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*Swallowing Disorders

(Stroke. 1996;27:1200-1204.)
© 1996 American Heart Association, Inc.


Articles

Complications and Outcome After Acute Stroke

Does Dysphagia Matter?

D.G. Smithard, MRCP; P.A. O'Neill, MD; C. Park, BSc; J. Morris, BSc; R. Wyatt, BSc; R. England, FRCR D.F. Martin, FRCR

the University Department of Geriatric Medicine (D.G.S., P.A.O'N.) and the Departments of Speech and Language Therapy (C.P., R.W.), Medical Statistics (J.M.), and Radiology (R.E., D.F.M.), South Manchester University Hospitals Trust (UK).

Correspondence to Dr P.A. O'Neill, University Department of Geriatric Medicine, South Manchester University Hospitals NHS Trust, Nell Lane, Manchester M20 8LR, UK.


*    Abstract
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*Abstract
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Background and PurposeThe published data on the relationship between dysphagia and both outcome and complications after acute stroke have been inconclusive. We examined the relationship between these, using bedside assessment and videofluoroscopic examination.

MethodsWe prospectively studied 121 consecutive patients admitted with acute stroke. A standardized bedside assessment was performed by a physician. We performed videofluoroscopy blinded to this assessment within 3 days of stroke onset and within a median time of 24 hours of the bedside evaluations. The presence of aspiration was recorded. Mortality, functional outcome, length of stay, place of discharge, occurrence of chest infection, nutritional status, and hydration were the main outcome measures.

ResultsPatients with an abnormal swallow (dysphagia) on bedside assessment had a higher risk of chest infection (P=.05) and a poor nutritional state (P<.001). The presence of dysphagia was associated with an increased risk of death (P=.001), disability (P=.02), length of hospital stay (P<.001), and institutional care (P<.05). When other factors were taken into account, dysphagia remained as an independent predictor of outcome only with regard to mortality. The use of videofluoroscopy in detecting aspiration did not add to the value of bedside assessment.

ConclusionsBedside assessment of swallowing is of use in identifying patients at risk of developing complications. The value of routine screening with videofluoroscopy to detect aspiration is questioned.


Key Words: aspiration • dysphagia • prognosis • stroke outcome • videofluoroscopy


*    Introduction
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up arrowAbstract
*Introduction
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Swallowing difficulties (dysphagia) after acute stroke are common, with a reported incidence as high as 47%.1 2 3 4 Most recover within 1 week,1 5 although dysphagia persists in a small number of subjects. A significant proportion of time is spent on the management of these patients by speech and language therapists, yet the importance of dysphagia is unclear in terms of complications and ultimate outcome from stroke.

Dysphagia after stroke could be associated with a number of problems. Aspiration of food or saliva may cause a chest infection; in one study 19% of dysphagic patients experienced bronchopneumonia compared with 8% of those without dysphagia, although this difference did not reach statistical significance.1 Patients may also be at risk of dehydration, as reported by both Gordon et al1 and Barer,5 although again these changes were not statistically significant. Nutritional status deteriorates after stroke,6 but this has not been studied in relation to the presence of swallowing difficulties.

Dysphagia may be an independent marker of poor outcome after stroke. Wade and Langton-Hewer7 reported increased mortality in those with clinically apparent swallowing difficulties, although the analysis did not include dysphagia as an independent predictor. Using multivariate analysis, Barer5 identified decreased functional outcome in dysphagic patients, but this accounted for only 4% of the variance. Axelsson et al6 reported an increase in the length of hospital stay associated with eating problems but considered this to be due to the associated severe functional deficits. Gordon et al1 found that more patients with dysphagia were still hospitalized at 2 weeks, but lengths of stay were not described in their report.

We conducted a prospective study to determine whether dysphagia is related to the development of complications after acute stroke and whether it is an independent predictor of final outcome.


*    Subjects and Methods
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*Subjects and Methods
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Over a 12-month period, all patients presenting within 24 hours of the onset of acute stroke to the University Hospital of South Manchester were assessed for recruitment into the study. Exclusion criteria were admission after 24 hours, failure to obtain consent, or the presence of serious intercurrent illness (eg, advanced malignancy). The study had the approval of the ethical committee. Patients entered into the study were assessed clinically by one of the authors (D.G.S.) within 24 hours of admission to confirm the diagnosis of stroke. All patients underwent unenhanced CT scan of the brain unless they were too ill.

We have obtained validation of our standardized bedside assessment of swallowing (see "Appendix") (D.G.S., P.A.O., C.P., J.M., R.W., R.E., D.F.M., unpublished data, 1994).8 Briefly, the patient's ability to swallow was assessed clinically on days 0 to 3 and on day 7 by one physician. When possible, the physician performed the bedside assessment within 24 hours of videofluoroscopy (VF). We performed all clinical evaluations blinded to the results of VF.

When feasible, VF was conducted within 3 days of the stroke. The standard protocol used was adapted from that of Logemann.8 VF was performed in both the anteroposterior and lateral projections, with the use of different consistencies and volumes of barium. It was not performed if the consciousness level of the patient was reduced (Glasgow Coma Scale score <10) or if the patient was considered to be medically unfit to undergo the assessment. The VF results were stored on U-matic (Sanyo) videotapes and reported at a later date by one of the authors (R.E.). Patients were placed into two categories: aspiration (barium below the true vocal cords) or no aspiration. We performed VF and reported the results blinded to the clinical assessment.

Intermediate outcomes were dehydration, nutrition, or occurrence of chest infection. The patients were examined on days 0 to 7 by the same person (D.G.S.) for the presence of chest infection (diagnosis based on the presence of two or more of the following variables: tachypnea [>22/min], tachycardia, inspiratory crackles, bronchial breathing, and use of antibiotics) from days 0 to 7. A chest radiograph was performed on admission and at day 7. The diagnosis of a chest infection made by the responsible admitting clinical team was also noted.

At each of the four assessment points, change in hydration was determined by measurement of hematocrit, plasma sodium, urea, and osmolality. Nutrition was assessed at the same time with the use of anthropometric and laboratory indices. Weight and body mass index were recorded, and skinfold thickness was measured (Harpenden calipers, Crymch Wales) at four sites: triceps (TSF, midway between the olecranon and acromion), suprailiac, subscapular, and periumbilical. Midarm circumference (MAC) was measured at the site of the TSF; from these the arm muscle circumference (AMC) was calculated (AMC=MAC-[TSFx0.314]). Total protein, albumin, and globulins were assayed. Absolute values were not compared with "normal" ranges, but changes with time were analyzed within groups.

Outcome measures were survival, functional outcome according to Barthel activities of daily living scores, length of stay, and residence at discharge and at 6 months.

Statistical Analysis
Associations between categorical outcome measures (such as chest infection) and the swallowing assessments were determined with the use of the {chi}2 test or Fisher's exact test. For continuous outcome measures, two-sample t tests and one-factor ANOVA were used. Length of stay had a log-normal distribution and required a loge transformation to produce an adequate approximation to a normal distribution. The Barthel Index score was non-normally distributed and was analyzed with the use of the Mann-Whitney and Kruskal-Wallis tests.

Multiple regression and multiple logistic regression analyses were performed to investigate the association between outcome and swallowing assessments after adjustment for other prognostic factors.

We assessed changes in nutritional indices, serum albumin, and serum globulin using paired t tests, comparing each assessment with results at day 0.


*    Results
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*Results
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General
One hundred forty-nine subjects with a median age of 79 years (range, 40 to 93 years) entered the study. Eighty-six (58%) were female. Twenty-eight patients had a significantly reduced level of consciousness during the first week, and we were unable to assess their ability to swallow. The results are based on the 121 patients in whom the swallowing assessment could be performed.

Swallowing Problems
Sixty (50%) of the 121 patients were considered to have an unsafe swallow. There were no significant differences between groups with unsafe and safe swallows in terms of age, sex, or smoking habits.

Ninety-four patients (77.7%) had VF within a median time of 2 days (interquartile range, 1 to 4 days). Twenty patients aspirated and 74 did not. All these patients had had a bedside assessment within a median of 24 hours (interquartile range, 24 to 72 hours) of VF.

Outcome Measures
Chest infections occurring in the first week were seen more frequently in those patients with an unsafe swallow (33% versus 16%, {chi}2 [1 df]=3.9, P<.05). Aspiration as demonstrated on VF was not associated with an increased incidence of chest infection (P>.05, Fisher's exact test) (Table 1Down).


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Table 1. Occurrence of Chest Infection, Mortality, Institutionalization Rate, and (Geometric) Mean Length of Stay

Twenty-two patients were withdrawn early (after 1 week) from the study (further stroke [14], hip surgery [3], carotid endarterectomy [2], dementia [2], and at the patient's request [1]). They have not been included in the analysis of outcome measures documented below. There was an equal number of patients with safe and unsafe swallows within each category.

Mortality was higher in those with dysphagia ({chi}2 [1 df]=12.2, P<.001). Aspiration on VF was not associated with an increase in mortality (P>.1, Fisher's exact test). These results are summarized in Table 1Up.

Dysphagia was associated with a lower median Barthel Index score at 6 months after stroke (15 versus 18, P=.02), but aspiration was not associated with a statistically significant lower Barthel Index score (13 versus 18, P>.1). Patients with dysphagia were more likely to be discharged to institutionalized care (45% versus 21%, P<.05) (Table 1Up).

In patients with dysphagia the (geometric) mean length of stay was prolonged to 44.8 days (95% confidence interval, 32 to 62 days) compared with 24.5 days (95% confidence interval, 18 to 33 days) for those with a normal swallow (P<.01) (Table 1Up). The presence of aspiration on VF was not associated with an increased length of stay (Table 1Up).

Changes in nutritional indices at each assessment point were compared with time (day) 0 with the use of paired t tests (Table 2Down). Nutritional indices deteriorated over the first month in patients with dysphagia: triceps skinfold thickness decreased from 14.9 to 14.7 mm (P>.1), arm muscle circumference from 295.3 to 288.2 mm (P<.02), and midarm circumference from 300.9 to 292.5 mm (P<.01). Significant decreases were also seen in those patients in whom aspiration had been demonstrated.


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Table 2. Changes in Mean Skinfold Thickness (Triceps, Midarm Circumference, and Arm Muscle Circumference) Related to Presence of Swallowing Difficulties

Serum albumin (Table 3Down) decreased over the first month in those with an unsafe swallow (P<.02) and with aspiration (P<.05). Serum globulin increased in parallel with the albumin results.


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Table 3. Changes in Mean Serum Albumin Concentrations Over 6 Months Related to Presence of Swallowing Difficulties

We were unable to demonstrate any changes in hydration, regardless of ability to swallow. Patients with swallowing difficulties were more likely to use parenteral fluids (P<.001), and these were continued for longer times (P<.0001). The results are presented in more detail in Table 4Down.


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Table 4. Use of Parenteral Fluids During First Week of Admission

Multivariate logistical regression analysis was performed to determine whether the association between dysphagia or aspiration with poor outcome (mortality, lower Barthel Index score, increased length of stay, and occurrence of chest infection) remained after other accepted indicators of poor prognosis had been taken into account (weakness, neglect, hemianopia, incontinence, apraxia, age, and sex). The presence of a reduced level of consciousness is a major prognostic marker for outcome after stroke, but such patients were excluded at entry. The presence of an unsafe swallow remained a significant predictor of mortality ({chi}2 [1 df]=6.4, P=.01) after adjustments were made for the above confounding variables. The presence of aspiration as demonstrated on VF was not an independent predictor of mortality or the presence of chest infection.


*    Discussion
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up arrowAbstract
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up arrowResults
*Discussion
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Previous studies have linked clinical difficulties with swallowing to poor outcome after stroke,5 7 9 but only one of these has included data from VF imaging. We examined the different and separate roles of clinical assessment and VF examination on outcome and complications after stroke. We have shown that dysphagia was significantly related to outcome.

The factors considered were mortality, occurrence of chest infection, disability, length of hospital stay, place of discharge, nutrition, and hydration. We have confirmed that mortality after acute stroke is increased if swallowing problems are present even in patients with no reduction in level of consciousness.7 Mortality in those with dysphagia was 37%, which was the same order of magnitude as that reported by Wade and Langton-Hewer7 (42%). We did not find any relationship between aspiration on VF and mortality, although the number of deaths within these groups was small.

Axelsson et al6 suggested that swallowing difficulties were associated with an increased length of stay, which we have confirmed in relation to clinical assessment but not for radiological examination. Similar to the findings of others,5 7 we found that the presence of dysphagia was associated with a worse functional outcome as assessed by the Barthel Index score. There was also an association between the presence of dysphagia and the likelihood of being discharged to institutionalized care; this agrees with the findings of Kalra et al,10 in which the presence of dysphagia at 2 weeks was predictive of admission to a nursing home.

The presence of dysphagia was independently linked to the likelihood of chest infection. Gordon et al1 previously noted that in patients with swallowing difficulties, there was a twofold but nonsignificant increase in the occurrence of chest infection. In this study the relationship was statistically significant and remained so whether or not aspiration was identified on VF, which is in agreement with the work by Kidd et al.9

All of the above indicate that dysphagia was associated with poor outcome after stroke. Once other factors known to be strongly related to poor outcome were taken into account (weakness, neglect, hemianopia, incontinence, apraxia, age, and sex11 12 13 ), the presence of dysphagia remained an independent predictor of mortality, but it was not an independent predictor of a low score on the Barthel Index or length of stay. The results suggest that dysphagia is a marker of stroke severity12 and also plays an important role in stroke morbidity.

The presence of aspiration on VF was not an independent predictor of any outcome marker. Because of the small number of patients shown to be aspirating on VF and the number of patients withdrawn from the study, a real effect on outcome may have been missed. Nevertheless, the data obtained suggest that the usefulness of VF in identifying aspiration during the acute phase of stroke may be limited. A controlled intervention trial examining the management of dysphagia and aspiration in relation to complications and outcome is needed.

Many investigators have noted that patients admitted to the hospital are malnourished,14 15 and this is true for stroke patients.6 Axelsson et al6 noted a gradual deterioration in nutritional status with time but considered this to be a function of the stroke severity and age of the patients rather than the ability to swallow. In this study significant worsening of nutritional indices occurred in the patients with dysphagia, suggesting that the problem lay more with the nutritional support that these patients received rather than specific changes due to the stroke, for example, an increase in metabolic rate with cerebral hemorrhage.16

The deterioration continued until 1 month after the stroke, when these markers began to improve. This improvement could have been artifactual, in that those with the worst indices had died, or as patients recovered and dysphagia resolved, the intake of food increased. We minimized this confounding variable by comparing each assessment point with that at day 0, which permitted the comparison of data from only those patients surviving at each assessment point (Table 2Up). Recently, Woo et al17 showed that despite supplementation of the diet after chest infection, it can take longer than 6 months to achieve the previous level of nutrition. Certainly the surviving patients with unsafe swallows had not returned to their baseline at 6 months, whereas the groups with safe swallows either had or had nearly done so. Whether early feeding of stroke patients with oral or enteral supplements will improve outcome and shorten hospital stay, as shown by Bastow et al14 in patients with fractured neck of femur, is open to debate. It has been shown that nutritional deficiency results in an impaired immune response to infection.18 Furthermore, a spiral of decline may result with worsening nutritional status, leading to increasing dysphagia.19

Two studies have reported a tendency for dehydration to occur,1 5 but our results do not support these findings. In our unit, there is a written policy of fluid but not nutritional support for patients at risk. Therefore, in the early stages patients with swallowing difficulties were hydrated with parenteral fluids, and we have previously shown that in some patients overhydration occurs because of arginine vasopressin release.20

In conclusion, our study confirmed that dysphagia, as detected at the bedside, was an independent predictor of mortality and occurrence of chest infection and served to identify patients at risk for inadequate nutrition. Detection of aspiration by VF did not appear to add greatly to this risk profile. A quick, reliable bedside assessment would be of benefit.8 We have found no evidence to justify the routine use of VF in screening for aspiration in acute stroke.


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Table 5. Bedside Swallowing Assessment


*    Acknowledgments
 
This study was supported by grants from Action Research, Horsham, Sussex, and North West Regional Health Authority (UK).

Received October 17, 1995; revision received March 6, 1996; accepted March 7, 1996.


*    References
up arrowTop
up arrowAbstract
up arrowIntroduction
up arrowSubjects and Methods
up arrowResults
up arrowDiscussion
*References
 
1. Gordon C, Langton-Hewer R, Wade DT. Dysphagia in acute stroke. Br Med J. 1987;295:411-414.

2. Horner J, Massey EW, Riski JE, Lathrop DL, Chase KN. Aspiration following a stroke: clinical correlates and outcome. Neurology. 1988;38:1359-1362.[Abstract/Free Full Text]

3. Horner J, Buoyer FG, Alberts MJ, Helms MJ. Dysphagia following brain-stem stroke. Arch Neurol. 1991;48:1170-1173.[Abstract/Free Full Text]

4. Robbins J, Levine RL, Master A, Rosenbek JC, Kempster GB. Swallowing after unilateral stroke of the cerebral cortex. Arch Phys Med Rehabil. 1993;74:1295-1300.[Medline] [Order article via Infotrieve]

5. Barer DH. The natural history and functional consequences of dysphagia after hemisphere stroke. J Neurol Neurosurg Psychiatry.. 1989;52:236-241.

6. Axelsson K, Asplund K, Norberg A, Eriksson S. Eating problems and nutritional status during hospital stay of patients with severe stroke. J Am Diet Assoc. 1989;89:1092-1096.[Medline] [Order article via Infotrieve]

7. Wade DT, Langton-Hewer R. Motor loss and swallowing difficulty after stroke: frequency, recovery, and prognosis. Acta Neurol Scand. 1987;76:50-54.[Medline] [Order article via Infotrieve]

8. Logemann JA. Evaluation and Treatment of Swallowing Disorders. San Diego, Calif: College-Hill Press Inc; 1983.

9. Kidd D, Lawson J, Nesbitt R, MacMahon J. The natural history and clinical consequences of aspiration following acute stroke. Q J Med. 1995;88:409-413.

10. Kalra L, Smith DH, Crome P. Stroke in patients aged over 75 years: outcome and predictors. Postgrad Med J. 1993;69:33-36.[Abstract/Free Full Text]

11. Barer DH, Mitchell JRA. Predicting the outcome of stroke: do multivariate models help? Q J Med.. 1989;70:27-39.[Abstract/Free Full Text]

12. Fullerton KJ, MacKenzie G, Stout RW. Prognostic indices in stroke. Q J Med. 1988;66:147-162.[Abstract/Free Full Text]

13. Allen CMC. Predicting recovery after acute stroke. Br J Hosp Med. 1984;34:428-434.

14. Bastow MD, Rawlings J, Allinson SP. Benefits of supplementary tube feeding after fractured neck of femur: a randomised controlled trial. Br Med J. 1983;287:1589-1592.

15. Ek A-C, Larsson J, von Schenck H, Thorslund S, Unosson M, Bjurulf P. The correlation between anergy, malnutrition, and clinical outcome in an elderly population. Clin Nutr.. 1990;9:185-189.

16. Touho H, Karasawa J, Shishido H, Morisako T, Yamada K, Shibamoto K. Hypermetabolism in the acute stage of hemorrhagic cerebrovascular disease. J Neurosurg. 1990:72:710-714.

17. Woo J, Ho SC, Mak YT, Law LK, Cheung A. Nutritional status of elderly patients during recovery from chest infection and the role of nutritional supplementation assessed by a prospective randomised single-blind trial. Age Ageing. 1994;23:40-48.[Abstract/Free Full Text]

18. Chandra RK. The relation between immunology, nutrition and disease in elderly people. Age Ageing. 1990;19:S-25-S-31.

19. Veldee MS, Peth LD. Can protein-calorie malnutrition cause dysphagia? Dysphagia. 1992;7:86-101.[Medline] [Order article via Infotrieve]

20. O'Neill PA, Davies I, Fullerton KJ, Bennett D. Fluid balance in elderly patients following acute stroke. Age Ageing. 1992;21:280-285.[Abstract/Free Full Text]




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*Swallowing Disorders