Journal of Back and Musculoskeletal Rehabilitation 32 (2019) 85–91 85

DOI 10.3233/BMR-170801
IOS Press

Dysphagia and aspiration pneumonia in

elderly hospitalization stroke patients: Risk
factors, cerebral infarction area comparison
Zeqin Xua , Yongquan Gua , Jianxin Lia , Chunmei Wanga , Rong Wangb , Ying Huanga and Jian Zhanga,∗
a
Department of Vascular Surgery, Xuanwu Hospital and Institute of Vascular Surgery, Capital Medical University,
Beijing 100053, China
b
Department of Central Laboratory, Xuanwu Hospital, Capital Medical University, Beijing 100053, China

Abstract.
OBJECTIVE: Stroke is the most common neurological disease that is associated with deglutition disorders. The aim of this
study was to analyze dysphagia and aspiration pneumonia risk factors in post-stroke elderly inpatients.
METHOD: We consecutively enrolled 212 stroke patients over sixty years of age from July 2014 to June 2015. Seventeen
patients were eliminated. Stroke patients’ demographics, clinical symptoms and biochemistry data were collected. Modified
water swallowing test was used for the assessment of deglutition difficulty. These inpatients were classified into two groups:
territorial anterior circulation infarction (n = 114) and territorial posterior circulation infarction (n = 82). Finally, dysphagia
and aspiration pneumonia risk factor were analyzed between these two groups.
RESULT: Number of previous cerebral infarction, National Institutes of Health Stroke Scale (NIHSS) score, masticatory muscle
paralysis, abolition of gag reflex were correlated with the deglutition difficulty in these patients. In addition, NIHSS score (p =
0.017) and dysphagia (p = 0.02) were correlated with aspiration pneumonia.
CONCLUSION: In stroke inpatients over sixty years of age, it is necessary to distinguish the patients with multiple previ-
ous cerebral infarctions, high NIHSS score, masticatory muscle paralysis, and abolition of gag reflex for early detection and
rehabilitation of dysphagia.

Keywords: Stroke, dysphagia, deglutition disorders, aspiration pneumonia

1. Introduction Dysphagia is the most significant risk factor for

Dysphagia is present in 45–65% of patients in the
acute period following stroke and it can lead to reduc-
tion of dietary intake, malnutrition and result in aspi-
ration pneumonia in post-stroke individuals [1,2]. In
addition, it is reported that the underlying functional
changes in tongue and jaw muscles might result in dys-
phagia with aging [3,4].
∗ Corresponding author: Jian Zhang, Department of Vascular
Surgery, Xuanwu Hospital and Institute of Vascular Surgery, Capital
Medical University, Beijing 100053, China. Tel.: +86 10 83198498;
Fax: +86 10 83198868; E-mail: zhangjiandoctor@126. com.
the development of pneumonia. Patients with dyspha-
gia have a three-fold increase in the risk of acquir-
ing pneumonia (relative risk (RR) of 3.17), and aspira-
tion further increases this risk (RR of 11.56) [5]. Ad-
ditionally, impairment of pharyngeal sensory nerves,
common after acute stroke, is associated with an in-
creased risk of aspiration pneumonia [6].Pneumonia is
the third-highest cause of death during the first month
after stroke [7], Furthermore, it adversely affects pa-
tient outcomes by increasing the length of hospitaliza-
tion and increasing the risk of mortality [8–10].
Recognition of vascular lesion patterns might help
practitioners to distinguish stroke patients who have
a special need for further diagnostics and protective

ISSN 1053-8127/19/$35.00

c 2019 – IOS Press and the authors. All rights reserved
86 Z. Xu et al. / Dysphagia and aspiration pneumonia in elderly hospitalization stroke patients
measures of severe dysphagia. However, findings were
inconsistent since several studies have tried to identify
lesion patterns for the prediction of dysphagia [11–13].
Moreover, studies were often restricted to a small sam-
ple size and a low number of roughly classified brain
regions of interest.
Although clinical bedside assessment of swallow-
ing function is lower sensitive and specific in com-
parison to instrumental swallowing examination, it is
still a frequently applied screening method [14–16].
To initiate early oral feeding, it is extremely important
to evaluate swallowing function by bedside swallow-
ing assessment (BSA). As recommended by the Japan
Guidelines for the Management of Stroke 2009, mod-
ified water swallowing test (MWST) is a simple and
easy technique for bedside assessment of swallowing
function [17]. The aim of our study is to identify high
risk patients of dysphagia after cerebral infarction by
comparing the dysphagia incidence between patients
with territorial anterior circulation infarction (TAI) and
territorial posterior circulation infarction (TPI). Since
swallowing process requires the collaboration of swal-
lowing center, intact cortical and cerebral fiber bundle,
we favor the hypothesis that the incidence of dysphagia
is higher in TAI patients.
2. Methods
2.1. Subjects
The study gathered elderly ischemic post-stroke pa-
tients that presented to the Department of Neurology,
Xuanwu Hospital of Capital Medical University be-
tween July 2014 and June 2015. This study was ap-
proved by the Ethics Committee of Xuanwu Hospi-
tal of Capital Medical University. All subjects or their
legally authorized representatives provided informed
consent before enrollment. Inclusion criteria included:
(1) participants are over sixty years old, and (2) partic-
ipants had an ischemic stroke confirmed by magnetic
resonance imaging (MRI), within seven days after ad-
mission. Exclusion criteria included: (1) impaired level
of consciousness, poor cognitive status, or inability to
obey instructions, (2) poor control of neck and head,
(3) hemorrhagic stroke, (4) abnormal anatomy of the
oropharynx, (5) transitory ischemic attack, multiple
or bilateral cerebral infarct, and (6) residual dyspha-
gia after a previous stroke or history of other diseases
potentially causing swallowing disorders (e.g. Parkin-
son’s disease, myasthenia gravis, multiple sclerosis, or
mouth tumors).
Patients’ data were registered in detailed tables and
divided under age, gender, date of admission, underly-
ing diseases, National Institutes of Health Stroke Scale
(NIHSS) score, body mass index (BMI), number of
previous cerebral infarction, and days of hospitaliza-
tion. Biochemistry data included triglyceride, choles-
terol total, high density lipoprotein (HDL), low density
lipoprotein (LDL), apolipoprotein A, and apolipopro-
tein B.
2.2. Clinical symptoms assessment
Clinical symptoms assessment was performed by
an experienced speech and language pathologist with
six years of experience in stroke ward. Researchers
were blinded to patients’ infarction results of vascu-
lar territory categorization. The assessment of clini-
cal physical examination included dysarthria, mastica-
tory muscle paralysis, abnormal gag reflex, uvula devi-
ation and tongue deviation facial symmetry and muscle
strength [18].
2.3. Assessment of swallowing function
Assessment of swallowing function consisted of
modified water swallowing test (MWST). Also, re-
searchers were blinded to patients’ infarction results of
vascular territory categorization. A five-point scale was
used for recording MWST score, All patients were ex-
amined in a sitting position with an accurate amount
of 3 ml cold water pouring into the vestibule of the
mouth. Subsequently, they were asked to swallow vol-
untarily. Finally, patients needed to repeat the volun-
tary saliva swallowing two more times. The test was
repeated three times when the score was four or higher,
and the worst swallow was recorded. A score of three
or lower was considered abnormal [19]. Patients with
abnormal MWST results were diagnosed with degluti-
tion disorders (dysphagia).
2.4. Vascular territory categorization
For further comparisons among patients, all partici-
pants were categorized into two vascular territory sub-
groups. The test was performed by experienced radi-
ologists, who were blinded to the results of swallow-
ing function and clinical assessment. The location of
the cerebral infarction was determined by reviewing
the magnetic resonance angiogram (MRA) and imag-
ing (MRI) taken at the onset of stroke. The vascular
territory was determined by the method proposed by
 Z. Xu et al. / Dysphagia and aspiration pneumonia in elderly hospitalization stroke patients 87

Table 1
Rovira et al. [19]. Briefly, brain lesions were divided Univariate of dysphagia risk factor in patients with cerebral infarc-
into two groups: territorial anterior circulation infarc- tion
tion (TAI), which designated anatomic infarction terri- Variables MWST (N = 196)
tory involving the deep or superficial artery of the mid- Normal (152) Abnormal (44) P value
dle cerebral artery, and the territorial posterior circu- M (SD) M (SD)
lation infarction (TPI), which designated anatomic in- Age 66.49(7.49) 68.23(6.94) 0.33
NOPCI 0.27(0.49) 0.95(1.17) 0.00*
farction territory involving the posterior inferior, ante-
NIHSS score 4.80(4.43) 11.36(6.14) 0.00*
rior inferior and superior cerebellar arteries and poste- BMI 25.31(3.76) 25.56(3.02) 0.69
rior cerebral arteries. Triglyceride 1.52(0.85) 1.29(0.46) 0.09
Cholesterol total 4.26(1.02) 4.48(1.02) 0.23
HDL 1.36(0.33) 1.42(0.44) 0.32
2.5. Aspiration pneumonia diagnostic criteria LDL 2.26(0.80) 2.73(0.83) 0.20
MWST: modified water swallowing test, M (SD): mean (standard
Aspiration pneumonia was diagnosed by inflamma- deviation), NOPCI: Number of previous cerebral infarction, NIHSS:
tion in the lungs and one of these three conditions: National Institutes of Health Stroke Scale, BMI: body mass index,
HDL: high density lipoprotein, LDL: low density lipoprotein, ∗ P <
(1) overt aspiration (apparent aspiration), (2) a con- 0.05.
dition in which aspiration is strongly suspected, and
(3) the existence of dysphagia. Because a direct diag- deviation (p = 0.048) were correlated with deglutition
nosis of apparent aspiration is rare, it is considered to difficulty (Tables 1 and 2).
be diagnosed based on the existence of abnormal swal- Through multivariable logistic regression analysis,
lowing function or dysphagia, infiltrative shadows on number of previous cerebral infarction (p = 0.02),
chest radiography and elevated peripheral white blood NIHSS score (p = 0.00), masticatory muscle paral-
cell count (> 10,000/µL) [21]. ysis (p = 0.01) and abolition of gag reflex (p =
0.00) were correlated with the deglutition difficulty
2.6. Statistical analysis (Table 3). NIHSS score (p = 0.017) and dysphagia
(p = 0.02) were correlated with the aspiration pneu-
Statistical analysis was performed using SPSS 17.0 monia (Table 4).
In the remaining 196 subjects, 114 patients were
(SPSS Inc. Released 2008. SPSS Statistics for Win-
categorized in territorial anterior circulation infarction
dows, Version 17.0. Chicago: SPSS Inc.). Qualita-
(TAI) group (63% males) and 82 patients were catego-
tive data were described by number and percent and
rized in territorial posterior circulation infarction (TPI)
was compared to Chi-square test. Normally distributed
group (69% males, P = 0.220). The mean ages were
quantitative data were expressed as mean ± standard
69 years (± 7.8) and 68.8 years (± 7.2) for the TAI and
deviation (SD) and compared to Student’s t-test. Ab-
TPI groups (P = 0.639), respectively. Mean NIHSS
normally distributed data were expressed as median
score on admission was 7.4 (± 5.8, range 0–27) in TAI
(min-max) and compared to Mann-Whitney U test.
group and 4.7 (± 4.8, range 0–24) in TPI group (P =
Multivariate logistic regression analysis was used to
0.003). Other demographic and baseline characteristics
assess variables potentially related to the risk factors of
for the participants are presented in Table 5.
dysphagia and aspiration pneumonia. Statistical signif- Through subgroup analysis we found that in group
icance was determined where P < 0.05. with 0–5 NIHSS score, the incidence of abolition of
gag reflex was higher in TAI group with significant dif-
ference (p = 0.024). In group with an NIHSS score
3. Results over 10, TPI group was found with higher incidence of
abolition of gag reflex with significant difference (p =
A total of 212 patients were enrolled in the study 0.028). Other dysphagia risk variables showed no sig-
and 16 patients were excluded due to their failure to nificant differences among the groups (Table 6).
cooperate with our physical examination and MWST.
Through univariate analysis, number of previous cere-
bral infarction (p = 0.001), NIHSS score (p = 0.000), 4. Discussion
dysarthria (p = 0.000), masticatory muscle paralysis
(p = 0.034), facial paralysis (p = 0.001), abolition of Although many patients recover from their dyspha-
gag reflex (p = 0.000), uvula deviation (0.000), tongue gia within a week after stroke, approximately 50%
88 Z. Xu et al. / Dysphagia and aspiration pneumonia in elderly hospitalization stroke patients

Table 2
Univariate analysis of dysphagia risk factor in patients with cerebral infarction
Variables MWST (N = 196)
Normal (152) Abnormal (44) P value
SEX (male,%) 99 (66.4) 30 (68.2) 0.491
Hypertension (n, %) 106 (72.1) 28 (63.6) 0.186
CHD (n, %) 22 (14.5) 5 (11.4) 0.373
DM (n, %) 49 (32.2) 14 (31.8) 0.503
Dysarthria (n, %) 81 (53.3) 39 (88.6) 0.000*
Masticatory muscle paralysis (n, %) 66 (43.4) 27 (61.4) 0.034*
Facial paralysis (n, %) 72 (47.4) 33 (75) 0.001*
Abolition of gag reflex (n, %) 5 (3.3) 19 (44.2) 0.000*
Uvula deviation (n, %) 3 (2.0) 9 (20.5) 0.000*
Tongue deviation (n, %) 53 (34.9) 22 (51.2) 0.048*
Smoke (n, %) 59 (38.8) 20 (45.5) 0.30
Drink (n, %) 114 (94.7) 34 (77.3) 0.547
MWST: modified water swallowing test, n: number, CHD: coronary heart disease, DM: diabetes mellitus, ∗ P < 0.05.

Table 3
Multiple logistic regression analysis of dysphagia risk factor in patients with cerebral infarction
Variables B value P value OR (95% CI)
NOPCI 0.88 0.02* 2.41(1.14,5.14)
NIHSS score 0.20 0.00* 1.22(1.10,1.35)
Dysarthria 1.25 0.12 3.49(0.73,16.73)
Masticatory muscle paralysis 1.49 0.01* 4.44(1.46,13.51)
Facial paralysis 0.90 0.15 2.46(0.71,8.50)
Abolition of gag reflex 3.27 0.00* 26.31(5.73,120.81)
Uvula deviation 0.50 0.63 1.64(0.21,12.53)
Tongue deviation 0.63 0.30 0.53(0.16,1.74)
B: beta, OR: odds ratio, NOPCI: number of previous cerebral infarction, ∗ P < 0.05.

Table 4 Table 5
Multiple logistic regression analysis of aspiration pneumonia risk Demographic variables for patients with TAI and TPI
factor
TAI TPI P value
Variables B value P value OR (95%CI) Age in years (M ± SD) 69.4 ± 7.8 68.8 ± 7.2 0.639
NOPCI 0.17 0.34 1.18(0.84,1.65) Male/female 72/42 57/25 0.220
NIHSS score 0.14 0.017* 1.15(1.03,1.30) NIHSS score (M ± SD) 7.4 ± 5.8 4.7 ± 4.8 0.003*
Masticatory muscle paralysis 0.62 0.45 0.54(0.11,2.64) BMI (M ± SD) 25.3 ± 3.7 25.5 ± 3.4 0.437
Abolition of gag reflex 0.39 0.64 1.48(0.29,7.46) Triglyceride (M ± SD) 1.4 ± 0.7 1.5 ± 0.8 0.443
Dysphagia 2.27 0.02* 9.70(1.45,65.05) Cholesterol total (M ± SD) 4.3 ± 1.1 4.3 ± 0.8 0.117
NOPCI: number of previous cerebral infarction, ∗ P < 0.05. HDL (M ± SD) 1.4 ± 0.4 1.3 ± 0.3 0.082
LDL (M ± SD) 2.6 ± 0.9 2.6 ± 0.7 0.427
Apolipoprotein A (M ± SD) 1.2 ± 0.4 1.3 ± 0.3 0.208
of dysphagic patients are still left with swallowing Apolipoprotein B (M ± SD) 0.7 ± 0.2 0.7 ± 0.2 0.726
deficits [10]. Unfortunately, studies investigating dys- Days of hospitalization 14.7 ± 12.7 9.0 ± 2.1 0.11
phagia in elderly patients after stroke between TAI and (M ± SD)
TPI are scarce, and the classification of stroke is differ- TAI: Territorial anterior circulation infarction, TPI: Territorial pos-
terior circulation infarction, NIHSS: National Institutes of Health
ent across studies. The present study aimed to compare Stroke Scale, BMI: body mass index, HDL: High density lipopro-
the distinction of swallowing difficulty in post-stroke tein, LDL: Low density lipoprotein, SD: standard deviation, ∗ P <
patients between different cerebral infarction territo- 0.05.
ries. Subsequently, cerebral infarction were classified
according to vascular territory in our study. Although lar activity from the mouth to the pharynx. Since the
the incidence of dysphagia risk variable was different brain’s swallowing center is localized to the right in-
between these two groups, we have not investigated a sular lobe and anterior cingulate [22], the areas impli-
statistically significant result in the incidence of dys- cated in the swallowing process include the caudolat-
phagia due to the limitation of sample size. eral sensori-motor cortex, the premotor, orbitofrontal
Deglutition requires a complex set of reflexes in and temporopolar cortex, the insula and the amyg-
the brain to coordinate bolus propulsion by muscu- dala [23]. In addition, intact cortical function is also
 Z. Xu et al. / Dysphagia and aspiration pneumonia in elderly hospitalization stroke patients 89

Table 6
Dysphagia risk factor comparison in different NIHSS score (TAI vs. TPI )
NIHSS score Variables TAI TPI p
0–5 NOPCI (M, SD) 0.56(0.74) 0.22(0.34) 0.08
NIHSS score (M, SD) 2.59(1.43) 2.48(1.57) 0.70
Masticatory muscle paralysis (n, %) 24(44.4) 29(48.3) 0.41
Abolition of Gag reflex (n, %) 53(98.1) 52(86.7) 0.024*
Dysphagia (n, %) 2(3.7) 6(10.0) 0.17
6–10 NOPCI (M, SD) 0.71(0.85) 0.25(0.32) 0.42
NIHSS score (M, SD) 8.21(1.45) 8.08(1.83) 0.81
Masticatory muscle paralysis (n, %) 12(42.9) 6(50) 0.47
Abolition of Gag reflex (n, %) 24(85.7) 11(91.7) 0.52
Dysphagia (n, %) 12(42.9) 3(25.0) 0.24
>10 NOPCI (M, SD) 0.50(0.97) 0.38(0.74) 0.74
NIHSS score (M, SD) 16.25(5.23) 15.13(4.02) 0.51
Masticatory muscle paralysis (n, %) 3(37.5) 17(54.8) 0.32
Abolition of Gag reflex (n, %) 3(37.5) 25(80.6) 0.028*
Dysphagia (n, %) 5(62.5) 16(51.6) 0.44
TAI: Territorial anterior circulation infarction, TPI: Territorial posterior circulation infarction, NOPCI: Number of previous cerebral infarction,
NIHSS: National Institutes of Health Stroke Scale, ∗ P < 0.05.

necessary for awareness of food in the mouth, driv-

ing oral behaviors of chewing and bolus manipula-
tion, as well as sensation of the pharynx, larynx and
esophagus. Specifically, a frontal lobe infarction is im-
portant for tongue movement that is integral to swal-
lowing compared to the parietotemporal lobe [24] and
supratentorial lesions are more related to buccofacial
apraxia [25]. Furthermore, it also required respiratory
cessation during swallowing, as well as reflexive and
voluntary cough mechanisms following microaspira-
tion [26].
In stroke patients with dysphagia, dysfunction of
the oral phase occurs more commonly in patients with
cerebral infarction from occlusion of the anterior cir-
culation such as the middle cerebral artery [27]. We
found that the incidence of dysphagia was highest in
patients with temporal parietal lobe infarction in TAI
group and it is bulbus medulla infarction the highest
incidence of dysphagia in TPI group (Fig. 1). Previ-
ously, it has been shown that abnormal gag reflex, ab-
normal volitional cough, cough after swallow, aphasia
and buccofacial apraxia were significantly more fre-
quent in dysphagic patients than non-dysphagic pa-
tients. Moreover, Somasundaram et al. reported apha-
sia and buccofacial apraxia have the highest sensitiv-
ity (97% and 78%, respectively) and negative predic-
tive values (89% and 68%, respectively) for dyspha-
gia [18]. In our study, we found masticatory muscle
paralysis (p = 0.01) and abolition of gag reflex (p =
0.00) were indeed correlated with the function of deg-
lutition. In subgroup analysis, we also found the in-
cidence of abolition of gag reflex was higher in TAI
group (Table 6).
Fig. 1. Incidence of dysphagia according to different areas of infarc-
tion.
Owing to the presence of excessive residues in the
valleculae or pyriform sinuses, patients with TPI are
also thought to present a higher risk of aspiration of
both thick and thin liquids than TAI patients during
swallowing. Consequently, TPI is also thought to be re-
lated to dysphagia of pharyngeal phase abnormalities
compared to TAI [27]. Study reported that swallow re-
sponse is generated in the brain stem swallowing center
in the medulla oblongata. The interneuronal network
of this area (central pattern generator (CPG)) receives
both central inputs from the cortex and also peripheral
sensory inputs from the pharynx and larynx [28]. We
found that the incidence of dysphagia was highest in
patients with bulbus medulla infarction in TPI group.
Furthermore, in group with NIHSS score greater than
10, TPI group was higher in the incidence of abolition
of gag reflex with significant difference (p = 0.028,
Table 6).
90 Z. Xu et al. / Dysphagia and aspiration pneumonia in elderly hospitalization stroke patients
With regard to aspiration pneumonia, Okamura et
al. [28] reported that regional cerebral blood flow in
the bilateral anterior insular gyrus was significantly de-
creased in stroke patients with a history of aspiration
of pneumonia, compared to those without such a his-
tory. Further investigation illustrated impaired levels
of consciousness and dysphagia were important risk
factors for stroke-associated pneumonia across differ-
ent clinical studies [30]. Additionally, post-stroke dys-
phagia carried a seven-fold increased risk of aspiration
pneumonia and is an independent predictor of mortal-
ity [31]. Through our study, we found that in elderly
stroke patients NIHSS score was another risk factor for
aspiration pneumonia in addition to deglutition disor-
ders (Table 4).
As for the treatment of post-stroke dysphagic and
aspiration pneumonia patients, it is essential to im-
prove our knowledge of the swallowing processing.
Although MWST cannot match the sensitivity and
specificity of radiological examinations such as video-
fluoroscopy, it is undeniable that MWST assessment is
a simple and easy technique to distinguish risk factors
of aspiration. A bedside swallowing assessment alone
sometimes does not provide sufficient information in
clinical practice. This is one limitation of our study
since our department is not equipped with any radio-
logical tools.
Dysphagia not only results in impaired quality of
life, nutritional deficiency and poor hydration, it is also
an indicator of aspiration risk and result in delay in pa-
tient discharge. In addition, dysphagia is more preva-
lent than presently recognized, especially in stroke pa-
tients and the elderly aged between 75 and 80. For
these reasons, it is particularly important to apply a
comprehensive approach for early and effective treat-
ment for patients with a high risk of dysphagia [32].
5. Conclusion
In stroke inpatients over sixty years of age, it is nec-
essary to distinguish the patients with multiple previ-
ous cerebral infarctions, high NIHSS score, mastica-
tory muscle paralysis and abolition of gag reflex for
early detection and rehabilitation of dysphagia.
Acknowledgments
The authors would like to thank the Department of
Neurology, Xuanwu Hospital of Capital Medical Uni-
versity. Financial support was provided by the Min-
istry of Health, P.R. China (No. 201302008), the Bei-
jing Chinese Medical Science and Technique Develop-
ment Foundation Project (No. JJ2015-09) and the Bei-
jing Clinical Translational Research of Decelluarized
Artificial Blood Vessels from the Capital Health Re-
search and Development of Special Fund (No. 2016-1-
2012).
Conflict of interest
None to report.
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