- Email: [email protected]
The 2-Minute Spontaneous Swallowing Screening Predicts Independence on Enteral Feeding in Patients with Acute Stroke
ARTICLE IN PRESS
The 2-Minute Spontaneous Swallowing Screening Predicts Independence on Enteral Feeding in Patients with Acute Stroke Masachika Niimi, MD, PhD,* Gentaro Hashimoto, MD,† Takatoshi Hara, MD, PhD,* Naoki Yamada, MD, PhD,* Hiroto Fujigasaki, MD, PhD,‡ Takafumi Ide, MD, PhD,$ and Masahiro Abo, MD, PhD* Background: It is recommended that enteral feeding should be offered to patients with dysphagia estimated to be unable to take adequate diet orally within 7 days of admission after acute stroke, but there is no clear criterion for initiation of enteral feeding. Recent studies have reported that the frequency of spontaneous swallowing is useful in screening for dysphagia in acute stroke. The present study was aimed to investigate whether measurement of frequency of spontaneous swallowing for 2 minutes could predict independence on enteral feeding 1 week after admission in patients with acute stroke. Methods: Patients with acute stroke were subjected. Within 72 hours of stroke onset, the number of swallows for 2 minutes was measured by auscultation. Subsequently, 1-hour frequency of spontaneous swallowing was measured using a laryngeal microphone. Functional Oral Intake Scale (FOIS) was evaluated 1 week after admission. Results: Twenty-six out of 40 patients were independent on enteral feeding 1 week after admission based on FOIS. The presence of spontaneous swallowing for 2 minutes had .89 sensitivity, .54 specificity to predict independence on enteral feeding 1 week after admission, whereas the 1-hour frequency of spontaneous swallowing had 1.00 sensitivity, .46 specificity. Logistic regression analysis demonstrated that the presence of spontaneous swallowing for 2 minutes was independent predictor for independence on enteral feeding 1 week after admission, independently of age, sex, and NIHSS. Conclusions: The 2-minute spontaneous swallowing screening predicts independence on enteral feeding 1 week after admission in patients with acute stroke. Key Words: Dysphagia—substance P—aspiration pneumonia—acute stroke— deglutition—stroke-associated pneumonia © 2019 Elsevier Inc. All rights reserved.
Introduction From the *Department of Rehabilitation Medicine, The Jikei University School of Medicine, Minato-Ku, Tokyo, Japan; †Department of Rehabilitation Medicine, Tokyo Metropolitan Bokutoh Hospital, Sumida-Ku, Tokyo, Japan; ‡Department of Internal Medicine, Tokyo Metropolitan Bokutoh Hospital, Tokyo, Sumida-Ku, Tokyo, Japan; and $Department of Neurosurgery, Tokyo Metropolitan Bokutoh Hospital, Tokyo, Sumida-Ku, Tokyo, Japan. Received September 20, 2019; revision received October 16, 2019; accepted October 28, 2019. Financial Disclosure: This study was funded partly by Tokyo Metropolitan Clinical Research (Grant No. H27040308). Address correspondence to Masachika Niimi, MD, PhD, Department of Rehabilitation Medicine, The Jikei University School of Medicine, 3-25-8, Nishi-Shimbashi, Minato-Ku, Tokyo 105-8461, Japan. E-mail: [email protected]. 1052-3057/$ - see front matter © 2019 Elsevier Inc. All rights reserved. https://doi.org/10.1016/j.jstrokecerebrovasdis.2019.104508
Dysphagia is a frequent consequence of acute stroke and a critical risk factor for stroke-associated pneumonia.1 It should be careful to start oral intake in patients with acute stroke so as to avoid stroke-associated pneumonia. Therefore, screening for dysphagia has been recommended as early management for patients with acute stroke.2 There are limited validated screening protocols for dysphagia in patients with acute stroke.3 The patients tend to be deprived of oral intake tentatively, when they have dysphagia according to screening protocols for dysphagia. However, it remains challenging to determine the correct time for oral intake. In the meanwhile, there is concern that the patients in the fasting state would become malnourished. Malnutrition is associated with poor outcome of patients with acute stroke.4 The American Heart Association and the American Stroke Association have recommended that early enteral
Journal of Stroke and Cerebrovascular Diseases, Vol. &&, No. && (&&), 2019: 104508
1
ARTICLE IN PRESS M. NIIMI ET AL.
2
feeding should be started in patients with dysphagia within 1 week of admission after acute stroke onset in order to avoid malnutrition.2 This requires an assumption that the patients would not be able to start oral intake at least 1 week. However, it is difficult to predict swallowing function 1 week after admission, because most of screening protocols for dysphagia are aimed at detection of dysphagia at the present moment. Recent studies have reported that the frequency of spontaneous swallowing is useful in screening for dysphagia in acute stroke.5 Frequency of spontaneous swallowing decreased in patients with dysphagia. Frequency of spontaneous swallowing can be increased by treatment such as drugs6 and vibratory stimulation on the neck over the larynx7, though patients with acute stroke are not subjected in these studies. These studies suggest that frequency of spontaneous swallowing would be a potential indicator for swallowing function in patients with acute stroke. However, the direct application of the methodology into practice is not convenient, because it takes several hours to measure frequency of spontaneous swallowing according to the reported method.5 In the present study, we aim to investigate whether measurement of frequency of spontaneous swallowing for 2 minutes could predict independence on enteral feeding 1 week after admission in patients with acute stroke.
Materials and Methods Subjects Consecutive inpatients admitted to the stroke care unit at Tokyo Metropolitan Bokutoh Hospital because of acute stroke onset during the period between October and December in 2015 were subjected. The patients aged 80 or more were excluded from the study, because frequency of spontaneous swallowing decreases in elderly people.8 The patients who received sedatives were excluded, because sedatives impair the swallowing reflex9 and would decrease frequency of spontaneous swallowing. The patients who received angiotensin-converting enzyme inhibitors were excluded, because these drugs increase frequency of spontaneous swallowing. 6 This study was conducted in addition to the previous study. Therefore, this study subjected the same patients as the subjects in the previous study.10 This study was approved by the ethics committee of Tokyo Metropolitan Bokutoh Hospital. A signed informed consent was obtained from every patient before study participation.
The 2-Minute Frequency of Spontaneous Swallowing Within 72 hours of acute stroke onset, the attending nurses measured the number of swallows for 2 minutes by listening to the sound of spontaneous swallowing with a stethoscope placed over the anterolateral side of the
subject’s neck. The optimal site of measurement was defined as the midpoint between the location over the center of the cricoid cartilage and the location immediately superior to the jugular notch according to the previous study.11
The One-Hour Frequency of Spontaneous Swallowing The sound of spontaneous swallowing was recorded for 1 hour using a laryngeal microphone according to the previous study.12 The laryngeal microphone (SH-12iK; Nanzu, Shizuoka, Japan) connected to a digital voice recorder was placed onto the location where the stethoscope was placed on the subject’s neck soon after measurement of 2-minute frequency of spontaneous swallowing. The recorded sound data was analyzed by use of acoustic signal analysis software (WavePad for Macintosh, NCH Software, Greenwood Village, CO). The number of swallows per hour was measured based on visual waveform of the sound and acoustic signal of the sound. Clinical information about the subjects was blinded to measurers.
Clinical Evaluation and Management The National Institutes of Health Stroke Scale (NIHSS) was evaluated on admission by the attending physicians.13 The speech therapist evaluated swallowing function in every subjected patient for consecutive days except holidays from the next day of admission. Oral intake in subjected patients was started based on the evaluation of swallowing function by the speech therapist. Food texture was modified depending on improvement in swallowing function, if necessary. Enteral feeding via nasogastric tub was offered to the patients with dysphagia in order to meet nutrient requirements, if necessary. Functional Oral Intake Scale (FOIS)14 was evaluated 1 week after admission by the speech therapist. The speech therapist was blinded to information on frequency of spontaneous swallowing. The FOIS is an ordinal scale that rates the functional oral intake of patients with dysphagia. The maximum level of FOIS rated as 7 indicates total oral intake with no restrictions, whereas the minimum level rated as 1 indicates no oral intake. If the patients are rated as 4 or more, they are independent on enteral feeding.
Statistical Analysis All statistical analyses were conducted using SPSS version 21.0 (IBM, Somers, NY). The Pearson correlation analysis was used for correlation between 2-minute frequency of spontaneous swallowing and 1-hour frequency of spontaneous swallowing. In logistic regression analysis for independence on enteral feeding 1 week after admission, explanatory variables were age, sex, NIHSS, and presence of spontaneous swallowing for 2 minutes. P value under .05 was regarded as statistically significant.
ARTICLE IN PRESS 2-MINUTE SPONTANEOUS SWALLOWING SCREENING
Table 1. Clinical characteristics of subjected patients Clinical characteristics Sex (N, %) Age (years § SD) Stroke type (N, %) Cerebral infarction Intracerebral hemorrhage Subarachnoid hemorrhage NIHSS on admission (Points, Mean § SD) 2-minute frequency of spontaneous swallowing 1-hour frequency of spontaneous swallowing FOIS 1 week after admission (Median, IQR) Independence on enteral feeding 1 week after admission (N, %)
3
Table 2. Prediction for independence on enteral feeding 1 week after admission by presence of spontaneous swallowing for 2 minutes
Male: 26 (65.0), Female: 14 (35.0) 63.2 § 12.4 23 (57.5) 13 (32.5) 4 (10.0) 6.7 § 6.7 1.7 § 1.9 22.2 § 17.3 6.0 [2.0-7.0] 26 (67.5)
Abbreviations: FOIS, Functional Oral Intake Scale; IQR, interquartile range; NIHSS, National Institutes of Health Stroke Scale; SD, standard deviation.
Enteral feeding after 1 week Dependent Spontaneous swallowing for 2 minutes
Independent
Presence
6
24
Absence
7
3
value, and 1.00 negative predictive value to predict independence on enteral feeding 1 week after admission (Table 3). Logistic regression analysis demonstrated that the presence of spontaneous swallowing for 2 minutes was independent predictor for independence on enteral feeding 1 week after admission, independently of age, sex, and NIHSS on admission (Table 4).
Discussion Results Forty stroke patients were subjected. Clinical characteristics are shown at Table 1. Twenty-six patients were independent on enteral feeding 1 week after admission based on FOIS. There was a significant correlation between 2-minute frequency of spontaneous swallowing and 1-hour frequency of spontaneous swallowing (Fig 1). The presence of spontaneous swallowing for 2 minutes had .89 sensitivity, .54 specificity, .80 positive predictive value, and .70 negative predictive value to predict independence on enteral feeding 1 week after admission (Table 2). The 1-hour frequency of spontaneous swallowing had 1.00 sensitivity, .46 specificity, .79 positive predictive
The present study showed measurement of 2-minute frequency of spontaneous swallowing would predict independence on enteral feeding 1 week after admission in patients with acute stroke. It is known that malnutrition has negative impact on poor outcome of patients with acute stroke.4 The previous study showed that early enteral feeding within 1 week of admission led an absolute reduction in risk of death of 5.8% and a reduction in death or poor outcome of 1.2%.15 It suggests dysphagic stroke patients should receive enteral feeding via a nasogastric tube within the first few days of admission. However it is difficult in practice to determine when to insert a nasogastric tube in dysphagic patients with acute stroke, because dysphagia might improve after a few days and a nasogastric tube would inflict pain on the patients. In addition, prolonged
Figure 1. Correlation between 2-minute frequency of spontaneous swallowing and 1-hour frequency of spontaneous swallowing. The 2-minute frequency of spontaneous swallowing was significantly correlated with 1-hour frequency of spontaneous swallowing (r = .479, P = .002).
ARTICLE IN PRESS M. NIIMI ET AL.
4
Table 3. Prediction for independence on enteral feeding 1 week after admission by 1-hour frequency of spontaneous swallowing Enteral feeding after 1 week Dependent 1-hour frequency of spontaneous swallowing
Independent
310
7
27
<10
6
0
Table 4. Logistic regression analysis for independence on enteral feeding 1 week after admission Variables Age < 65 years Male NIHSS < 10 Presence of spontaneous swallowing for 2 minutes
P
OR
95%CI
.154 .291 .725 .031
1.86 1.22 -.49 2.66
.50 - 82.11 .35 - 32.37 .039 - 9.590 1.27 - 160.78
Abbreviations: CI, confidence interval; NIHSS, OR; odds ratio; National Institutes of Health Stroke Scale. Bold value significance at P < .05.
placement of the nasogastric tube gives a negative impact on swallowing function of poststroke patients.16 Screening for predicting swallowing function 1 week after admission is necessary. The present study demonstrated that measurement of 2-minute frequency of spontaneous swallowing had high sensitivity and negative predictive value to predict independence on enteral feeding 1 week after admission in patients with acute stroke. It suggests absence of spontaneous swallowing for 2 minutes on admission would lead to the recommendation that enteral feeding via a nasogastric tube should be started. According to the previous study, 1-hour frequency of spontaneous swallowing in healthy people was 24.4§8.7 counts.17 Another study reported that the mean frequency of spontaneous swallowing was 1.18 § .47 counts per 1 minute in healthy people.18 In the present study, the mean frequency of spontaneous swallowing were 22.2 § 17.3 per 1 hour and 1.7 § 1.9 for 2mintes. It suggests that frequency of spontaneous swallowing would decrease in patients with acute stroke. In the present study, 1-hour frequency of spontaneous swallowing had higher sensitivity and negative predictive value than 2-minute frequency of spontaneous swallowing to predict independence on enteral feeding 1 week after admission. It suggests longer measurement of frequency of spontaneous swallowing is better. However, longer measurement would take longer time to analyze and not be practical. The 2-minute measurement for frequency of spontaneous swallowing is appropriate for use in clinical practice because of convenience and sufficiently high sensitivity and negative predictive value.
Few studies have investigated predictors for oral or nonoral intake in patients with acute stroke. Nakajima et al19 demonstrated absence of gag reflex (OR = 7.95) and NIHSS score (OR = 1.13) were independent predictors for nonoral intake 4 weeks after admission, whereas consciousness disturbance (OR = 12.3), absence of gag reflex (OR = 5.34), and NIHSS score (OR = 1.20) were independent predictors for nonoral intake within 48 hours of admission. It suggests that ability for oral intake depends mainly on consciousness within only a few days of admission. Surprisingly, NIHSS had a little impact on prediction for nonoral intake. In the present study, logistic regression analysis also demonstrated that NIHSS on admission had little impact on prediction for independence on enteral feeding 1 week after admission. Furthermore, presence of spontaneous swallowing for 2 minutes could predict independence on enteral feeding 1 week after admission. The previous study reported that frequency of spontaneous swallowing decreases in acute stroke patients with low substance P levels in saliva.10 It suggests frequency of spontaneous swallowing would reflect degree of swallowing reflex, because substance P controls the swallowing reflex. Although swallowing reflex is difficult to evaluate directly, gag reflex can be evaluated by touching posterior pharyngeal wall with a tongue depressor blade. Gag reflex examination is easy to conduct and common procedure for patients with acute stroke. Based on the study of Nakajima et al, absence of gag reflex might be useful for prediction for independence on enteral feeding 1 week after admission. However, it has been reported that the sensitivity of the absence of the gag reflex for detecting dysphagia in patients with acute stroke is low.20 Presence of spontaneous swallowing for 2 minutes would be more useful than gag reflex to predict independence on enteral feeding 1 week after admission because that has high sensitivity. Repetitive saliva swallowing test (RSST) and modified water swallowing test (MWST) are often used as screening for dysphagia in poststroke patients.21 In RSST, patients are requested to swallow saliva as frequently as possible for 30 seconds. In MWST, patients are requested to swallow 3-ml cold water. However, all of patients with acute stroke cannot follow commands, because they often have consciousness disturbance or aphasia. Swallowing water itself might cause aspiration in patients with acute stroke. Measurement of frequency of spontaneous swallowing for 2 minutes does not need command-following and spontaneous saliva swallowing is safer than swallowing water. Therefore, it seems that measurement of frequency of spontaneous swallowing for 2 minutes is more useful to predict oral intake in patients with acute stroke than RSST and MWST. The present study had some limitations. First the population of the present study was small. Further studies including large population are necessary to confirm conclusion. Second, reliability was not investigated in this study.
ARTICLE IN PRESS 2-MINUTE SPONTANEOUS SWALLOWING SCREENING
Different persons had to measure frequency of spontaneous swallowing for 2 minutes separately to investigate interrater reliability. Third, validity was not sufficient in this study. To investigate criterion validity, confirmed swallowing examination such as videofluoroscopic swallowing study should be conducted in order to determine independence on enteral feeding 1 week after admission.22
Conclusion Measurement of frequency of spontaneous swallowing for 2 minutes is useful for prediction of independence on enteral feeding 1 week after admission in patients with acute stroke. This screening method would provide crucial information on whether physicians should start enteral feeding in patients with acute stroke.
Acknowledgment The authors gratefully acknowledge the support and the participation of the patients in this study.
Conflict of Interest The authors declare that there are no conflicts of interest.
References 1. Cohen DL, Roffe C, Beavan J, et al. Post-stroke dysphagia: a review and design considerations for future trials. Int J Stroke 2016;11:399-411. 2. Powers WJ, Rabinstein AA, Ackerson T, et al. 2018 Guidelines for the Early management of patients with acute ischemic stroke: a guideline for healthcare professionals from the American Heart Association/American Stroke Association. Stroke. 2018;49:e46-e110. 3. Kertscher B, Speyer R, Palmieri M, et al. Bedside screening to detect oropharyngeal dysphagia in patients with neurological disorders: an updated systematic review. Dysphagia 2014;29:204-212. 4. Yoo SH, Kim JS, Kwon SU, et al. Undernutrition as a predictor of poor clinical outcomes in acute ischemic stroke patients. Arch Neurol 2008;65:39-43. 5. Crary MA, Carnaby GD, Sia I, et al. Spontaneous swallowing frequency has potential to identify dysphagia in acute stroke. Stroke 2013;44:3452-3457. 6. He M, Ohrui T, Azumi M, et al. Depressed involuntary swallowing and risk of pneumonia. J Am Geriatr Soc 2004;52:1032-1033.
5 7. Mulheren RW, Ludlow CL. Vibration over the larynx increases swallowing and cortical activation for swallowing. J Neurophysiol 2017;118:1698-1708. 8. Tanaka N, Nohara K, Kotani Y, et al. Swallowing frequency in elderly people during daily life. J Oral Rehabil 2013;40:744-750. 9. Nishino T, Takizawa K, Yokokawa N, et al. Depression of the swallowing reflex during sedation and/or relative analgesia produced by inhalation of 50% nitrous oxide in oxygen. Anesthesiology 1987;67:995-998. 10. Niimi M, Hashimoto G, Hara T, et al. Relationship between frequency of spontaneous swallowing and salivary substance P level in patients with acute stroke. Dysphagia 2018;33:414-418. 11. Takahashi K, Groher ME, Michi K. Methodology for detecting swallowing sounds. Dysphagia 1994;9:54-62. 12. Tanaka N, Nohara K, Okuno K, et al. Development of a swallowing frequency meter using a laryngeal microphone. J Oral Rehabil 2012;39:411-420. 13. Lyden P, Brott T, Tilley B, et al. Improved reliability of the NIH Stroke Scale using video training. NINDS TPA Stroke Study Group. Stroke 1994;25:2220-2226. 14. Crary MA, Mann GD, Groher ME. Initial psychometric assessment of a functional oral intake scale for dysphagia in stroke patients. Arch Phys Med Rehabil 2005;86:1516-1520. 15. Dennis MS, Lewis SC, Warlow C, FOOD Trial Collaboration. Effect of timing and method of enteral tube feeding for dysphagic stroke patients (FOOD): a multicentre randomised controlled trial. Lancet 2005;365:764-772. 16. Wang ZY, Chen JM, Ni GX. Effect of an indwelling nasogastric tube on swallowing function in elderly post-stroke dysphagia patients with long-term nasal feeding. BMC Neurol 2019;19:83. 17. Lear CS, Flanagan Jr JB, Moorrees CF. The frequency of deglutition in man. Arch Oral Biol 1965;10:83-100. 18. Pehlivan M, Y€ uceyar N, Ertekin C, et al. An electronic device measuring the frequency of spontaneous swallowing: digital phagometer. Dysphagia 1996;11:259-264. 19. Nakajima M, Takada T, Terasaki Y, et al. Clinical significance of oral intake in patients with acute stroke. Dysphagia 2010;25:192-197. 20. Ramsey D, Smithard D, Donaldson N, et al. Is the gag reflex useful in the management of swallowing problems in acute stroke? Dysphagia 2005;20:105-107. 21. Watanabe S, Oh-Shige H, Oh-Iwa I, et al. Reconsideration of three screening tests for dysphagia in patients with cerebrovascular disease performed by non-expert examiners. Odontology 2019. https://doi.org/10.1007/ s10266-019-00431-9. [Epub ahead of print]. 22. Daniels SK, Ballo LA, Mahoney MC, et al. Clinical predictors of dysphagia and aspiration risk: outcome measures in acute stroke patients. Arch Phys Med Rehabil 2000;81:1030-1033.
The 2-Minute Spontaneous Swallowing Screening Predicts Independence on Enteral Feeding in Patients with Acute Stroke Masachika Niimi, MD, PhD,* Gentaro Hashimoto, MD,† Takatoshi Hara, MD, PhD,* Naoki Yamada, MD, PhD,* Hiroto Fujigasaki, MD, PhD,‡ Takafumi Ide, MD, PhD,$ and Masahiro Abo, MD, PhD* Background: It is recommended that enteral feeding should be offered to patients with dysphagia estimated to be unable to take adequate diet orally within 7 days of admission after acute stroke, but there is no clear criterion for initiation of enteral feeding. Recent studies have reported that the frequency of spontaneous swallowing is useful in screening for dysphagia in acute stroke. The present study was aimed to investigate whether measurement of frequency of spontaneous swallowing for 2 minutes could predict independence on enteral feeding 1 week after admission in patients with acute stroke. Methods: Patients with acute stroke were subjected. Within 72 hours of stroke onset, the number of swallows for 2 minutes was measured by auscultation. Subsequently, 1-hour frequency of spontaneous swallowing was measured using a laryngeal microphone. Functional Oral Intake Scale (FOIS) was evaluated 1 week after admission. Results: Twenty-six out of 40 patients were independent on enteral feeding 1 week after admission based on FOIS. The presence of spontaneous swallowing for 2 minutes had .89 sensitivity, .54 specificity to predict independence on enteral feeding 1 week after admission, whereas the 1-hour frequency of spontaneous swallowing had 1.00 sensitivity, .46 specificity. Logistic regression analysis demonstrated that the presence of spontaneous swallowing for 2 minutes was independent predictor for independence on enteral feeding 1 week after admission, independently of age, sex, and NIHSS. Conclusions: The 2-minute spontaneous swallowing screening predicts independence on enteral feeding 1 week after admission in patients with acute stroke. Key Words: Dysphagia—substance P—aspiration pneumonia—acute stroke— deglutition—stroke-associated pneumonia © 2019 Elsevier Inc. All rights reserved.
Introduction From the *Department of Rehabilitation Medicine, The Jikei University School of Medicine, Minato-Ku, Tokyo, Japan; †Department of Rehabilitation Medicine, Tokyo Metropolitan Bokutoh Hospital, Sumida-Ku, Tokyo, Japan; ‡Department of Internal Medicine, Tokyo Metropolitan Bokutoh Hospital, Tokyo, Sumida-Ku, Tokyo, Japan; and $Department of Neurosurgery, Tokyo Metropolitan Bokutoh Hospital, Tokyo, Sumida-Ku, Tokyo, Japan. Received September 20, 2019; revision received October 16, 2019; accepted October 28, 2019. Financial Disclosure: This study was funded partly by Tokyo Metropolitan Clinical Research (Grant No. H27040308). Address correspondence to Masachika Niimi, MD, PhD, Department of Rehabilitation Medicine, The Jikei University School of Medicine, 3-25-8, Nishi-Shimbashi, Minato-Ku, Tokyo 105-8461, Japan. E-mail: [email protected]. 1052-3057/$ - see front matter © 2019 Elsevier Inc. All rights reserved. https://doi.org/10.1016/j.jstrokecerebrovasdis.2019.104508
Dysphagia is a frequent consequence of acute stroke and a critical risk factor for stroke-associated pneumonia.1 It should be careful to start oral intake in patients with acute stroke so as to avoid stroke-associated pneumonia. Therefore, screening for dysphagia has been recommended as early management for patients with acute stroke.2 There are limited validated screening protocols for dysphagia in patients with acute stroke.3 The patients tend to be deprived of oral intake tentatively, when they have dysphagia according to screening protocols for dysphagia. However, it remains challenging to determine the correct time for oral intake. In the meanwhile, there is concern that the patients in the fasting state would become malnourished. Malnutrition is associated with poor outcome of patients with acute stroke.4 The American Heart Association and the American Stroke Association have recommended that early enteral
Journal of Stroke and Cerebrovascular Diseases, Vol. &&, No. && (&&), 2019: 104508
1
ARTICLE IN PRESS M. NIIMI ET AL.
2
feeding should be started in patients with dysphagia within 1 week of admission after acute stroke onset in order to avoid malnutrition.2 This requires an assumption that the patients would not be able to start oral intake at least 1 week. However, it is difficult to predict swallowing function 1 week after admission, because most of screening protocols for dysphagia are aimed at detection of dysphagia at the present moment. Recent studies have reported that the frequency of spontaneous swallowing is useful in screening for dysphagia in acute stroke.5 Frequency of spontaneous swallowing decreased in patients with dysphagia. Frequency of spontaneous swallowing can be increased by treatment such as drugs6 and vibratory stimulation on the neck over the larynx7, though patients with acute stroke are not subjected in these studies. These studies suggest that frequency of spontaneous swallowing would be a potential indicator for swallowing function in patients with acute stroke. However, the direct application of the methodology into practice is not convenient, because it takes several hours to measure frequency of spontaneous swallowing according to the reported method.5 In the present study, we aim to investigate whether measurement of frequency of spontaneous swallowing for 2 minutes could predict independence on enteral feeding 1 week after admission in patients with acute stroke.
Materials and Methods Subjects Consecutive inpatients admitted to the stroke care unit at Tokyo Metropolitan Bokutoh Hospital because of acute stroke onset during the period between October and December in 2015 were subjected. The patients aged 80 or more were excluded from the study, because frequency of spontaneous swallowing decreases in elderly people.8 The patients who received sedatives were excluded, because sedatives impair the swallowing reflex9 and would decrease frequency of spontaneous swallowing. The patients who received angiotensin-converting enzyme inhibitors were excluded, because these drugs increase frequency of spontaneous swallowing. 6 This study was conducted in addition to the previous study. Therefore, this study subjected the same patients as the subjects in the previous study.10 This study was approved by the ethics committee of Tokyo Metropolitan Bokutoh Hospital. A signed informed consent was obtained from every patient before study participation.
The 2-Minute Frequency of Spontaneous Swallowing Within 72 hours of acute stroke onset, the attending nurses measured the number of swallows for 2 minutes by listening to the sound of spontaneous swallowing with a stethoscope placed over the anterolateral side of the
subject’s neck. The optimal site of measurement was defined as the midpoint between the location over the center of the cricoid cartilage and the location immediately superior to the jugular notch according to the previous study.11
The One-Hour Frequency of Spontaneous Swallowing The sound of spontaneous swallowing was recorded for 1 hour using a laryngeal microphone according to the previous study.12 The laryngeal microphone (SH-12iK; Nanzu, Shizuoka, Japan) connected to a digital voice recorder was placed onto the location where the stethoscope was placed on the subject’s neck soon after measurement of 2-minute frequency of spontaneous swallowing. The recorded sound data was analyzed by use of acoustic signal analysis software (WavePad for Macintosh, NCH Software, Greenwood Village, CO). The number of swallows per hour was measured based on visual waveform of the sound and acoustic signal of the sound. Clinical information about the subjects was blinded to measurers.
Clinical Evaluation and Management The National Institutes of Health Stroke Scale (NIHSS) was evaluated on admission by the attending physicians.13 The speech therapist evaluated swallowing function in every subjected patient for consecutive days except holidays from the next day of admission. Oral intake in subjected patients was started based on the evaluation of swallowing function by the speech therapist. Food texture was modified depending on improvement in swallowing function, if necessary. Enteral feeding via nasogastric tub was offered to the patients with dysphagia in order to meet nutrient requirements, if necessary. Functional Oral Intake Scale (FOIS)14 was evaluated 1 week after admission by the speech therapist. The speech therapist was blinded to information on frequency of spontaneous swallowing. The FOIS is an ordinal scale that rates the functional oral intake of patients with dysphagia. The maximum level of FOIS rated as 7 indicates total oral intake with no restrictions, whereas the minimum level rated as 1 indicates no oral intake. If the patients are rated as 4 or more, they are independent on enteral feeding.
Statistical Analysis All statistical analyses were conducted using SPSS version 21.0 (IBM, Somers, NY). The Pearson correlation analysis was used for correlation between 2-minute frequency of spontaneous swallowing and 1-hour frequency of spontaneous swallowing. In logistic regression analysis for independence on enteral feeding 1 week after admission, explanatory variables were age, sex, NIHSS, and presence of spontaneous swallowing for 2 minutes. P value under .05 was regarded as statistically significant.
ARTICLE IN PRESS 2-MINUTE SPONTANEOUS SWALLOWING SCREENING
Table 1. Clinical characteristics of subjected patients Clinical characteristics Sex (N, %) Age (years § SD) Stroke type (N, %) Cerebral infarction Intracerebral hemorrhage Subarachnoid hemorrhage NIHSS on admission (Points, Mean § SD) 2-minute frequency of spontaneous swallowing 1-hour frequency of spontaneous swallowing FOIS 1 week after admission (Median, IQR) Independence on enteral feeding 1 week after admission (N, %)
3
Table 2. Prediction for independence on enteral feeding 1 week after admission by presence of spontaneous swallowing for 2 minutes
Male: 26 (65.0), Female: 14 (35.0) 63.2 § 12.4 23 (57.5) 13 (32.5) 4 (10.0) 6.7 § 6.7 1.7 § 1.9 22.2 § 17.3 6.0 [2.0-7.0] 26 (67.5)
Abbreviations: FOIS, Functional Oral Intake Scale; IQR, interquartile range; NIHSS, National Institutes of Health Stroke Scale; SD, standard deviation.
Enteral feeding after 1 week Dependent Spontaneous swallowing for 2 minutes
Independent
Presence
6
24
Absence
7
3
value, and 1.00 negative predictive value to predict independence on enteral feeding 1 week after admission (Table 3). Logistic regression analysis demonstrated that the presence of spontaneous swallowing for 2 minutes was independent predictor for independence on enteral feeding 1 week after admission, independently of age, sex, and NIHSS on admission (Table 4).
Discussion Results Forty stroke patients were subjected. Clinical characteristics are shown at Table 1. Twenty-six patients were independent on enteral feeding 1 week after admission based on FOIS. There was a significant correlation between 2-minute frequency of spontaneous swallowing and 1-hour frequency of spontaneous swallowing (Fig 1). The presence of spontaneous swallowing for 2 minutes had .89 sensitivity, .54 specificity, .80 positive predictive value, and .70 negative predictive value to predict independence on enteral feeding 1 week after admission (Table 2). The 1-hour frequency of spontaneous swallowing had 1.00 sensitivity, .46 specificity, .79 positive predictive
The present study showed measurement of 2-minute frequency of spontaneous swallowing would predict independence on enteral feeding 1 week after admission in patients with acute stroke. It is known that malnutrition has negative impact on poor outcome of patients with acute stroke.4 The previous study showed that early enteral feeding within 1 week of admission led an absolute reduction in risk of death of 5.8% and a reduction in death or poor outcome of 1.2%.15 It suggests dysphagic stroke patients should receive enteral feeding via a nasogastric tube within the first few days of admission. However it is difficult in practice to determine when to insert a nasogastric tube in dysphagic patients with acute stroke, because dysphagia might improve after a few days and a nasogastric tube would inflict pain on the patients. In addition, prolonged
Figure 1. Correlation between 2-minute frequency of spontaneous swallowing and 1-hour frequency of spontaneous swallowing. The 2-minute frequency of spontaneous swallowing was significantly correlated with 1-hour frequency of spontaneous swallowing (r = .479, P = .002).
ARTICLE IN PRESS M. NIIMI ET AL.
4
Table 3. Prediction for independence on enteral feeding 1 week after admission by 1-hour frequency of spontaneous swallowing Enteral feeding after 1 week Dependent 1-hour frequency of spontaneous swallowing
Independent
310
7
27
<10
6
0
Table 4. Logistic regression analysis for independence on enteral feeding 1 week after admission Variables Age < 65 years Male NIHSS < 10 Presence of spontaneous swallowing for 2 minutes
P
OR
95%CI
.154 .291 .725 .031
1.86 1.22 -.49 2.66
.50 - 82.11 .35 - 32.37 .039 - 9.590 1.27 - 160.78
Abbreviations: CI, confidence interval; NIHSS, OR; odds ratio; National Institutes of Health Stroke Scale. Bold value significance at P < .05.
placement of the nasogastric tube gives a negative impact on swallowing function of poststroke patients.16 Screening for predicting swallowing function 1 week after admission is necessary. The present study demonstrated that measurement of 2-minute frequency of spontaneous swallowing had high sensitivity and negative predictive value to predict independence on enteral feeding 1 week after admission in patients with acute stroke. It suggests absence of spontaneous swallowing for 2 minutes on admission would lead to the recommendation that enteral feeding via a nasogastric tube should be started. According to the previous study, 1-hour frequency of spontaneous swallowing in healthy people was 24.4§8.7 counts.17 Another study reported that the mean frequency of spontaneous swallowing was 1.18 § .47 counts per 1 minute in healthy people.18 In the present study, the mean frequency of spontaneous swallowing were 22.2 § 17.3 per 1 hour and 1.7 § 1.9 for 2mintes. It suggests that frequency of spontaneous swallowing would decrease in patients with acute stroke. In the present study, 1-hour frequency of spontaneous swallowing had higher sensitivity and negative predictive value than 2-minute frequency of spontaneous swallowing to predict independence on enteral feeding 1 week after admission. It suggests longer measurement of frequency of spontaneous swallowing is better. However, longer measurement would take longer time to analyze and not be practical. The 2-minute measurement for frequency of spontaneous swallowing is appropriate for use in clinical practice because of convenience and sufficiently high sensitivity and negative predictive value.
Few studies have investigated predictors for oral or nonoral intake in patients with acute stroke. Nakajima et al19 demonstrated absence of gag reflex (OR = 7.95) and NIHSS score (OR = 1.13) were independent predictors for nonoral intake 4 weeks after admission, whereas consciousness disturbance (OR = 12.3), absence of gag reflex (OR = 5.34), and NIHSS score (OR = 1.20) were independent predictors for nonoral intake within 48 hours of admission. It suggests that ability for oral intake depends mainly on consciousness within only a few days of admission. Surprisingly, NIHSS had a little impact on prediction for nonoral intake. In the present study, logistic regression analysis also demonstrated that NIHSS on admission had little impact on prediction for independence on enteral feeding 1 week after admission. Furthermore, presence of spontaneous swallowing for 2 minutes could predict independence on enteral feeding 1 week after admission. The previous study reported that frequency of spontaneous swallowing decreases in acute stroke patients with low substance P levels in saliva.10 It suggests frequency of spontaneous swallowing would reflect degree of swallowing reflex, because substance P controls the swallowing reflex. Although swallowing reflex is difficult to evaluate directly, gag reflex can be evaluated by touching posterior pharyngeal wall with a tongue depressor blade. Gag reflex examination is easy to conduct and common procedure for patients with acute stroke. Based on the study of Nakajima et al, absence of gag reflex might be useful for prediction for independence on enteral feeding 1 week after admission. However, it has been reported that the sensitivity of the absence of the gag reflex for detecting dysphagia in patients with acute stroke is low.20 Presence of spontaneous swallowing for 2 minutes would be more useful than gag reflex to predict independence on enteral feeding 1 week after admission because that has high sensitivity. Repetitive saliva swallowing test (RSST) and modified water swallowing test (MWST) are often used as screening for dysphagia in poststroke patients.21 In RSST, patients are requested to swallow saliva as frequently as possible for 30 seconds. In MWST, patients are requested to swallow 3-ml cold water. However, all of patients with acute stroke cannot follow commands, because they often have consciousness disturbance or aphasia. Swallowing water itself might cause aspiration in patients with acute stroke. Measurement of frequency of spontaneous swallowing for 2 minutes does not need command-following and spontaneous saliva swallowing is safer than swallowing water. Therefore, it seems that measurement of frequency of spontaneous swallowing for 2 minutes is more useful to predict oral intake in patients with acute stroke than RSST and MWST. The present study had some limitations. First the population of the present study was small. Further studies including large population are necessary to confirm conclusion. Second, reliability was not investigated in this study.
ARTICLE IN PRESS 2-MINUTE SPONTANEOUS SWALLOWING SCREENING
Different persons had to measure frequency of spontaneous swallowing for 2 minutes separately to investigate interrater reliability. Third, validity was not sufficient in this study. To investigate criterion validity, confirmed swallowing examination such as videofluoroscopic swallowing study should be conducted in order to determine independence on enteral feeding 1 week after admission.22
Conclusion Measurement of frequency of spontaneous swallowing for 2 minutes is useful for prediction of independence on enteral feeding 1 week after admission in patients with acute stroke. This screening method would provide crucial information on whether physicians should start enteral feeding in patients with acute stroke.
Acknowledgment The authors gratefully acknowledge the support and the participation of the patients in this study.
Conflict of Interest The authors declare that there are no conflicts of interest.
References 1. Cohen DL, Roffe C, Beavan J, et al. Post-stroke dysphagia: a review and design considerations for future trials. Int J Stroke 2016;11:399-411. 2. Powers WJ, Rabinstein AA, Ackerson T, et al. 2018 Guidelines for the Early management of patients with acute ischemic stroke: a guideline for healthcare professionals from the American Heart Association/American Stroke Association. Stroke. 2018;49:e46-e110. 3. Kertscher B, Speyer R, Palmieri M, et al. Bedside screening to detect oropharyngeal dysphagia in patients with neurological disorders: an updated systematic review. Dysphagia 2014;29:204-212. 4. Yoo SH, Kim JS, Kwon SU, et al. Undernutrition as a predictor of poor clinical outcomes in acute ischemic stroke patients. Arch Neurol 2008;65:39-43. 5. Crary MA, Carnaby GD, Sia I, et al. Spontaneous swallowing frequency has potential to identify dysphagia in acute stroke. Stroke 2013;44:3452-3457. 6. He M, Ohrui T, Azumi M, et al. Depressed involuntary swallowing and risk of pneumonia. J Am Geriatr Soc 2004;52:1032-1033.
5 7. Mulheren RW, Ludlow CL. Vibration over the larynx increases swallowing and cortical activation for swallowing. J Neurophysiol 2017;118:1698-1708. 8. Tanaka N, Nohara K, Kotani Y, et al. Swallowing frequency in elderly people during daily life. J Oral Rehabil 2013;40:744-750. 9. Nishino T, Takizawa K, Yokokawa N, et al. Depression of the swallowing reflex during sedation and/or relative analgesia produced by inhalation of 50% nitrous oxide in oxygen. Anesthesiology 1987;67:995-998. 10. Niimi M, Hashimoto G, Hara T, et al. Relationship between frequency of spontaneous swallowing and salivary substance P level in patients with acute stroke. Dysphagia 2018;33:414-418. 11. Takahashi K, Groher ME, Michi K. Methodology for detecting swallowing sounds. Dysphagia 1994;9:54-62. 12. Tanaka N, Nohara K, Okuno K, et al. Development of a swallowing frequency meter using a laryngeal microphone. J Oral Rehabil 2012;39:411-420. 13. Lyden P, Brott T, Tilley B, et al. Improved reliability of the NIH Stroke Scale using video training. NINDS TPA Stroke Study Group. Stroke 1994;25:2220-2226. 14. Crary MA, Mann GD, Groher ME. Initial psychometric assessment of a functional oral intake scale for dysphagia in stroke patients. Arch Phys Med Rehabil 2005;86:1516-1520. 15. Dennis MS, Lewis SC, Warlow C, FOOD Trial Collaboration. Effect of timing and method of enteral tube feeding for dysphagic stroke patients (FOOD): a multicentre randomised controlled trial. Lancet 2005;365:764-772. 16. Wang ZY, Chen JM, Ni GX. Effect of an indwelling nasogastric tube on swallowing function in elderly post-stroke dysphagia patients with long-term nasal feeding. BMC Neurol 2019;19:83. 17. Lear CS, Flanagan Jr JB, Moorrees CF. The frequency of deglutition in man. Arch Oral Biol 1965;10:83-100. 18. Pehlivan M, Y€ uceyar N, Ertekin C, et al. An electronic device measuring the frequency of spontaneous swallowing: digital phagometer. Dysphagia 1996;11:259-264. 19. Nakajima M, Takada T, Terasaki Y, et al. Clinical significance of oral intake in patients with acute stroke. Dysphagia 2010;25:192-197. 20. Ramsey D, Smithard D, Donaldson N, et al. Is the gag reflex useful in the management of swallowing problems in acute stroke? Dysphagia 2005;20:105-107. 21. Watanabe S, Oh-Shige H, Oh-Iwa I, et al. Reconsideration of three screening tests for dysphagia in patients with cerebrovascular disease performed by non-expert examiners. Odontology 2019. https://doi.org/10.1007/ s10266-019-00431-9. [Epub ahead of print]. 22. Daniels SK, Ballo LA, Mahoney MC, et al. Clinical predictors of dysphagia and aspiration risk: outcome measures in acute stroke patients. Arch Phys Med Rehabil 2000;81:1030-1033.