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The Journals of Gerontology Series A: Biological Sciences and Medical Sciences 60:120-124 (2005)
© 2005 The Gerontological Society of America

Prognostic Implications of Swallowing Ability in Elderly Patients After Initial Recovery From Stroke

Toshihiko Iwamoto1,, Sarah Fukuda1, Masayuki Kikawada1, Masaru Takasaki1 and Toshiharu Imamura2

1 Department of Geriatric Medicine, Tokyo Medical University Hospital, Japan.
2 Department of Internal Medicine, Musashinoryouen Hospital, Tokyo, Japan.

Address correspondence to Toshihiko Iwamoto, MD, Department of Geriatric Medicine, Tokyo Medical University Hospital, 6-7-1 Nishishinjuku, Shinjuku-ku, Tokyo, 160-0023, Japan. E-mail: i-wam{at}ma.kcom.ne.jp


   Abstract
Top
 Abstract
Methods
 Results
 Discussion
 References
 
Background. It remains unclear how swallowing assessment can help clinicians to predict the risk for pneumonia in elderly persons after ischemic stroke. A prospective case-control study was conducted to evaluate the prognostic utility of swallowing ability assessments.

Methods. Participants were 136 elderly persons who had an acute ischemic stroke 3–12 months previously. They were separated into four groups based on their history of repeated episodes of pneumonia in combination with swallowing ability: Group 1 had neither repeated pneumonia nor swallowing abnormality (n = 69); group 2 had repeated pneumonia but no swallowing abnormality (n = 0); group 3 had swallowing abnormality but no repeated pneumonia (n = 54); and group 4 had both swallowing abnormality and repeated pneumonia (n = 13). The follow-up period was as long as 2.2 years. Outcomes and causes of death were compared among the groups.

Results. During the study, the overall mortality rate was higher in group 3 (24 deaths, 44.4%) and group 4 (9 deaths, 69.2%) than in group 1 (3 deaths, 4.3%, both p <.05). The annual mortality rate from pneumonia was also significantly higher in group 3 (21.2%) and group 4 (38.2%) than in group 1 (0.8%, p <.0001). The odds ratio for patients who subsequently died of pneumonia was 46.8 between groups 1 and 3.

Conclusions. The high sensitivity (.96) and specificity (.68) of swallowing ability indicate that the method is useful for identifying those persons at greatest risk for pneumonia and death after ischemic stroke.

OUTCOMES for persons who survive acute ischemic stroke depend largely on whether subsequent vascular disease or pneumonia develops. We have previously studied outcomes among elderly persons after initial ischemic stroke and reported 5-year mortality rates of approximately 20% from aspiration pneumonia (1). In addition to adversely affecting outcomes in persons with ischemic stroke, pneumonia can also compromise activities of daily living and is associated with the development of dementia (2). Prevention of pneumonia should therefore be an important goal in medical care. Because the risk for aspiration pneumonia is linked to dysphagia (3,4), accurate evaluation of swallowing ability is a prerequisite for the care of persons after ischemic stroke. Many techniques have been developed to assess swallowing ability (5–16), but the method described by Smithard and colleagues (5) is straightforward and can be performed at the bedside. However, the proportion of patients with an identifiable risk for dysphagia remains unclear. In the current study, we used the Smithard method to evaluate dysphagia in patients after ischemic stroke, and we considered the relationship between dysphagia status and outcome.


   METHODS
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 Abstract
 Methods
Results
 Discussion
 References
 
We conducted this prospective study from June 1999 through September 1999 at an urban, long-term rehabilitation ward. We performed the study in accordance with the Declaration of Helsinki (17). All patients gave their informed consent to undergo the water drinking test. The study group consisted of 136 elderly patients aged 60 years or older, for whom 3–12 months had elapsed since their last ischemic stroke, as verified on brain computed tomography.

All patients had some degree of motor disturbance and had been admitted to the hospital for rehabilitation. We excluded patients who were already receiving parenteral nutrition or had a gastrostomy tube. However, we did include patients treated in this manner after the swallowing assessment in the study. We separated patients into four groups based on their history of repeated episodes of pneumonia in combination with swallowing ability, which was evaluated according to the method described by Smithard and colleagues (5): Group 1 had neither repeated episodes of pneumonia nor swallowing abnormality (n = 69); group 2 had repeated pneumonia but no swallowing abnormality (n = 0); group 3 had swallowing abnormality but no repeated pneumonia (n = 54); and group 4 had both swallowing abnormality and repeated pneumonia (n = 13). In this study, we defined repeated episodes of pneumonia as a history of more than two episodes of pneumonia between the time of initial cerebral infarction and enrollment. We defined swallowing abnormality as any abnormality of swallowing during study stages 1, 2, or both. We omitted group 2 from analyses because all patients with repeated episodes of pneumonia displayed swallowing abnormality, and thus not a single patient belonged in this group.

We evaluated swallowing ability in the afternoon, with the patient in a sitting position (if the patient's head or back were unstable, the patient sat in bed with the back inclined at 60° and the neck in anterior flexion). We enrolled patients with impaired consciousness only if they were drowsy but rousable. To evaluate swallowing ability, the patient was given 5 ml of water in a spoon three times (stage 1), followed by 60 ml of water in a cup (stage 2). In stage 2 of the test, the patient had to drink the water (60 ml) within 1 minute, although any number of sips was allowed. Swallowing was clearly abnormal in stage 1 of the test in 40 patients, and therefore testing did not proceed to stage 2 for them (Table 1). Among the remaining 96 patients who proceeded to stage 2, swallowing was abnormal in 27.


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  		Table 1. Results of Bedside Swallowing Assessment.

 
We registered eligible patients after evaluation and observed them for as long as 2.2 years. We reevaluated patients on return visits to the hospital or on the basis of medical records or telephone interviews. We observed 96 survivors until the end of the study. Among the other 40 patients, we terminated the study because of death in 36 patients and loss to follow-up after discharge in 4. Thirty-two of the 36 deaths occurred in the hospital. Time and cause of death in the 4 patients lost to follow-up were eventually determined from death certificates. All episodes of pneumonia that required admission for treatment and all patients who received parenteral nutrition or a gastrostomy tube were closely documented. In the follow-up period, we based the diagnosis of aspiration pneumonia principally on clinical findings of a rapid increase in purulent sputum that displayed mixed infection, including anaerobes on bacteriologic examination, and findings on chest radiography showing infiltration shadows in the lower lung fields (18,19).

We recorded the following clinical characteristics of the patients: interval after first stroke, history of pneumonia after first stroke, main neurologic signs and symptoms, risk factors, main findings on computed tomography scans, activities of daily living status, and severity of dementia.

We defined risk factors as hypertension, diabetes mellitus, hyperlipidemia, and atrial fibrillation. We considered hypertension and diabetes mellitus to be present in patients who were receiving some type of pharmacotherapy or dietetic therapy to manage these diseases. We defined hyperlipidemia as a total serum cholesterol concentration of 220 mg/dl or more at the time of registration. Patients already receiving lipid-lowering agents were also considered to have hyperlipidemia. The presence of atrial fibrillation was confirmed electrocardiographically.

We assessed activities of daily living status according to the Rankin disability scale (20) and classified them, based on the patients' ability to move and walk, as "independent" (Rankin scale, 0–3), "partially dependent" (Rankin scale 4, unable to walk without assistance), or "totally dependent" (Rankin scale 5, bedridden). The presence and severity of dementia were evaluated according to the Clinical Dementia Rating (CDR) score (21). The severity of dementia was classified as "none" (CDR = 0 or 0.5), "mild" (CDR = 1), "moderate" (CDR = 2), or "severe" (CDR = 3).

Statistical Methods
We evaluated differences between groups using analysis of variance, the Kruskal–Wallis test, and Fisher's exact probability test. We analyzed survival using the Kaplan–Meier method, the log-rank test, and StatView software version 5.0 (SAS Institute, Cary, NC). We considered probability values less than.05 to be significant.


   RESULTS
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 Abstract
 Methods
 Results
Discussion
 References
 
Evaluation of Dysphagia
Swallowing was abnormal in 40 patients at stage 1 of testing. The most common abnormalities were repeated movements, coughing on swallowing, and abnormal laryngeal function after swallowing (Table 1). Nearly all of the 27 patients with abnormal results in stage 2 testing had abnormal laryngeal function after swallowing.

Clinical Characteristics
The three groups displayed no differences in age and sex ratio (Table 2). The interval from first stroke until testing varied considerably, but there was no statistical difference in the interval among the groups. Frequencies of hypertension, diabetes, and atrial fibrillation did not differ among the groups. However, the frequency of hyperlipidemia was lower in groups 3 and 4 (p <.05). The proportions of patients who required assistance to perform activities of daily living or who had severe dementia were significantly greater in groups 3 and 4 (p <.05). Many patients in group 4 were lethargic or had poor head and trunk control or abnormal movement of the lips, palate, larynx, or tongue. Bilateral hemispheric infarcts were frequently seen in groups 3 and 4.


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  		Table 2. Clinical Characteristics of Each Group.

 
Outcomes
Survival and mortality rates.-- During follow-up, 3 deaths occurred in group 1, 24 in group 3, and 9 in group 4. Annual mortality rates were significantly higher in group 3 (29.7%) and group 4 (49.2%) than in group 1 (2.2%, Table 3).


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  		Table 3. Outcome in Each Group.

 
Annual mortality rate related to aspiration pneumonia.-- Aspiration pneumonia was considered the cause of death in 1 patient in group 1, in 22 patients in group 3, and in 7 patients in group 4. The patient who died of aspiration pneumonia in group 1 had Wallenberg's syndrome, and dysphagia developed after relapse. Annual mortality rates from aspiration pneumonia were significantly higher in group 3 (27.2%) and group 4 (38.2%) than in group 1 (0.8%) (log-rank test: c2 = 38.8, Df = 2, p <.0001; Figure 1).



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  		Figure 1. Kaplan–Meier survival curves for each group based on deaths due to pneumonia

 
Episodes of pneumonia during follow-up.-- During the follow-up period, aspiration pneumonia developed at least once in 4 patients in group 1, in 36 patients in group 3, and in 10 patients in group 4. Aspiration pneumonia led to death in 30 of these patients.

Gastrostomy.-- During the follow-up period, 24 patients in group 3 and all 13 patients in group 4 received a gastrostomy tubes. Sixteen of these patients died as a result of pneumonia.

Utility of swallowing assessment for screening.-- Among the 123 patients in groups 1 and 3, 23 died of aspiration pneumonia, and 22 of these patients displayed positive results on swallowing assessment (sensitivity, 0.96; Table 4). Of the 100 patients who did not die of pneumonia, 68 had negative results on swallowing assessment (specificity, 0.68). Thirteen of the 23 patients who died of aspiration pneumonia had a history of repeated pneumonia after first stroke (sensitivity, 0.57). Of the 100 patients who did not die of pneumonia, 80 had no history of repeated pneumonia (specificity, 0.80; Table 5).


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  		Table 4. Sensitivity and Specificity of Swallowing Assessment Test for Identifying Patients at Risk for Subsequent Fatal Pneumonia.

 

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  		Table 5. Sensitivity and Specificity of Past History of Pneumonia for Identifying Patients at Risk for Subsequent Fatal Pneumonia.

 

   DISCUSSION
Top
 Abstract
 Methods
 Results
 Discussion
References
 
Stroke is the most common disease underlying aspiration pneumonia (18). The mortality rate from aspiration pneumonia is particularly high during the acute phase of stroke (5–9,22). In elderly patients in the chronic phase of ischemic stroke, the risk for death from aspiration pneumonia remains high (10,23). Because dysphagia influences outcomes in elderly persons after stroke, straightforward techniques that can accurately evaluate swallowing ability are needed. Various techniques have been developed (5–16), although most screening tests for dysphagia evaluate the ability to swallow water. However, some tests fail to identify mild dysphagia or subclinical aspiration (24,25). To overcome the problems of conventional methods, Smithard and colleagues (5) developed a bedside test to assess swallowing ability. This test consists of two stages, can be performed easily at the bedside, and evaluates swallowing ability at multiple time points. We wanted to determine whether this method was useful for diagnosing dysphagia and predicting outcomes in patients with ischemic stroke.

An important feature of this method is inclusion of a pretest evaluation of laryngeal function, palate movement, gag reflex, and voluntary cough, in addition to level of consciousness and control of the head and trunk. Speech, the ability to repeatedly swallow saliva, and voluntary cough also can be assessed as baseline values for bedside swallowing assessments. When our patients performed water-swallowing tests after such evaluations, we observed high incidences of repeated movements, stridor on swallowing, and abnormal laryngeal function after swallowing. Repeated movements refer to laryngeal movement two or more times on attempts to swallow 5 ml of water. Such repeated movements suggest problems in the oral or laryngeal phases of swallowing (5,6). Stridor on swallowing and abnormal laryngeal function after swallowing suggest decreased laryngeal perception or swallowing reflex, or the presence of aspiration (11,26).

Because repeated episodes of pneumonia were probably caused by aspiration, we excluded data from group 4 when we evaluated the utility of the Smithard method for risk screening. We followed groups 1 and 3 for as long as 2.2 years (average follow-up, 1.7 years), and the accuracy for predicting the risk for death from pneumonia based on the Smithard method was 0.65 (sensitivity, 0.96; specificity, 0.68). In contrast, accuracy for predicting risk for death from pneumonia based on the presence or absence of a history of pneumonia was 0.46 (sensitivity, 0.57; specificity, 0.80). These results suggest that this method is useful for identifying patients with a history of ischemic stroke who are at increased risk for aspiration pneumonia (odds ratio, 46.8).

In addition, the mortality rate from aspiration pneumonia increased at a similar pace in groups 3 and 4. We found no difference in the mortality rate from aspiration pneumonia in groups 3 and 4. Perhaps this lack of difference was related to the fact that many patients in group 3 and all patients in group 4 received gastrostomy tubes after evaluation for dysphagia. Despite this procedure, however, outcomes based on annual mortality rates in groups 3 and 4 were poorer than in group 1. One of the reasons for the poor outcomes would be gastroesophageal reflux phenomenon and oral hygiene, so meticulous attention must be focused on food processing and oral hygiene care (27).

These findings indicate that the Smithard method is helpful for predicting the risk for aspiration pneumonia in patients with ischemic stroke. The study by Smithard and colleagues (5) of outcomes in patients with acute stroke who had dysphagia on bedside swallowing assessment and were followed for 6 months showed high rates of pneumonia, poor nutritional status, and mortality (5). Furthermore, the diagnostic accuracy of the bedside swallowing assessment to detect dysphagia seemed similar to that of videofluoroscopy, the most accurate diagnostic procedure available, based on a comparison of diagnostic accuracy between the two methods (5). In the current study, we show the utility of the bedside swallowing assessment as a screening procedure for dysphagia. In addition to the validity, the convenience of bedside assessment, the use of water volumes, and evaluation variables similar to those of other water-swallowing tests (7,8) further enhance the value of this technique as a screening evaluation for dysphagia. Patients who display even one abnormal finding according to the Smithard method should be followed carefully for aspiration pneumonia. After ischemic stroke, patients should be evaluated carefully and retested at regular intervals, because the results of the bedside swallowing assessment may become positive during follow-up.

Study Limitations
We evaluated swallowing ability 3–12 months after the last acute ischemic stroke, regardless of recurrence or the interval after the first stroke. The interval from the first stroke to the time of testing, therefore, varied considerably. This variation in interval between the first stroke and testing was probably related to the incidence of pneumonia or cerebrovascular diseases, perhaps indicating selection bias. Groups 3 and 4 showed a high incidence of bilateral hemispheric infarction, suggesting that these groups may have had frequent recurrence of ischemic stroke during an extended period, or that stroke may have occurred after the development of unrecognized lesions. This was corroborated by the high incidences of impaired activities of daily living and disturbed consciousness in groups 3 and 4. Background differences in the presence of disturbed consciousness and dementia between the groups could introduce bias in the study and influence prognosis. Furthermore, it is unclear whether episodes of aspiration pneumonia during follow-up were caused by aspiration during meals or during sleep (24,25). Finally, the diagnosis of pneumonia is often attributed to aspiration pneumonia, particularly in patients after stroke, because the diagnosis apparently depends on clinical findings (18,19).

Conclusion
Our results indicate that the bedside swallowing assessment in elderly patients after initial recovery from stroke is useful for identifying those at greatest risk for pneumonia and death.


   Acknowledgments
 
Supported by the Department of Geriatric Medicine, Tokyo Medical University Hospital, Tokyo, Japan.

We thank Professors Raoul Breugelmans and J. Patrick Barron of the International Medical Communications Center of Tokyo Medical University for reviewing their manuscript.


   Footnotes
 
Decision Editor: John E. Morley, MB, BCh

Received July 14, 2003

Accepted September 3, 2003


   References
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 Abstract
 Methods
 Results
 Discussion
 References
 

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