Dysphagia and aspiration pneumonia in elderly hospitalization stroke patients: Risk factors,cerebral infarction area comparison

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 previous 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 present in 45–65% of patients in the acute period following stroke and it can lead to reduction of dietary intake, malnutrition and result in aspiration 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 dysphagia with aging [3, 4].

Dysphagia is the most significant risk factor for the development of pneumonia. Patients with dysphagia have a three-fold increase in the risk of acquiring pneumonia (relative risk (RR) of 3.17), and aspiration further increases this risk (RR of 11.56) [5]. Additionally, impairment of pharyngeal sensory nerves, common after acute stroke, is associated with an increased risk of aspiration pneumonia [6].Pneumonia is the third-highest cause of death during the first month after stroke [7], Furthermore, it adversely affects patient outcomes by increasing the length of hospitalization and increasing the risk of mortality [8, 9, 10].

Recognition of vascular lesion patterns might help practitioners to distinguish stroke patients who have a special need for further diagnostics and protective measures of severe dysphagia. However, findings were inconsistent since several studies have tried to identify lesion patterns for the prediction of dysphagia [11, 12, 13]. Moreover, studies were often restricted to a small sample size and a low number of roughly classified brain regions of interest.

Although clinical bedside assessment of swallowing function is lower sensitive and specific in comparison to instrumental swallowing examination, it is still a frequently applied screening method [14, 15, 16]. To initiate early oral feeding, it is extremely important to evaluate swallowing function by bedside swallowing assessment (BSA). As recommended by the Japan Guidelines for the Management of Stroke 2009, modified 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 swallowing 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 patients that presented to the Department of Neurology, Xuanwu Hospital of Capital Medical University between July 2014 and June 2015. This study was approved by the Ethics Committee of Xuanwu Hospital 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) participants had an ischemic stroke confirmed by magnetic resonance imaging (MRI), within seven days after admission. 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 dysphagia after a previous stroke or history of other diseases potentially causing swallowing disorders (e.g. Parkinson’s disease, myasthenia gravis, multiple sclerosis, or mouth tumors).

Patients’ data were registered in detailed tables and divided under age, gender, date of admission, underlying diseases, National Institutes of Health Stroke Scale (NIHSS) score, body mass index (BMI), number of previous cerebral infarction, and days of hospitalization. Biochemistry data included triglyceride, cholesterol total, high density lipoprotein (HDL), low density lipoprotein (LDL), apolipoprotein A, and apolipoprotein 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 vascular territory categorization. The assessment of clinical physical examination included dysarthria, masticatory muscle paralysis, abnormal gag reflex, uvula deviation 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, researchers were blinded to patients’ infarction results of vascular territory categorization. A five-point scale was used for recording MWST score, All patients were examined 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 voluntarily. Finally, patients needed to repeat the voluntary 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 deglutition disorders (dysphagia).

2.4 Vascular territory categorization

For further comparisons among patients, all participants were categorized into two vascular territory subgroups. The test was performed by experienced radiologists, who were blinded to the results of swallowing function and clinical assessment. The location of the cerebral infarction was determined by reviewing the magnetic resonance angiogram (MRA) and imaging (MRI) taken at the onset of stroke. The vascular territory was determined by the method proposed by Rovira et al. [19]. Briefly, brain lesions were divided into two groups: territorial anterior circulation infarction (TAI), which designated anatomic infarction territory involving the deep or superficial artery of the middle cerebral artery, and the territorial posterior circulation infarction (TPI), which designated anatomic infarction territory involving the posterior inferior, anterior inferior and superior cerebellar arteries and posterior cerebral arteries.

2.5 Aspiration pneumonia diagnostic criteria

Aspiration pneumonia was diagnosed by inflammation in the lungs and one of these three conditions: (1) overt aspiration (apparent aspiration), (2) a condition in which aspiration is strongly suspected, and (3) the existence of dysphagia. Because a direct diagnosis of apparent aspiration is rare, it is considered to be diagnosed based on the existence of abnormal swallowing function or dysphagia, infiltrative shadows on chest radiography and elevated peripheral white blood cell count ( $\geqslant$ 10,000/ $\mu$ L) [21].

2.6 Statistical analysis

Statistical analysis was performed using SPSS 17.0 (SPSS Inc. Released 2008. SPSS Statistics for Windows, Version 17.0. Chicago: SPSS Inc.). Qualitative data were described by number and percent and was compared to Chi-square test. Normally distributed quantitative data were expressed as mean $\pm$ standard deviation (SD) and compared to Student’s t-test. Abnormally distributed data were expressed as median (min-max) and compared to Mann-Whitney U test. Multivariate logistic regression analysis was used to assess variables potentially related to the risk factors of dysphagia and aspiration pneumonia. Statistical significance was determined where $P<$ 0.05.

3. Results

A total of 212 patients were enrolled in the study and 16 patients were excluded due to their failure to cooperate with our physical examination and MWST. Through univariate analysis, number of previous cerebral infarction ( $p=$ 0.001), NIHSS score ( $p=$ 0.000), dysarthria ( $p=$ 0.000), masticatory muscle paralysis ( $p=$ 0.034), facial paralysis ( $p=$ 0.001), abolition of gag reflex ( $p=$ 0.000), uvula deviation (0.000), tongue deviation ( $p=$ 0.048) were correlated with deglutition difficulty (Tables 1 and 2).

Table 1
Univariate of dysphagia risk factor in patients with cerebral infarction

	Variables MWST ( $N=$ 196)
	Normal (152)	Abnormal (44)	P value
	M (SD)	M (SD)
Age	66.49(7.49)	68.23(6.94)	0.33
NOPCI	0.27(0.49)	0.95(1.17)	0.00*
NIHSS score	4.80(4.43)	11.36(6.14)	0.00*
BMI	25.31(3.76)	25.56(3.02)	0.69
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
LDL	2.26(0.80)	2.73(0.83)	0.20

MWST: modified water swallowing test, M (SD): mean (standard deviation), NOPCI: Number of previous cerebral infarction, NIHSS: National Institutes of Health Stroke Scale, BMI: body mass index, HDL: high density lipoprotein, LDL: low density lipoprotein, ${}^{*}P<$ 0.05.

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.

Through multivariable logistic regression analysis, number of previous cerebral infarction ( $p=$ 0.02), NIHSS score ( $p=$ 0.00), masticatory muscle paralysis ( $p=$ 0.01) and abolition of gag reflex ( $p=$ 0.00) were correlated with the deglutition difficulty (Table 3). NIHSS score ( $p=$ 0.017) and dysphagia ( $p=$ 0.02) were correlated with the aspiration pneumonia (Table 4).

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

Multiple logistic regression analysis of aspiration pneumonia risk factor

Variables	B value	P value	OR (95%CI)
NOPCI	0.17	0.34	1.18(0.84,1.65)
NIHSS score	0.14	0.017*	1.15(1.03,1.30)
Masticatory muscle paralysis	0.62	0.45	0.54(0.11,2.64)
Abolition of gag reflex	0.39	0.64	1.48(0.29,7.46)
Dysphagia	2.27	0.02*	9.70(1.45,65.05)

NOPCI: number of previous cerebral infarction, ${}^{*}P<$ 0.05.

In the remaining 196 subjects, 114 patients were categorized in territorial anterior circulation infarction (TAI) group (63% males) and 82 patients were categorized in territorial posterior circulation infarction (TPI) group (69% males, $P=$ 0.220). The mean ages were 69 years ( $\pm$ 7.8) and 68.8 years ( $\pm$ 7.2) for the TAI and TPI groups ( $P=$ 0.639), respectively. Mean NIHSS score on admission was 7.4 ( $\pm$ 5.8, range 0–27) in TAI group and 4.7 ( $\pm$ 4.8, range 0–24) in TPI group ( $P=$ 0.003). Other demographic and baseline characteristics for the participants are presented in Table 5.

Table 5

Demographic variables for patients with TAI and TPI

	TAI	TPI	P value
Age in years (M $\pm$ SD)	69.4 $\pm$ 7.8	68.8 $\pm$ 7.2	0.639
Male/female	72/42	57/25	0.220
NIHSS score (M $\pm$ SD)	7.4 $\pm$ 5.8	4.7 $\pm$ 4.8	0.003*
BMI (M $\pm$ SD)	25.3 $\pm$ 3.7	25.5 $\pm$ 3.4	0.437
Triglyceride (M $\pm$ SD)	1.4 $\pm$ 0.7	1.5 $\pm$ 0.8	0.443
Cholesterol total (M $\pm$ SD)	4.3 $\pm$ 1.1	4.3 $\pm$ 0.8	0.117
HDL (M $\pm$ SD)	1.4 $\pm$ 0.4	1.3 $\pm$ 0.3	0.082
LDL (M $\pm$ SD)	2.6 $\pm$ 0.9	2.6 $\pm$ 0.7	0.427
Apolipoprotein A (M $\pm$ SD)	1.2 $\pm$ 0.4	1.3 $\pm$ 0.3	0.208
Apolipoprotein B (M $\pm$ SD)	0.7 $\pm$ 0.2	0.7 $\pm$ 0.2	0.726
Days of hospitalization	14.7 $\pm$ 12.7	9.0 $\pm$ 2.1	0.11
(M $\pm$ SD)

TAI: Territorial anterior circulation infarction, TPI: Territorial posterior circulation infarction, NIHSS: National Institutes of Health Stroke Scale, BMI: body mass index, HDL: High density lipoprotein, LDL: Low density lipoprotein, SD: standard deviation, ${}^{*}P<$ 0.05.

Through subgroup analysis we found that in group with 0–5 NIHSS score, the incidence of abolition of gag reflex was higher in TAI group with significant difference ( $p=$ 0.024). In group with an NIHSS score over 10, TPI group was found with higher incidence of abolition of gag reflex with significant difference ( $p=$ 0.028). Other dysphagia risk variables showed no significant differences among the groups (Table 6).

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.

4. Discussion

Although many patients recover from their dysphagia within a week after stroke, approximately 50% of dysphagic patients are still left with swallowing deficits [10]. Unfortunately, studies investigating dysphagia in elderly patients after stroke between TAI and TPI are scarce, and the classification of stroke is different across studies. The present study aimed to compare the distinction of swallowing difficulty in post-stroke patients between different cerebral infarction territories. Subsequently, cerebral infarction were classified according to vascular territory in our study. Although the incidence of dysphagia risk variable was different between these two groups, we have not investigated a statistically significant result in the incidence of dysphagia due to the limitation of sample size.

Deglutition requires a complex set of reflexes in the brain to coordinate bolus propulsion by muscular activity from the mouth to the pharynx. Since the brain’s swallowing center is localized to the right insular lobe and anterior cingulate [22], the areas implicated in the swallowing process include the caudolateral sensori-motor cortex, the premotor, orbitofrontal and temporopolar cortex, the insula and the amygdala [23]. In addition, intact cortical function is also necessary for awareness of food in the mouth, driving oral behaviors of chewing and bolus manipulation, as well as sensation of the pharynx, larynx and esophagus. Specifically, a frontal lobe infarction is important for tongue movement that is integral to swallowing 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 microaspiration [26].

In stroke patients with dysphagia, dysfunction of the oral phase occurs more commonly in patients with cerebral infarction from occlusion of the anterior circulation 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). Previously, it has been shown that abnormal gag reflex, abnormal volitional cough, cough after swallow, aphasia and buccofacial apraxia were significantly more frequent in dysphagic patients than non-dysphagic patients. Moreover, Somasundaram et al. reported aphasia and buccofacial apraxia have the highest sensitivity (97% and 78%, respectively) and negative predictive values (89% and 68%, respectively) for dysphagia [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 deglutition. In subgroup analysis, we also found the incidence of abolition of gag reflex was higher in TAI group (Table 6).

Figure 1.

Incidence of dysphagia according to different areas of infarction.

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 related to dysphagia of pharyngeal phase abnormalities compared to TAI [27]. Study reported that swallow response 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).

With regard to aspiration pneumonia, Okamura et al. [28] reported that regional cerebral blood flow in the bilateral anterior insular gyrus was significantly decreased in stroke patients with a history of aspiration of pneumonia, compared to those without such a history. Further investigation illustrated impaired levels of consciousness and dysphagia were important risk factors for stroke-associated pneumonia across different clinical studies [30]. Additionally, post-stroke dysphagia carried a seven-fold increased risk of aspiration pneumonia and is an independent predictor of mortality [31]. Through our study, we found that in elderly stroke patients NIHSS score was another risk factor for aspiration pneumonia in addition to deglutition disorders (Table 4).

As for the treatment of post-stroke dysphagic and aspiration pneumonia patients, it is essential to improve 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 radiological 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 patient discharge. In addition, dysphagia is more prevalent than presently recognized, especially in stroke patients and the elderly aged between 75 and 80. For these reasons, it is particularly important to apply a comprehensive approach for early and effective treatment for patients with a high risk of dysphagia [32].

5. Conclusion

In stroke inpatients over sixty years of age, it is necessary to distinguish the patients with multiple previous cerebral infarctions, high NIHSS score, masticatory muscle paralysis and abolition of gag reflex for early detection and rehabilitation of dysphagia.

Footnotes

Acknowledgments

The authors would like to thank the Department of Neurology, Xuanwu Hospital of Capital Medical University. Financial support was provided by the Ministry of Health, P.R. China (No. 201302008), the Beijing Chinese Medical Science and Technique Development Foundation Project (No. JJ2015-09) and the Beijing Clinical Translational Research of Decelluarized Artificial Blood Vessels from the Capital Health Research and Development of Special Fund (No. 2016-1-2012).

Conflict of interest

None to report.

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Dysphagia and aspiration pneumonia in elderly hospitalization stroke patients: Risk factors,cerebral infarction area comparison

Abstract

OBJECTIVE:

METHOD:

RESULT:

CONCLUSION:

Keywords

1. Introduction

2. Methods

2.1 Subjects

2.2 Clinical symptoms assessment

2.3 Assessment of swallowing function

2.4 Vascular territory categorization

2.5 Aspiration pneumonia diagnostic criteria

2.6 Statistical analysis

3. Results

Table 1 Univariate of dysphagia risk factor in patients with cerebral infarction

Footnotes

Acknowledgments

Conflict of interest

References

Table 1
Univariate of dysphagia risk factor in patients with cerebral infarction