phase dysphagia through
Brain Sci. 2022, 12, 1664 7 of 12

descriptive statistics (p < 0.05, Table 2). When these factors were included in the logis-
tic regression analysis, the results suggested that total tracheostomy time; (odds ratio
[OR] = 5.040; p = 0.001), cough reflex dysfunction (OR = 0.241; p = 0.008), and oropharyn-
geal phase dysfunction (OR = 2.976; p = 0.034) were risk factors for pneumonia in patients
with stroke, dysphagia and tracheostomy (Table 6).

Table 6. The multivariate logistic regression analysis for the risk factors of pneumonia.

Variables OR 95% CI p-Value

Total tracheostomy time 5.040 1.966 to 12.922 0.001 **
Cough reflex dysfunction 0.241 0.084 to 0.695 0.008 **
Present of oropharyngeal phase dysfunction 2.976 1.087 to 8.148 0.034 *
Note: OR, odds ratio; 95% CI, 95% Confidence interval; * p < 0.05; ** p < 0.01.

3.4. Correlation Analysis of Tracheostomy and Dysphagia

Spearman’s correlation analysis was performed for PAS scores, UES opening, cough
reflex, oropharyngeal phase dysfunction, total tracheostomy time, and number of instances
of ventilator support. PAS scores were significantly correlated with cough reflex dysfunc-
tion (r = 0.277, p = 0.03), oropharyngeal phase dysfunction (r = 0.318, p < 0.01) and total
tracheostomy time (r = 0.178, p = 0.045). The oropharyngeal phase dysfunction was sig-
nificantly correlated with cough reflex (r = 0.549, p < 0.001) and UES opening (r = 0.643,
p < 0.01) (Table 7).

Table 7. The correlation analysis of tracheostomy and dysphagia.

Oropharyngeal Total Number of

UES Cough
PAS Scores Phase Tracheostomy Instances of
Opening Reflex
Dysfunction Time Ventilator Support
PAS scores 1 0.118 0.277 * 0.318 * 0.178 * 0.024
UES opening 0.118 1 0.139 0.643 ** −0.033 0.36
Cough reflex 0.277 * 0.139 1 0.549 ** −0.010 0.223
Oropharyngeal
0.318 ** 0.643 ** 0.549 ** 1 −0.010 0.034
phase dysfunction
Total
0.178 * −0.033 −0.010 0.59 1 0.016
tracheostomy time
Number of instances of
0.024 0.36 0.223 0.034 0.016 1
ventilator support
Note: * p < 0.05; ** p < 0.01.

4. Discussion
The present study suggests that tracheostomy and dysphagia might increase the
incidence of pneumonia in patients with stroke. In addition, the total tracheostomy time,
impaired or absent cough reflex dysfunction, and oropharyngeal phase dysfunction are
risk factors for pneumonia. Furthermore, there may be a correlation among PAS score,
total tracheostomy time, cough reflex, UES opening and oropharyngeal phase dysfunction.
Lastly, patients with pneumonia may have an increased length of hospital stay and higher
direct medical costs.
We found that patients with tracheostomy, with a longer tracheostomy time and more
ventilator support, were more likely to develop pneumonia. Tracheostomy allows air
to enter the lungs, improving oxygenation and ventilation effectively. However, it is a
double-edged sword, as when breathing occurs through the tube, bypassing from the
mouth, nose, and throat, the risk of aspiration and pneumonia may increase [28,29]. There
were several possible causative mechanisms for pneumonia in patients with tracheostomy.
First of all, tracheostomy leads to pathophysiological changes in the upper airway and
pharyngeal cavity, change in airway resistance and a decrease in pharyngeal pressure
during swallowing, especially the subglottic air pressure [30]. In addition, tracheostomy
Brain Sci. 2022, 12, 1664 8 of 12

bypasses upper airway defense mechanisms, such as upper airway humidification and
ciliary movement, causing desensitization of the larynx and loss of the protective reflex
due to chronic air diversion. Furthermore, the coordination between swallowing and
breathing is impaired in patients with a tracheostomy [31]. Studies have confirmed that
swallowing and breathing are coordinated, which is considered to be one of the mechanisms
of airway protection [32]; additionally, tube cuff compression can result in vocal cord
paresis/paralysis and may prohibit competent airway protection, resulting in insufficient
airway closure, reduced cough reflex, and decreased airway protection, which may increase
the risk of pneumonia [14].
Although several possible causative mechanisms have been suggested, the association
of tracheostomy with an increased incidence of aspiration remains under debate. Some
other experts and scholars believe that a tracheal cannula with an inflated cuff protects from
aspiration, and is thus assumed to lower the risk of pneumonia in these patients [12,13].
The results of this study may serve as supporting evidence. The longer the duration
of endotracheal intubation and tracheostomy time, the greater the damage to airway
integrity. Most studies have reported total tracheostomy time and the benefits of its
reduction [33]. Christopher et al. demonstrated that earlier decannulation has important
clinical benefits for speech and swallowing, and restoring normal respiratory physiology
including cough function [34]. There is also less risk for adverse events and reduced
potential for infection [35]. Moreover, patients with more ventilator support are more likely
to suffer from pneumonia. This may be related to respiratory muscle weakness. Symptoms
of respiratory muscle weakness are common in patients with mechanical ventilation and
long-term intubation, which cause a significant decrease in the ability to cough and clear
secretions, which can develop into pneumonia. Membrane proteolysis can be detected
in patients with invasive mechanical ventilation within 18 to 69 hours. This means that
the respiratory muscles rapidly atrophy [36]. After 24 hours of mechanical ventilation,
respiratory muscle weakness was almost twice as high as limb muscle weakness (63% vs.
34%) [37].
The stage of dysphagia may be related to stroke and tracheostomy. Chang et al. re-
ported that in patients with acute cerebral infarction, dysphagia usually occurs in the oral
and pharyngeal stages [38]. Betts et al. reported that the tube cuff could obstruct the pha-
ryngeal pathway directly [39]. After tracheostomy, the mechanical effects of a tracheostomy
tube may negatively affect swallowing function, including a reduction in laryngeal ele-
vation, less subglottic pressure, reduced vocal fold adduction reflex, increased external
cuff pressure in the esophagus and occurrence of stasis in the supraglottic region, While
the function of food transport in the oral cavity and pharynx is impaired, oropharyngeal
dysphagia occurs, increasing the risk of aspiration [40,41]. These findings were similar to
those in our study; tracheostomized patients after stroke accompanied with pneumonia
tend to manifest oropharyngeal phase dysfunction.
However, recent studies have indicated that the presence of a tracheostomy tube
may not affect the biomechanics or kinematics of swallowing. Terk et al. reported that
tracheostomy did not significantly alter hyoid bone movement and laryngeal excursion,
which are important components of normal pharyngeal swallow biomechanics [42]. Kang
et al., also found that the extubation of a tracheostomy tube did not affect the kinematics of
swallowing, implying no relationship between tracheostomy tube placement and dyspha-
gia [11]. More recently, Park et al. reported that swallowing function did not change before
and after tracheostomy decannulation [40]. In our study, a correlation was observed be-
tween tracheostomy time and PAS score (r = 0.178, p = 0.045), and no correlation was found
in other indicators, such as oropharyngeal phase dysfunction and UES opening, which
may suggest that dysphagia is related to tracheostomy but there is insufficient evidence.
Hence, future study will be needed to verify the relationship between tracheostomy and
dysphagia.
In addition, a significant correlation between dysphagia and pneumonia was found.
Patients with higher PAS scores and impaired cough reflex were more likely to develop
Brain Sci. 2022, 12, 1664 9 of 12

pneumonia, and cough reflex was significantly correlated with PAS score (r = 0.277, p = 0.03).
Coughing is one of the defense mechanisms that can effectively prevent foreign bodies
from entering the airway and lungs, and reduce the risks of aspiration. However, tra-
cheostomized patients often have difficulty in initiating the compressive coughing phase,
and cough flows are typically insufficient [43]. McKim et al. demonstrated that peak cough
flow significantly increased after tracheostomy tube decannulation [44].
Moreover, oropharyngeal phase dysfunction was significantly correlated with cough
reflex (r = 0.549, p < 0.001) and UES opening (r = 0.643, p < 0.001), as well as PAS score
(r = 0.318, p < 0.001). Oropharyngeal dysphagia is a health problem that refers to a distur-
bance in the oral preparatory, oral, and/or pharyngeal phases of swallowing, resulting in
difficulty in eating, drinking, or swallowing. Oropharyngeal aspiration causes frequent
respiratory infections and aspiration pneumonias. Due to the complex pathophysiology
and great differences in etiologies and manifestations, the diagnosis of oropharyngeal
dysphagia remains a challenge [45]. In our study, cough reflex, UES opening, and PAS
score were all related to oropharyngeal phase dysfunction. Therefore, current research
aimed at improving the diagnosis and treatment of oropharyngeal dysphagia still needs to
be further carried out in patients with stroke and tracheostomy.
We found that males were over-represented in this cohort. This may be related to
the epidemiological characteristics of stroke and tracheostomy. A previous review article
focusing on the sex-specific information showed that male stroke incidence rate was 33%
higher than for females [46]. In recent years, genetic factors, the positive effects of estro-
gen on cerebral circulation, and blood pressure were considered as the epidemiological
differences between the sexes [47]. There is no specific report on the relationship between
tracheostomy and gender, but in previous retrospective analyses with large sample sizes,
the risk of tracheostomy complications in male patients was higher than that in female pa-
tients [48]. In summary, the ratio of males in this study is similar to that in previous studies,
which may suggest that males are at higher risk of developing stroke and tracheostomy,
but the specific relationship needs to be studied with a larger sample size.
Patients with pneumonia after tracheostomy experienced a longer length of hospi-
tal stay and higher direct medical costs than those without pneumonia. In the present
study, it means that the burden of pneumonia in patients after stroke, accompanied with
tracheostomy and dysphagia, may be increased; more medical resources are needed for
patients with pneumonia after stroke, such as airway management, drugs, and physiother-
apy. Some studies indicate that pneumonia may be a risk factor that increases the burden
of tracheostomy and stroke [49,50]. More recently, Kaur et al. reviewed the costs of stroke
in low- and middle-income countries, mostly in Asia. The average length of hospital stay
was longest (20 days) in China [51], which was a significantly lower hospital stay than in
this study. Meanwhile, there are many evidence-based guidelines for tracheostomy man-
agement reporting that multidisciplinary methods have benefits for reducing pneumonia
risk, shortening the length of hospital stay and saving costs [7]. We may be able to conduct
research on this in a future study.
The current study had several limitations. First, only 116 patients who had complete
VFSS medical records were included in the subgroup analysis to explore the relationship
between dysphagia and pneumonia. Moreover, we lacked a comparison with patients who
did not have dysphagia. Some parameters are lacking due to the limitations of the database,
such as mechanical ventilation time, type of tracheostomy, laryngeal elevation, and tongue
motility, which may have biased the results. Second, despite our attempts to control for
confounders, there is still a risk of uncontrolled residual confounders, such as differences
in tracheostomy management, consciousness level, or clinical interventions used. Third,
the study was conducted at a single medical center with a unique clinical approach, and
we did not have any information about discharges or other hospitals, which suggests the
need for further validation to determine whether these results could be generalized to other
hospitals or regions. In addition, this study focused only on the phases of swallowing and
not on physiology, and the etiologies of pneumonia were not clarified. Whether the risk of
Brain Sci. 2022, 12, 1664 10 of 12

pneumonia can be reduced by improving dysphagia in stroke patients with tracheostomy

needs to be explored in future studies. Hence, the interpretation of these results should be
undertaken with caution, and more high-quality prospective studies are urgently needed.

5. Conclusions
In summary, tracheostomy and dysphagia may increase the risk of pneumonia in
patients with stroke. The total tracheostomy time, impaired or absent cough reflex, and
oropharyngeal phase dysfunction were the risk factors for pneumonia, and there may be a
correlation among PAS score, tracheostomy time, cough reflex, oropharyngeal phase dys-
function and UES opening. Patients with pneumonia had an increased hospital length of
stay and higher costs. These findings suggest that appropriate management of tracheostomy
combined with precise rehabilitation interventions for dysphagia may be considered to
reduce the risk of pneumonia in patients with stroke, dysphagia and tracheostomy. There-
fore, future prospective studies with larger sample sizes should be conducted to verify
our findings. In addition, the relationship between tracheostomy and dysphagia remains
unclear, and further studies are needed.

Author Contributions: Y.D., J.Q., Q.-P.Y., X.-Y.L. and J.-H.H. have performed data collation and
analysis, Y.D drafted the manuscript and conducted critical editing. J.Q. and X.-Y.L. have contributed
to the illustrations. Z.-L.D. and Q.-P.Y. have carefully supervised this manuscript’s preparation and
writing. All authors have read and agreed to the published version of the manuscript.
Funding: This research was funded by the Natural Science Foundation of China [NSFC, No.
81972159], Natural Science Foundation of China [NSFC, No. 82202807], and the Science and Technol-
ogy Program of Guangzhou [No. 201604020153].
Institutional Review Board Statement: The inclusion met the ethical standards of ethical committees
of the Third Affiliated Hospital of Sun Yat-sen University (02-351-01), and an exemption to informed
consent requirements was granted.
Data Availability Statement: The authors declare that data supporting the findings of this study are
available within the article.
Conflicts of Interest: The authors declare no conflict of interest.

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