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. 2021 Jun 4;16(6):e0252837. doi: 10.1371/journal.pone.0252837

Relationship between tongue pressure and dysphagia diet in patients with acute stroke

Masahiro Nakamori 1,2,*, Kenichi Ishikawa 1,2, Eiji Imamura 2, Haruna Yamamoto 3, Keiko Kimura 3, Tomoko Ayukawa 4, Tatsuya Mizoue 5, Shinichi Wakabayashi 5
Editor: Wisit Cheungpasitporn6
PMCID: PMC8177488  PMID: 34086830

Abstract

A dysphagia diet is important for patients with stroke to help manage their nutritional state and prevent aspiration pneumonia. Tongue pressure measurement is a simple, non-invasive, and objective method for diagnosing dysphagia. We hypothesized that tongue pressure may be useful in making a choice of diet for patients with acute stroke. Using balloon-type equipment, tongue pressure was measured in 80 patients with acute stroke. On admission, a multidisciplinary swallowing team including doctors, nurses, speech therapists, and management dietitians evaluated and decided on the possibility of oral intake and diet form; the tongue pressure was unknown to the team. Diet form was defined and classified as dysphagia diet Codes 0 to 4 and normal form (Code 5 in this study) according to the 2013 Japanese Dysphagia Diet Criteria. In multivariate analysis, only tongue pressure was significantly associated with the dysphagia diet form (p<0.001). Receiver operating characteristic analyses revealed that the optimal cutoff tongue pressure for predicting diet Codes 1, 2, 3, 4, and 5 was 3.6 (p<0.001, area under the curve [AUC] = 0.997), 9.6 (p<0.001, AUC = 0.973), 12.8 (p<0.001, AUC = 0.963), 16.5 (p<0.001, AUC = 0.979), and 17.3 kPa (p<0.001, AUC = 0.982), respectively. Tongue pressure is one of the sensitive indicators for choosing dysphagia diet forms in patients with acute stroke. A combination of simple modalities will increase the accuracy of the swallowing assessment and choice of the diet form.

Introduction

For patients with stroke, dysphagia may lead to aspiration pneumonia and malnutrition. Prevention of aspiration pneumonia and nutrition management decreases the duration of hospitalization and mortality [1–3]. Thus, it is essential to serve a dysphagia diet to manage the patient’s nutritional state and prevent aspiration pneumonia. In particular, the multidisciplinary swallowing team approach decreases the onset of pneumonia in patients with acute stroke [4].

Videofluoroscopic and videoendoscopic examinations are the most accurate instrumental assessment tools for evaluating swallowing function. However, some patients cannot be evaluated fully due to their conditions or the unavailability of such tools. Thus, bedside screening tests, such as the repetitive saliva swallowing test and water swallowing test, are simple and non-invasive tests for assessing swallowing dysfunction [5, 6]. However, these tests are not accurate. Other auxiliary methods such as tongue ultrasonography and tongue pressure measurement are useful for evaluating dysphagia [7–9].

Concerning the prevention of pneumonia and management of nutrition, the possibility of oral intake and dysphagia diet should be chosen after assessing the swallowing function. However, there are few objective, simple, and non-invasive methods. It is very important to find an objective scale for choosing a suitable dysphagia diet form in clinical practice. In this study on acute stroke care, we hypothesized that tongue pressure would be a useful indicator for choosing the diet form for patients with acute stroke. We investigated the association between tongue pressure and dysphagia diet form and searched for the suitable tongue pressure for choosing each diet form.

Materials and methods

Ethics approval

This study had a prospective cohort design. This study was approved by the ethics committee of Suiseikai Kajikawa Hospital and was performed according to the national government’s guidelines based on the Helsinki Declaration of 1964. Written informed consent was obtained from all the patients or their relatives. All assessors were blinded to the data for analyses.

Subjects

All consecutive patients with acute ischemic or hemorrhagic stroke who were admitted to Suiseikai Kajikawa Hospital within 1 week of disease onset between June 1, 2015, and August 31, 2015 were included in this cohort study. Patients who were under 20 years old, did not provide consent (for patients who could not provide consent, consent was obtained from their relatives), were in coma (best eye response score on the Glasgow coma scale of 1), underwent craniotomy, were on mechanical ventilation, or diagnosed with aspiration pneumonia in the hospital were excluded. Aspiration pneumonia was diagnosed according to the criteria of the Centers for Disease Control and Prevention [10]. We monitored patients for signs of pneumonia for 30 days after admission. If the patients were discharged before the 30th day, then they were monitored until the day of discharge.

Data acquisition

The stroke subtype was determined according to the Trial of Org 10172 in Acute Stroke Treatment classification [11]. Stroke severity was evaluated using the National Institutes of Health Stroke Scale (NIHSS) score [12].

On admission, a multidisciplinary swallowing team including doctors, nurses, speech therapists, and management dietitians evaluated and decided on the possibility of oral intake and diet form; the tongue pressure was unknown to the team. Diet form was defined and classified as dysphagia diet Codes 0 to 4 and normal form according to the 2013 Japanese Dysphagia Diet Criteria [13]. In this code, dysphagia diet Code 0 refers to a soft, homogeneous diet, with a low adherability, high coherence, less water separation, and which can form a suitable bolus. Code 1 refers to a homogeneous diet, with less water separation, and which can form a suitable bolus. This does not require the ability to chew. It is often called jelly, pudding, or mousse food. Code 2 refers to a diet that readily forms a suitable bolus via simple oral movement. The tongue is required to press the hard palate during transportation. It is often called blender, puree, or paste food. Code 3 refers to a solid diet that can be crushed without teeth or prosthodontics and can easily form a bolus. Owing to the need for mouth movements, less water separation, and moderate coherence, this food is difficult to separate during its passage via the pharynx. It is often referred to as soft food. Code 4 refers to a diet that needs adjustment of the material and cooking method to prevent aspiration or suffocation. It is not too hard to form, come apart, and it has a high adhesion. It is soft enough to be cut with a spoon or chopsticks. It does not require teeth or prosthodontics but can be crushed with both alveolar ridges. It is difficult to crush food if only the tongue is pressed onto the hard palate. In this study, we defined a diet with a normal form as Code 5. Swallowing was evaluated using the Food Intake Level Scale (FILS) [14]. The FILS is a 10-point observer-rating scale that measures the severity of swallowing dysfunction. Its convergent validity and intra-rater and inter-rater reliabilities have been established using the Functional Oral Intake Scale.

On the same day, clinical technicians measured the tongue pressure using balloon-type equipment (TPM-01; JMS Co. Ltd., Hiroshima, Japan) independently. The balloon-type equipment consists of a disposable oral probe, an infusion tube as a connector, and a recording device. The patients were seated during the tongue pressure measurement and were asked to put the balloon in their mouths. They held the pipe at the midpoint of their central teeth. They were asked to maintain this position while the examiners adjusted the probe and confirmed the correct position. The patients were then asked to raise their tongue and push the balloon against their palate using maximum efforts for seven seconds, according to previous reports [15, 16]. This measurement was performed three times; the patients rested for 30 seconds and rinsed their mouth between each measurement. The maximum value of the three measurements for each patient was considered as the tongue pressure.

The reliability of intraindividual measurements has been reported previously [17]. We reconfirmed the reliability of the measurements in this study. Measurements were taken repeatedly for ten days in normal subjects, and the resulting coefficient of variation was 5.64%.

Statistical analysis

Data are expressed as median (minimum, 25th percentile, 75th percentile, maximum) for continuous variables (age, body mass index, NIHSS score, FILS, diet form, and tongue pressure) and as frequencies (percentages) for categorical variables (stroke subtypes and histories of comorbidities). Statistical analysis was performed using JMP 15 statistical software (SAS Institute Inc., Cary, NC, USA). We calculated the required sample size based on our previous study on tongue pressure in acute stroke [7]. In the previous study, tongue pressure was compared using the modified Mann Assessment of Swallowing Ability (MASA) score, which is an established bedside assessment tool that indicates the risk of developing swallowing dysfunction. A modified MASA score of <95 suggests swallowing dysfunction. The difference in the tongue pressure between the modified MASA score <95 and ≥95 groups was investigated, and the effect size was strong. This parameter was used to calculate the study sample size. Using an alpha level of 0.05 and a power of 0.80, 56 participants were required to participate in this study. To evaluate the association between tongue pressure and dysphagia diet form, the baseline data of the patients were analyzed, and two-step strategies were used to assess the significant importance of variables in the association between tongue pressure and FILS/dysphagia diet form using a least square linear regression analysis. First, a univariate analysis was performed, and factors with p <0.05 were selected. In a multi-factorial analysis, least linear regression analyses were performed with the selected factors. The analysis of co-variance was used to compare the mean tongue pressure between the dysphagia diet groups. Moreover, receiver operating characteristic (ROC) analyses were performed to determine the tongue pressure to predict suitable diet forms. Statistical significance was set at p <0.05.

Results

A total of 105 patients were eligible for this study. No patient was below 20 years old. Eleven patients or their relatives did not provide consent, two patients underwent craniotomy, and one patient was on mechanical ventilation. Among the remaining patients, eight patients were not evaluated because of a poor general condition, and three patients were diagnosed with aspiration pneumonia. Therefore, 80 patients were included in the study. A flowchart of the inclusion and exclusion criteria is shown in Fig 1. Data of the subjects’ backgrounds and characteristics are shown in Table 1. The mean tongue pressure was 21.5±14.1 kPa.

Fig 1. Flow chart of the inclusion and exclusion criteria.

Fig 1

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Table 1. Patient characteristics (n = 80).

Factors
Age, years 75 (53, 67, 84, 98)
Women 41 (51.3)
Body mass index, kg/m2 22.2 (13.3, 19.8, 25.5, 32.9)
Stroke Subtypes
 ATBI 18 (22.50)
 CEI 12 (15.00)
 LI 13 (16.25)
 Others 24 (30.00)
 ICH 13 (16.25)
Hypertension 61 (76.25)
Diabetes mellitus 22 (27.50)
Dyslipidemia 30 (37.50)
Atrial fibrillation 14 (17.50)
NIHSS score 4 (0, 2, 9.75, 36)
FILS 9 (1, 7, 10, 10)
diet form 5 (0, 3, 5, 5)
Tongue pressure, kPa 21.7 (0, 12.1, 31.9, 53.1)
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Data are expressed as median (minimum, 25th percentile, 75th percentile, maximum) for continuous variables (age, body mass index, NIHSS score, FILS, diet form, and tongue pressure), and frequencies (percentages) for categorical variables (stroke subtypes and histories of comorbidities).

BMI, body mass index; ATBI, atherothrombotic brain infarction; CEI, cardiogenic embolism infarction; LI, lacunar infarction; ICH, intracerebral hemorrhage; NIHSS, National Institutes of Health Stroke Scale; FILS, Food Intake Level Scale.

The associations between the factors listed in Table 1 (except for FILS and dysphagia diet form because they are response variables) and tongue pressure at admission were evaluated. In univariate analysis, age, sex, body mass index, diabetes mellitus, dyslipidemia, and NIHSS score were associated with tongue pressure. In multivariate analysis, age and NIHSS score were significant independent factors for tongue pressure (Table 2).

Table 2. Factors influencing tongue pressure.

Univariate analysis Multivariate analysis
Factors p value Regression coefficient 95% CI p value
Age <0.001 -0.429 -0.693–-0.164 0.002
Sex <0.001 1.740 0.905–4.384 0.194
Body mass index 0.003 0.097 -0.593–0.787 0.779
Stroke Subtypes 0.087
Hypertension 0.815
Diabetes mellitus 0.032 -0.786 -3,551–1.979 0.573
Dyslipidemia 0.005 0.162 -2.519–2.844 0.904
Atrial fibrillation 0.299
NIHSS score <0.001 -0.712 -1.043–-0.380 <0.001
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Regarding the categorical variables, the reference for sex was female, and the reference for hypertension, diabetes mellitus, dyslipidemia, and atrial fibrillation were normal controls.

CI, confidence interval; NIHSS, National Institutes of Health Stroke Scale.

Next, the associations between the factors listed in Table 1 and FILS/dysphagia diet form were evaluated. Regarding FILS in univariate analysis, age, sex, dyslipidemia, NIHSS score, and tongue pressure were associated with FILS. In multivariate analysis, NIHSS score and tongue pressure were significant independent factors for FILS (Table 3A). Regarding dysphagia diet form, in univariate analysis, age, sex, body mass index, NIHSS score, and tongue pressure were associated with dysphagia diet form. In multivariate analysis, only tongue pressure was significantly associated with the dysphagia diet form (Table 3B).

Table 3. Factors influencing the Food Intake Level Scale and dysphagia diet form.

Univariate analysis Multivariate analysis
Factors p value Regression coefficient 95% CI p value
A. Factors influencing the Food Intake Level Scale
Age <0.001 -0.001 -0.047–0.045 0.957
Sex 0.006 0.093 -0.342–0.528 0.672
Body mass index 0.114
Stroke Subtypes 0.138
Hypertension 0.947
Diabetes mellitus 0.220
Dyslipidemia 0.001 -0.094 -0.512–0.324 0.656
Atrial fibrillation 0.457
NIHSS score <0.001 -0.146 -0.207–-0.084 <0.001
Tongue pressure <0.001 0.110 0.072–0.149 <0.001
B. Factors influencing the dysphagia diet form
Age <0.001 -0.013 -0.090–0.064 0.724
Sex 0.034 0.305 -0.391–1.012 0.398
Body mass index 0.023 0.022 -0.142–0.178 0.788
Stroke Subtypes 0.324
Hypertension 0.128
Diabetes mellitus 0.731
Dyslipidemia 0.068
Atrial fibrillation 0.248
NIHSS score <0.001 -0.058 -0.148–0.026 0.203
Tongue pressure <0.001 0.448 0.307–0.622 <0.001
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Regarding the categorical variables, the reference for sex was female, and the reference for hypertension, diabetes mellitus, dyslipidemia, and atrial fibrillation were normal controls.

CI, confidence interval; NIHSS, National Institutes of Health Stroke Scale.

The mean tongue pressures of the dysphagia diet groups were compared (Fig 2). After adjusting for age and NIHSS score, which were associated with tongue pressure, the mean tongue pressure increased significantly as the dysphagia diet code increased.

Fig 2. Tongue pressure by dysphagia diet code.

Fig 2

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In the analysis of co-variance, the mean tongue pressures increased significantly as the dysphagia diet code increased.

Because we revealed the association between FILS/dysphagia diet form and tongue pressure (Table 3), ROC analyses were performed to determine the tongue pressure that can be used to predict a suitable dysphagia diet. FILS measures swallowing ability without considering the diet form. However, in a real clinical setting, it is important to know whether the patient can take food completely orally. A state of complete oral intake corresponds to FILS ≥7; therefore, we investigated the optimal cutoff tongue pressure for predicting a FILS of ≥7. The cut-off was 9.6 kPa (χ2 = 46.83, p<0.001, sensitivity 100.0%, specificity 92.8%, AUC = 0.991) (Fig 3A). Next, the optimal cut-off tongue pressure for predicting suitable dysphagia diet forms using the diet form code was investigated. The optimal cutoff tongue pressures to predict Codes 1, 2, 3, 4, and 5 were 3.6 kPa (χ2 = 53.12, p<0.001, sensitivity 100.0%, specificity 97.1%, AUC = 0.997), 9.6 kPa (χ2 = 50.87, p<0.001, sensitivity 92.9%, specificity 95.5%, AUC = 0.973), 12.8 kPa (χ2 = 55.85, p<0.001, sensitivity 89.5%, specificity 90.2%, AUC = 0.963), 16.5 kPa (χ2 = 74.90, p<0.001, sensitivity 96.4%, specificity 88.5%, AUC = 0.979), and 17.3 kPa (χ2 = 83.34, p<0.001, sensitivity 95.7%, specificity 99.9%, AUC = 0.982), respectively. The ROC curves are shown in Fig 3B–3F.

Fig 3. Receiver operating characteristic curve of tongue pressure for predicting dysphagia diet form.

Fig 3

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FILS ≥7 (A), Code ≥1 (2013 Japanese Dysphagia Diet Criteria) (B), Code ≥2 (C), Code ≥3 (D), Code ≥4 (E), and Code 5 (F).

Discussion

In this study, we measured the tongue pressure in patients with acute stroke and found that it was significantly associated with the FILS and dysphagia diet forms. The optimal cutoff tongue pressure for predicting a FILS ≥7 (the FILS for patients to receive food orally completely without intravenous nutrition) was 9.6 kPa. The mean tongue pressure increased significantly with an increase in the dysphagia diet code. The ROC analyses revealed that the optimal cutoff tongue pressure for predicting diet form Codes 1, 2, 3, 4, and 5 was 3.6, 9.6, 12.8, 16.5, and 17.3 kPa (p<0.001, AUC = 0.982), respectively. These results provide objective, practical, and useful indications for choosing a suitable dysphagia diet.

The tongue has a significant role in swallowing [18]. The tongue forms a bolus and sends the bolus to the pharynx, where the epiglottis moves downward and closes the larynx. Tongue pressure is a quantitative measurement of the tongue biomechanics during swallowing [16, 19, 20]. A lower tongue pressure prevents bolus control and increases oral residues; these increase the risk of aspiration. Additionally, a lower tongue pressure is related to inadequate closing, which can be a risk of aspiration during swallowing. Tongue pressure is associated with oropharyngeal residues visualized during videofluoroscopic examination [21]. It is reported that with a water swallowing test, tongue pressure is lower in patients with dysphagia than in those without [22]. Tongue pressure measurement is a non-invasive and straightforward tool with significant advantages. Moreover, the relationship between tongue pressure and videofluoroscopic examination, which is the gold standard method, has been established.

Among healthy Japanese subjects, the standard tongue pressure, measured using the same device, reduced with increasing age (41.7±9.7 kPa in subjects in their 20s and 31.9±8.9 kPa in subjects in their 70s) [19]. In addition, frail elderly Japanese subjects had a tongue pressure of 18.0±12.0 kPa [20, 23]. Moreover, the tongue pressures were lower than those of healthy subjects [19]. Our institution reported that a tongue pressure <21.6 kPa suggested swallowing dysfunction, in which the modified MASA score was less than 95 [7]. This study revealed that the indication for a normal-form diet was 17.3 kPa, which was consistent with previous reports.

There are several standards for dysphagia diet. The diet differs among regions and countries because of the different food cultures. Thus, the definition and form of dysphagia diet foods might differ among countries. The 2013 Japanese Dysphagia Diet Criteria were introduced for a consensus of dysphagia diet form for many hospitals and institutions [13]. In addition, Code 0 was divided into jelly and thickened. In this study, tongue pressure was strongly associated with diet forms, and ROC analyses revealed the optimal tongue pressure for choosing the diet form. In patients with acute stroke, tongue pressure is useful in choosing the dysphagia diet form. In addition, these results indicate that the dysphagia diet is strongly dependent on tongue function. However, to prevent aspiration pneumonia, there are some important factors, such as cough function. The cough reflex is an essential function for protecting and clearing materials that are aspirated into the airway. It has also been reported that the cough test is useful for screening silent aspiration [24]. The decision of fasting should be done by such an assessment, but not by tongue pressure.

In clinical practice, it is important for a multidisciplinary swallowing team to diagnose dysphagia as early as possible to start managing nutrition and preventing aspiration pneumonia. Although we reconfirmed the reliability of tongue pressure measurement, it does not require special skills. In this study, tongue pressure was measured on admission—this is recommendable.

This study had limitations. First, it was performed in a single institution and might have sources of bias. The sample size was small. More than half of the patients had mild stroke, which could prevent the generalizability of the results to a population with severe stroke. It would be difficult to measure the tongue pressure of patients with severe stroke accurately. Future multicenter research would be needed to eliminate the effects of bias. Second, tongue pressure cannot reflect all functions for swallowing. Videofluoroscopic and videoendoscopy examinations are the gold standards for evaluating dysphagia; however, they have limitations, such as exposure to radiation and difficulties to be performed in disabled patients [25]. In addition, it is impossible to perform these examinations in all patients with acute stroke. Thus, the swallowing assessment and decision for the diet form must be accurately performed using a combination of simple, non-invasive, and bedside modalities such as ultrasonography and cough test [9].

Conclusions

Tongue pressure is a sensitive and useful indicator for choosing the dysphagia diet form in patients with acute stroke. As a bedside assessment tool, tongue pressure measurement helps in nutrition management and evaluation of the swallowing function. The combination of simple modalities will increase the accuracy of the swallowing assessment and choice of the diet form.

Supporting information

S1 Data. All relevant data of the study.

(XLSX)

Click here for additional data file. (14.3KB, xlsx)

Acknowledgments

We would like to sincerely thank the staff in the Department of Nutrition at the Suiseikai Kajikawa Hospital for their technical assistance.

Data Availability

All relevant data are within the manuscript and its Supporting information files.

Funding Statement

The authors received no specific funding for this work.

References

  • 1.Hinds NP, Wiles CM. Assessment of swallowing and referral to speech and language therapists in acute stroke. Q J M. 1998;91: 829–835. [DOI] [PubMed] [Google Scholar]
  • 2.Nilsson H, Ekberg O, Olsson R, Hindfelt B. Dysphagia in stroke: a prospective study of quantitative aspects of swallowing in dysphagic patients. Dysphagia. 1998;13: 32–38. doi: 10.1007/PL00009547 [DOI] [PubMed] [Google Scholar]
  • 3.Smithard DG, O’Neill PA, Parks C, Morris J. Complications and outcome after acute stroke. Does dysphagia matter? Stroke. 1996;27: 1200–1204. doi: 10.1161/01.str.27.7.1200 [DOI] [PubMed] [Google Scholar]
  • 4.Aoki S, Hosomi N, Hirayama J, Nakamori M, Yoshikawa M, Nezu T, et al. The multidisciplinary swallowing team approach decreases pneumonia onset in acute stroke patients. PLOS ONE. 2016;11: e0154608. doi: 10.1371/journal.pone.0154608 [DOI] [PMC free article] [PubMed] [Google Scholar]
  • 5.Persson E, Wardh I, Ostberg P. Repetitive saliva swallowing test: Norms, clinical relevance and the impact of saliva secretion. Dysphagia. 2019;34: 271–278. doi: 10.1007/s00455-018-9937-0 [DOI] [PMC free article] [PubMed] [Google Scholar]
  • 6.Tohara H, Saitoh E, Mays KA, Kuhlemeier K, Palmer JB. Three tests for predicting aspiration without videofluorography. Dysphagia. 2003;18: 126–134. doi: 10.1007/s00455-002-0095-y [DOI] [PubMed] [Google Scholar]
  • 7.Nakamori M, Hosomi N, Ishikawa K, Imamura E, Shishido T, Ohshita T, et al. Prediction of pneumonia in acute stroke patients using tongue pressure measurements. Plos One. 2016;11: e0165837. doi: 10.1371/journal.pone.0165837 [DOI] [PMC free article] [PubMed] [Google Scholar]
  • 8.Hiraoka A, Yoshikawa M, Nakamori M, Hosomi N, Nagasaki T, Mori T, et al. Maximum tongue pressure is associated with swallowing dysfunction in ALS patients. Dysphagia. 2017;32: 542–547. doi: 10.1007/s00455-017-9797-z [DOI] [PubMed] [Google Scholar]
  • 9.Nakamori M, Hosomi N, Takaki S, Oda M, Hiraoka A, Yoshikawa M, et al. Tongue thickness evaluation using ultrasonography can predict swallowing function in amyotrophic lateral sclerosis patients. Clin Neurophysiol. 2016;127: 1669–1674. doi: 10.1016/j.clinph.2015.07.032 [DOI] [PubMed] [Google Scholar]
  • 10.Harms H, Hoffmann S, Malzahn U, Ohlraun S, Heuschmann P, Meisel A. Decision-making in the diagnosis and treatment of stroke-associated pneumonia. J Neurol Neurosurg Psychiatry. 2012;83: 1225–1230. [DOI] [PubMed] [Google Scholar]
  • 11.Adams HP, Bendixen BH, Kappelle LJ, Biller J, Love BB, Gordon DL, et al. Classification of subtype of acute ischemic stroke. Definitions for use in a multicenter clinical trial. TOAST. Trial of Org 10172 in Acute Stroke Treatment. Stroke. 1993;24: 35–41. doi: 10.1161/01.str.24.1.35 [DOI] [PubMed] [Google Scholar]
  • 12.Lyden P, Brott T, Tilley B, Welch KM, Mascha EJ, Levine S, et al. Improved reliability of the NIH Stroke Scale using video training. NINDS TPA Stroke Study Group. Stroke. 1994;25: 2220–2226. doi: 10.1161/01.str.25.11.2220 [DOI] [PubMed] [Google Scholar]
  • 13.The Dysphagia Diet Committee of the Japanese Society of Dysphagia Rehabilitation. The Japanese Dysphagia diet 2013. Jpn J Dysphagia Rehabil. 2013;17: 255–267. [Google Scholar]
  • 14.Kunieda K, Ohno T, Fujishima I, Hojo K, Morita T. Reliability and validity of a tool to measure the severity of dysphagia: the Food Intake LEVEL Scale. J Pain Symptom Manag. 2013;46: 201–206. doi: 10.1016/j.jpainsymman.2012.07.020 [DOI] [PubMed] [Google Scholar]
  • 15.Tsuga K, Maruyama M, Yoshikawa M, Yoshida M, Akagawa Y. Manometric evaluation of oral function with a hand-held balloon probe. J Oral Rehabil. 2011;38: 680–685. doi: 10.1111/j.1365-2842.2011.02202.x [DOI] [PubMed] [Google Scholar]
  • 16.Yoshikawa M, Yoshida M, Tsuga K, Akagawa Y, Groher ME. Comparison of three types of tongue pressure measurement devices. Dysphagia. 2011;26: 232–237. doi: 10.1007/s00455-010-9291-3 [DOI] [PubMed] [Google Scholar]
  • 17.Hayashi R, Tsuga K, Hosokawa R, Yoshida M, Sato Y, Akagawa Y. A novel handy probe for tongue pressure measurement. Int J Prosthodont. 2002;15: 385–388. [PubMed] [Google Scholar]
  • 18.Shaker R, Cook IJ, Dodds WJ, Hogan WJ. Pressure-flow dynamics of the oral phase of swallowing. Dysphagia. 1988;3: 79–84. doi: 10.1007/BF02412424 [DOI] [PubMed] [Google Scholar]
  • 19.Utanohara Y, Hayashi R, Yoshikawa M, Yoshida M, Tsuga K, Akagawa Y. Standard values of maximum tongue pressure taken using newly developed disposable tongue pressure measurement device. Dysphagia. 2008;23: 286–290. doi: 10.1007/s00455-007-9142-z [DOI] [PubMed] [Google Scholar]
  • 20.Tsuga K, Yoshikawa M, Oue H, Okazaki Y, Tsuchioka H, Maruyama M, et al. Maximal voluntary tongue pressure is decreased in Japanese frail elderly persons. Gerodontology. 2012;29: e1078–e1085. doi: 10.1111/j.1741-2358.2011.00615.x [DOI] [PubMed] [Google Scholar]
  • 21.Ono T, Kumakura I, Arimoto M, Hori K, Dong J, Iwata H, et al. Influence of bite force and tongue pressure on oro-pharyngeal residue in the elderly. Gerodontology. 2007;24: 143–150. doi: 10.1111/j.1741-2358.2007.00172.x [DOI] [PubMed] [Google Scholar]
  • 22.Hirota N, Konaka K, Ono T, Tamine K, Kondo J, Hori K, et al. Reduced tongue pressure against the hard palate on the paralyzed side during swallowing predicts dysphagia in patients with acute stroke. Stroke. 2010;41: 2982–2984. doi: 10.1161/STROKEAHA.110.594960 [DOI] [PubMed] [Google Scholar]
  • 23.Yoshida M, Kikutani T, Tsuga K, Utanohara Y, Hayashi R, Akagawa Y. Decreased tongue pressure reflects symptom of dysphagia. Dysphagia. 2006;21: 61–65. doi: 10.1007/s00455-005-9011-6 [DOI] [PubMed] [Google Scholar]
  • 24.Nakamori M, Imamura E, Kuwabara M, Ayukawa T, Tachiyama K, Kamimura T, et al. Simplified cough test can predict the risk for pneumonia in patients with acute stroke. Plos One. 2020;15: e0239590. doi: 10.1371/journal.pone.0239590 [DOI] [PMC free article] [PubMed] [Google Scholar]
  • 25.Yoshikawa M, Yoshida M, Nagasaki T, Tanimoto K, Tsuga K, Akagawa Y, et al. Aspects of swallowing in healthy dentate elderly persons older than 80 years. J Gerontol A Biol Sci Med Sci. 2005;60: 506–509. doi: 10.1093/gerona/60.4.506 [DOI] [PubMed] [Google Scholar]

Decision Letter 0

Wisit Cheungpasitporn

9 Apr 2021

PONE-D-21-05820

The relationship between tongue pressure and dysphasia diet in acute stroke patients

PLOS ONE

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**********

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Reviewer #3: Yes

**********

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**********

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**********

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Reviewer #1: Methods:

Should state the study design and duration of study.

Please add explanation on sample size determination; the parameters used in the calculation.

Please explain on sampling method in related to “consecutive acute stroke patients…”.

Should report median with interquartile range.

Revise the findings. Should state the outcome for each analysis. Tongue pressure influence the dysphagia diet or vice versa. Please explain.

The authors should control the confounder for comparison of mean tongue pressure for each group of dysphagia diet; ANCOVA instead of ANOVA.

Do all the assumptions of the test fulfilled? Please explain.

Please justify the use of ROC analysis.

Results:

Revise the findings.

Table 1: Delete All. Should write n=80 at the end of table title. Replace it with n(%). Delete n(%) written after factors. Should report median (IQR).

Table 2: Any reason run different model. What is predictor? Does it refer to regression coefficient? Please the results of categorical factors. Should state the reference.

Reviewer #2: This study by Nakamori et al evaluated if tongue pressure measurement is a sensitive indicator for determining diet form and swallowing capability among a sample of 80 patients hospitalized for acute stroke in a Japanese hospital. The authors found that tongue pressure measured on admission by a multidisciplinary team is significantly associated with diet form and swallowing. The manuscript is very well-written and describes an interesting research question with clear clinical implications. I have some comments about the presentation of the methods and results:

Methods:

1. Page 10 lines 144-146: Please describe the additional parameters used to calculate sample size (e.g., effect size based on prior literature)

2. Page 10 lines 148: More details about the multivariable model are important to state. Please explicitly state what the dependent variable is and how it was operationalized (continuous, categorical, etc). Along the same lines, what type of multivariable model was used (linear, logistic, etc)? What covariates did you consider in the model and how were they operationalized (Was NIHSS at admission and was it measured as a continuous variable? Same with BMI and comorbidities.)

Results:

3. Page 11 (Table 1): It would be more helpful to know the IQR when you present descriptive statistics (rather than minimum and maximum), especially for your key variables of interest (FILS, diet form). More information about distribution of the FILS, diet form, and tongue pressure, would be helpful to the reader since these are key variables in your study.

4. Page 13 (Table 2): Some comments on the presentation of data in Table 2. What is the reference group for categorical variables (sex, hypertension, diabetes, etc)? This should be clearly labeled in the table. Is the “predictor” column referring to beta coefficients?

5. Page 15 Figure 1: Please indicate that the bars are (95%?) confidence intervals

6. Page 15 lines 191-192: The mention of ROC analyses was a surprise as I was reading the article. ROC needs to be described in the methods section.

General comments:

7. I’m a little confused about the wording in the manuscript. Are you classifying FILS (swallowing capability) as another measure of diet form? For example, the caption for figure 2 only refers to diet form, even though panel A discusses FILS.

8. It may be useful to have information about training to conduct tongue pressure. Who performed it in the multidisciplinary team? Was there standardized training or is this part of routine clinical practice so this type of standardization is not needed? This would be useful if the reader wants to consider how they can translate these results to their own clinical practice.

Reviewer #3: Dear Dr. Masahiro Nakamori:

Thank you for allowing us to read your interesting manuscript. This study provides information about the tongue pressure, such as a non-invasive bedside assessment tool for deciding the diet form for acute stroke patients. It is a great effort, congratulations. Please consider the following comments.

In many parts of the manuscript appears the word “dysphasia” (9 times) including the tittle, which I think should be corrected to “dysphagia”.

It should be important that the abstract conclusion make it clear that tongue pressure is just one tool within other evaluations (such cough function) that must be made to patient to decide the type of diet, similar to the idea expressed in the extend conclusion.

More than 50% of the sample were minor strokes (NIHSS �5), which could be a limitation when extending the results to more serious strokes.

It should be important that you give a recommendation regarding the appropriate timing for the initiation of this post-stroke test (tongue pressure), depending on the moment in which you carried out these evaluations in the study.

Thanks,

**********

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Reviewer #2: No

Reviewer #3: Yes: Vanessa Cano-Nigenda

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PLoS One. 2021 Jun 4;16(6):e0252837. doi: 10.1371/journal.pone.0252837.r002

Author response to Decision Letter 0

30 Apr 2021

Thank you for reviewing our work. We appreciate all your comments and suggestions. We have revised the manuscript accordingly. Our point-by-point responses are presented below.

Response to the Editor

Comment 1: Please ensure that your manuscript meets PLOS ONE's style requirements, including those for file naming. The PLOS ONE style templates can be found at https://journals.plos.org/plosone/s/file?id=wjVg/PLOSOne_formatting_sample_main_body.pdf and https://journals.plos.org/plosone/s/file?id=ba62/PLOSOne_formatting_sample_title_authors_affiliations.pdf

Response 1: We have ensured that the manuscript meets the style requirements of PLOS ONE.

Comment 2: Thank you for submitting the above manuscript to PLOS ONE. During our internal evaluation of the manuscript, we found significant text overlap between your submission and the following previously published work, of which you are an author.

- https://journals.plos.org/plosone/article?id=10.1371%2Fjournal.pone.0239590

We would like to make you aware that copying extracts from previous publications, especially outside the methods section, word-for-word is unacceptable. In addition, the reproduction of text from published reports has implications for the copyright that may apply to the publications.

Please revise the manuscript to rephrase the duplicated text, cite your sources, and provide details as to how the current manuscript advances on previous work. Please note that further consideration is dependent on the submission of a manuscript that addresses these concerns about the overlap in text with published work.

We will carefully review your manuscript upon resubmission, so please ensure that your revision is thorough.

Response 2: As you pointed out, we have checked and revised the manuscript. We have also ensured that all text overlaps were avoided. Our revisions are highlighted in red font in the revised manuscript.

 

Response to the reviewers

Reviewer #1:

Comment 1: Should state the study design and duration of study.

Response 1: Thank you for this suggestion. This study had a prospective cohort design. We monitored patients for signs of pneumonia for 30 days after admission. If the patients were discharged before the 30th day, then they were monitored until the day of discharge. We have added this information in the Methods section.

Page 5, Lines 69–73

This study had a prospective cohort design. This study was approved by the ethics committee of Suiseikai Kajikawa Hospital and was performed according to the national government's guidelines based on the Helsinki Declaration of 1964. Written informed consent was obtained from all the patients or their relatives. All assessors were blinded to the data for analyses.

Page 5, Line 76–Page 6, Line 86

All consecutive patients with acute ischemic or hemorrhagic stroke who were admitted to Suiseikai Kajikawa Hospital within 1 week of disease onset between June 1, 2015, and August 31, 2015 were included in this cohort study. Patients who were under 20 years old, did not provide consent (for patients who could not provide consent, consent was obtained from their relatives), were in coma (best eye response score on the Glasgow coma scale of 1), underwent craniotomy, were on mechanical ventilation, or diagnosed with aspiration pneumonia in the hospital were excluded. Aspiration pneumonia was diagnosed according to the criteria of the Centers for Disease Control and Prevention [10]. We monitored patients for signs of pneumonia for 30 days after admission. If the patients were discharged before the 30th day, then they were monitored until the day of discharge.

Comment 2: Please add explanation on sample size determination; the parameters used in the calculation.

Response 2: We calculated the sample size using data from our previous report. In the previous report, we measured the tongue pressure in patients with acute stroke and compared the modified Mann Assessment of Swallowing Ability (MASA) score, which is an established bedside assessment tool that indicates the risk of swallowing dysfunction. It is reported that a modified MASA score <95 suggests swallowing dysfunction. In the previous study, we investigated the difference in tongue pressure between the modified MASA score <95 and ≥95 groups; the effect size was 1.56 (strong). This parameter was used in calculating the sample size for this study. This explanation has been added to the Methods section.

Page 9, Lines 138–146

We calculated the required sample size based on our previous study on tongue pressure in acute stroke [7]. In the previous study, tongue pressure was compared using the modified Mann Assessment of Swallowing Ability (MASA) score, which is an established bedside assessment tool that indicates the risk of developing swallowing dysfunction. A modified MASA score of <95 suggests swallowing dysfunction. The difference in the tongue pressure between the modified MASA score <95 and ≥95 groups was investigated, and the effect size was strong. This parameter was used to calculate the study sample size. Using an alpha level of 0.05 and a power of 0.80, 56 participants were required to participate in this study.

Comment 3: Please explain on sampling method in related to “consecutive acute stroke patients…”.

Response 3: We revised the information on the sampling method accordingly. Following the inclusion and exclusion criteria, 80 patients were included in the study finally. We revised the manuscript and added the flowchart of the inclusion and exclusion criteria in the Results section.

Page 5, Line 76–Page 6, Line 86

All consecutive patients with acute ischemic or hemorrhagic stroke who were admitted to Suiseikai Kajikawa Hospital within 1 week of disease onset between June 1, 2015, and August 31, 2015 were included in this cohort study. Patients who were under 20 years old, did not provide consent (for patients who could not provide consent, consent was obtained from their relatives), were in coma (best eye response score on the Glasgow coma scale of 1), underwent craniotomy, were on mechanical ventilation, or diagnosed with aspiration pneumonia in the hospital were excluded. Aspiration pneumonia was diagnosed according to the criteria of the Centers for Disease Control and Prevention [10]. We monitored patients for signs of pneumonia for 30 days after admission. If the patients were discharged before the 30th day, then they were monitored until the day of discharge.

Page 10, Lines 159–165

A total of 105 patients were eligible for this study. No patient was below 20 years old. Eleven patients or their relatives did not provide consent, two patients underwent craniotomy, and one patient was on mechanical ventilation. Among the remaining patients, eight patients were not evaluated because of a poor general condition, and three patients were diagnosed with aspiration pneumonia. Therefore, 80 patients were included in the study. A flowchart of the inclusion and exclusion criteria is shown in Fig 1.

Comment 4: Should report median with interquartile range.

Response 4: We have added the interquartile range in the Manuscript and tables.

Page 9, Lines 134–137

Data are expressed as median (minimum, 25th percentile, 75th percentile, maximum) for continuous variables (age, body mass index, NIHSS score, FILS, diet form, and tongue pressure) and as frequencies (percentages) for categorical variables (stroke subtypes and histories of comorbidities).

Comment 5: Revise the findings. Should state the outcome for each analysis. Tongue pressure influence the dysphagia diet or vice versa. Please explain.

Response 5: Thank you for this recommendation. Tongue pressure influences the dysphagia diet form. Thus, tongue pressure should be an explanatory variable, and the dysphagia diet form should be the response variable. We have deleted FILS and the dysphagia diet form in Table 2. We also performed a reanalysis with FILS and dysphagia diet form as response variables (Table 3). We revised the tables and manuscript as follows. The Abstract was also revised.

Page 2, Lines 28–30

In multivariate analysis, only tongue pressure was significantly associated with the dysphagia diet form (p<0.001).

Page 9, Lines 146–150

To evaluate the association between tongue pressure and dysphagia diet form, the baseline data of the patients were analyzed, and two-step strategies were used to assess the significant importance of variables in the association between tongue pressure and FILS/dysphagia diet form using a least square linear regression analysis.

Page 11, Line 180–Page 12, Line 185

The associations between the factors listed in Table 1 (except for FILS and dysphagia diet form because they are response variables) and tongue pressure at admission were evaluated. In univariate analysis, age, sex, body mass index, diabetes mellitus, dyslipidemia, and NIHSS score were associated with tongue pressure. In multivariate analysis, age and NIHSS score were significant independent factors for tongue pressure (Table 2).

Page 12, Line 195–Page 13, Line 202

Next, the associations between the factors listed in Table 1 and FILS/dysphagia diet form were evaluated. Regarding FILS in univariate analysis, age, sex, dyslipidemia, NIHSS score, and tongue pressure were associated with FILS. In multivariate analysis, NIHSS score and tongue pressure were significant independent factors for FILS (Table 3A). Regarding dysphagia diet form, in univariate analysis, age, sex, body mass index, NIHSS score, and tongue pressure were associated with dysphagia diet form. In multivariate analysis, only tongue pressure was significantly associated with the dysphagia diet form (Table 3B).

Comment 6: The authors should control the confounder for comparison of mean tongue pressure for each group of dysphagia diet; ANCOVA instead of ANOVA.

Response 6: We re-analyzed using ANCOVA. We revised the Methods section.

Page 10, Lines 153–154

The analysis of co-variance was used to compare the mean tongue pressure between the dysphagia diet groups.

Page 14, Lines 214–216

The mean tongue pressures of the dysphagia diet groups were compared (Fig. 2). After adjusting for age and NIHSS score, which were associated with tongue pressure, the mean tongue pressure increased significantly as the dysphagia diet code increased.

Comment 7: Do all the assumptions of the test fulfilled? Please explain.

Response 7: As mentioned in “Response 5,” we reanalyzed the data and specified which variables were the response and explanatory variables. Based on those, we performed multivariate and ROC analyses. We have clearly presented the assumptions and made revisions to explain this in the revised manuscript.

Page 5, Lines 63–65

We investigated the association between tongue pressure and dysphagia diet form and searched for the suitable tongue pressure for choosing each diet form.

Page 9, Line 146–Page 10, Line 156

To evaluate the association between tongue pressure and dysphagia diet form, the baseline data of the patients were analyzed, and two-step strategies were used to assess the significant importance of variables in the association between tongue pressure and FILS/dysphagia diet form using a least square linear regression analysis. First, a univariate analysis was performed, and factors with p <0.05 were selected. In a multi-factorial analysis, least linear regression analyses were performed with the selected factors. The analysis of co-variance was used to compare the mean tongue pressure between the dysphagia diet groups. Moreover, receiver operating characteristic (ROC) analyses were performed to determine the tongue pressure to predict suitable diet forms. Statistical significance was set at p <0.05.

Comment 8: Please justify the use of ROC analysis.

Response 8: As we mentioned in “Response 5,” FILS and the dysphagia diet form are response variables. Because we revealed the association between FILS/dysphagia diet form and tongue pressure (Table 3), an ROC analysis was performed to determine the tongue pressure that could predict the dysphagia diet form.

Page 15, Lines 222–224

Because we revealed the association between FILS/dysphagia diet form and tongue pressure (Table 3), ROC analyses were performed to determine the tongue pressure that can be used to predict a suitable dysphagia diet.

Comment 9: Table 1: Delete All. Should write n=80 at the end of table title. Replace it with n(%). Delete n(%) written after factors. Should report median (IQR).

Response 9: We revised Table 1 as recommended.

Comment 10: Table 2: Any reason run different model. What is predictor? Does it refer to regression coefficient? Please the results of categorical factors. Should state the reference.

Response 10: We deleted FILS and the dysphagia diet form in Table 2 because they should be response variables. Thus, the different models were also deleted. Predictor means regression coefficient. Regarding categorical factors, we have stated the reference in the footnote of the tables (Revised Tables 2 and 3).

Reviewer #2: This study by Nakamori et al evaluated if tongue pressure measurement is a sensitive indicator for determining diet form and swallowing capability among a sample of 80 patients hospitalized for acute stroke in a Japanese hospital. The authors found that tongue pressure measured on admission by a multidisciplinary team is significantly associated with diet form and swallowing. The manuscript is very well-written and describes an interesting research question with clear clinical implications. I have some comments about the presentation of the methods and results:

Comment 1: Page 10 lines 144-146: Please describe the additional parameters used to calculate sample size (e.g., effect size based on prior literature)

Response 1: We calculated the sample size using data from our previous report. In the previous report, we measured the tongue pressure in patients with acute stroke and compared the modified Mann Assessment of Swallowing Ability (MASA) score, which is an established bedside assessment tool that indicates the risk of swallowing dysfunction. It is reported that a modified MASA score of <95 suggests swallowing dysfunction. In the previous study, we investigated the difference in tongue pressure between the modified MASA score <95 and ≥95 groups; the effect size was 1.56 (strong). This parameter was used for calculating the sample size for this study. This explanation has been added to the Methods section.

Page 9, Lines 138–146

We calculated the required sample size based on our previous study on tongue pressure in acute stroke [7]. In the previous study, tongue pressure was compared using the modified Mann Assessment of Swallowing Ability (MASA) score, which is an established bedside assessment tool that indicates the risk of developing swallowing dysfunction. A modified MASA score of <95 suggests swallowing dysfunction. The difference in the tongue pressure between the modified MASA score <95 and ≥95 groups was investigated, and the effect size was strong. This parameter was used to calculate the study sample size. Using an alpha level of 0.05 and a power of 0.80, 56 participants were required to participate in this study.

Comment 2: Page 10 lines 148: More details about the multivariable model are important to state. Please explicitly state what the dependent variable is and how it was operationalized (continuous, categorical, etc). Along the same lines, what type of multivariable model was used (linear, logistic, etc)? What covariates did you consider in the model and how were they operationalized (Was NIHSS at admission and was it measured as a continuous variable? Same with BMI and comorbidities.)

Response 2: Thank you for your recommendation. In the previous manuscript, there was some ambiguity related to the explanatory and response variables. The FILS and dysphagia diet form should be response variables; however, we analyzed them as explanatory variables in Table 2. Thus, we deleted FILS and the dysphagia diet form in Table 2. We also performed a reanalysis using FILS and dysphagia diet form as response variables (Table 3). We revised the tables and manuscript accordingly. We used age, body mass index, NIHSS score, FILS, diet form, and tongue pressure as continuous variables, whereas stroke subtypes and comorbidities were categorical variables. The multivariable models were least linear regressions. We have added this information in the Methods section.

Page 9, Lines 134–137

Data are expressed as median (minimum, 25th percentile, 75th percentile, maximum) for continuous variables (age, body mass index, NIHSS score, FILS, diet form, and tongue pressure) and as frequencies (percentages) for categorical variables (stroke subtypes and histories of comorbidities).

Page 9, Lines 146–150

To evaluate the association between tongue pressure and dysphagia diet form, the baseline data of the patients were analyzed, and two-step strategies were used to assess the significant importance of variables in the association between tongue pressure and FILS/dysphagia diet form using a least square linear regression analysis.

Page 10, Line 150–Page 10, Line 153

First, a univariate analysis was performed, and factors with p <0.05 were selected. In a multi-factorial analysis, least linear regression analyses were performed with the selected factors.

Page 11, Line 180–Page 12, Line 185

The associations between the factors listed in Table 1 (except for FILS and dysphagia diet form since they are response variables) and tongue pressure at admission were evaluated. In univariate analysis, age, sex, body mass index, diabetes mellitus, dyslipidemia, and NIHSS score were associated with tongue pressure. In multivariate analysis, age and NIHSS score were significant independent factors for tongue pressure (Table 2).

Page 12, Line 195–Page 13, Line 202

Next, the associations between the factors listed in Table 1 and FILS/dysphagia diet form were evaluated. Regarding FILS in univariate analysis, age, sex, dyslipidemia, NIHSS score, and tongue pressure were associated with FILS. In multivariate analysis, NIHSS score and tongue pressure were significant independent factors for FILS (Table 3A). Regarding dysphagia diet form, in univariate analysis, age, sex, body mass index, NIHSS score, and tongue pressure were associated with dysphagia diet form. In multivariate analysis, only tongue pressure was significantly associated with the dysphagia diet form (Table 3B).

Comment 3: Page 11 (Table 1): It would be more helpful to know the IQR when you present descriptive statistics (rather than minimum and maximum), especially for your key variables of interest (FILS, diet form). More information about distribution of the FILS, diet form, and tongue pressure, would be helpful to the reader since these are key variables in your study.

Response 3: We have added the interquartile range in the manuscript and tables. We have submitted all other relevant data of the study as supplemental data.

Page 9, Lines 134–137

Data are expressed as median (minimum, 25th percentile, 75th percentile, maximum) for continuous variables (age, body mass index, NIHSS score, FILS, diet form, and tongue pressure) and as frequencies (percentages) for categorical variables (stroke subtypes and histories of comorbidities).

Comment 4: Page 13 (Table 2): Some comments on the presentation of data in Table 2. What is the reference group for categorical variables (sex, hypertension, diabetes, etc)? This should be clearly labeled in the table. Is the “predictor” column referring to beta coefficients?

Response 4: First, as Reviewer 1 recommended, we have deleted FILS and the dysphagia diet form in Table 2 because they should be response variables. Thus, the different models were also deleted. Predictor means regression coefficient. Regarding categorical factors, we have stated the reference in the footnote of the tables (Revised Tables 2 and 3).

Comment 5: Page 15 Figure 1: Please indicate that the bars are (95%?) confidence intervals

Response 5: We have added the explanation of the bars in the footnotes.

Comment 6: Page 15 lines 191-192: The mention of ROC analyses was a surprise as I was reading the article. ROC needs to be described in the methods section.

Response 6: We have details of the ROC analyses in the Methods and Results sections.

Page 10, Lines 154–155

Moreover, receiver operating characteristic (ROC) analyses were performed to determine the tongue pressure to predict suitable diet forms.

Comment 7: I’m a little confused about the wording in the manuscript. Are you classifying FILS (swallowing capability) as another measure of diet form? For example, the caption for figure 2 only refers to diet form, even though panel A discusses FILS.

Response 7: FILS measures swallowing ability without considering the diet form. However, in a real clinical setting, it is important to know whether the patient can take food orally completely, which corresponds to a FILS of 7. We have explained this carefully in the manuscript for readers to understand.

Page 15, Lines 222–229

Because we revealed the association between FILS/dysphagia diet form and tongue pressure (Table 3), ROC analyses were performed to determine the tongue pressure that can be used to predict a suitable dysphagia diet. FILS measures swallowing ability without considering the diet form. However, in a real clinical setting, it is important to know whether the patient can take food completely orally. A state of complete oral intake corresponds to FILS ≥7; therefore, we investigated the optimal cutoff tongue pressure for predicting a FILS of ≥7. The cut-off was 9.6 kPa (χ2=46.83, p<0.001, sensitivity 100.0%, specificity 92.8%, AUC=0.991) (Fig 2A).

Comment 8: It may be useful to have information about training to conduct tongue pressure. Who performed it in the multidisciplinary team? Was there standardized training or is this part of routine clinical practice so this type of standardization is not needed? This would be useful if the reader wants to consider how they can translate these results to their own clinical practice.

Response 8: Tongue pressure measurement is part of the routine clinical practice in our institution, and it does not require special skills. However, since standardization is essential for any clinical study, the nurses were trained. Moreover, we reconfirmed the reliability of tongue pressure measurement. We have added this explanation in the revised manuscript.

Page 8, Lines 128–131

The reliability of intraindividual measurements has been reported previously [17]. We reconfirmed the reliability of the measurements in this study. Measurements were taken repeatedly for ten days in normal subjects, and the resulting coefficient of variation was 5.64%.

Page 18, Lines 289–293

In clinical practice, it is important for a multidisciplinary swallowing team to diagnose dysphagia as early as possible to start managing nutrition and preventing aspiration pneumonia. Although we reconfirmed the reliability of tongue pressure measurement, it does not require special skills. In this study, tongue pressure was measured on admission—this is recommendable.

Reviewer #3: Thank you for allowing us to read your interesting manuscript. This study provides information about the tongue pressure, such as a non-invasive bedside assessment tool for deciding the diet form for acute stroke patients. It is a great effort, congratulations. Please consider the following comments.

Comment 1: In many parts of the manuscript appears the word “dysphasia” (9 times) including the tittle, which I think should be corrected to “dysphagia”.

Response 1: Thank you for pointing out this error. We have corrected the word “dysphasia” to “dysphagia”.

Comment 2: It should be important that the abstract conclusion make it clear that tongue pressure is just one tool within other evaluations (such cough function) that must be made to patient to decide the type of diet, similar to the idea expressed in the extend conclusion.

Response 2: Thank you for this recommendation. We have revised the conclusion of the Abstract accordingly.

Page 2, Line 34–Page 3, Line 37

Tongue pressure is one of the sensitive indicators for choosing dysphagia diet forms in patients with acute stroke. A combination of simple modalities will increase the accuracy of the swallowing assessment and choice of the diet form.

Comment 3: More than 50% of the sample were minor strokes (NIHSS �5), which could be a limitation when extending the results to more serious strokes.

Response 3: Thank you for this recommendation. We added this as a limitation.

Page 19, Lines 294–299

This study had limitations. First, it was performed in a single institution and might have sources of bias. The sample size was small. More than half of the patients had mild stroke, which could prevent the generalizability of the results to a population with severe stroke. It would be difficult to measure the tongue pressure of patients with severe stroke accurately. Future multicenter research would be needed to eliminate the effects of bias.

Comment 4: It should be important that you give a recommendation regarding the appropriate timing for the initiation of this post-stroke test (tongue pressure), depending on the moment in which you carried out these evaluations in the study.

Response 4: It is important to evaluate dysphagia as early as possible to start managing nutrition and preventing aspiration pneumonia. In this study, we measured the tongue pressure on admission. We have added this recommendation in the Discussion section.

Page 18, Lines 289–293

In clinical practice, it is important for a multidisciplinary swallowing team to diagnose dysphagia as early as possible to start managing nutrition and preventing aspiration pneumonia. Although we reconfirmed the reliability of tongue pressure measurement, it does not require special skills. In this study, tongue pressure was measured on admission—this is recommendable.

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Decision Letter 1

Wisit Cheungpasitporn

24 May 2021

Relationship between tongue pressure and dysphagia diet in patients with acute stroke

PONE-D-21-05820R1

Dear Dr. Masahiro Nakamori,

We’re pleased to inform you that your manuscript has been judged scientifically suitable for publication and will be formally accepted for publication once it meets all outstanding technical requirements.

Within one week, you’ll receive an e-mail detailing the required amendments. When these have been addressed, you’ll receive a formal acceptance letter and your manuscript will be scheduled for publication.

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Kind regards,

Wisit Cheungpasitporn, MD

Academic Editor

PLOS ONE

Additional Editor Comments:

I reviewed the revised manuscript and the response to reviewers' comments. Revised Manuscript is well written. All comments have been addressed and thus accepted for publication.

Reviewers' comments:

Reviewer's Responses to Questions

Comments to the Author

1. If the authors have adequately addressed your comments raised in a previous round of review and you feel that this manuscript is now acceptable for publication, you may indicate that here to bypass the “Comments to the Author” section, enter your conflict of interest statement in the “Confidential to Editor” section, and submit your "Accept" recommendation.

Reviewer #2: All comments have been addressed

Reviewer #3: All comments have been addressed

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2. Is the manuscript technically sound, and do the data support the conclusions?

The manuscript must describe a technically sound piece of scientific research with data that supports the conclusions. Experiments must have been conducted rigorously, with appropriate controls, replication, and sample sizes. The conclusions must be drawn appropriately based on the data presented.

Reviewer #2: (No Response)

Reviewer #3: Yes

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3. Has the statistical analysis been performed appropriately and rigorously?

Reviewer #2: (No Response)

Reviewer #3: Yes

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4. Have the authors made all data underlying the findings in their manuscript fully available?

The PLOS Data policy requires authors to make all data underlying the findings described in their manuscript fully available without restriction, with rare exception (please refer to the Data Availability Statement in the manuscript PDF file). The data should be provided as part of the manuscript or its supporting information, or deposited to a public repository. For example, in addition to summary statistics, the data points behind means, medians and variance measures should be available. If there are restrictions on publicly sharing data—e.g. participant privacy or use of data from a third party—those must be specified.

Reviewer #2: (No Response)

Reviewer #3: Yes

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5. Is the manuscript presented in an intelligible fashion and written in standard English?

PLOS ONE does not copyedit accepted manuscripts, so the language in submitted articles must be clear, correct, and unambiguous. Any typographical or grammatical errors should be corrected at revision, so please note any specific errors here.

Reviewer #2: (No Response)

Reviewer #3: Yes

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6. Review Comments to the Author

Please use the space provided to explain your answers to the questions above. You may also include additional comments for the author, including concerns about dual publication, research ethics, or publication ethics. (Please upload your review as an attachment if it exceeds 20,000 characters)

Reviewer #2: (No Response)

Reviewer #3: Dr Masahiro Nakamori, thank you for making the requested changes, the article is much clearer now and I consider it is a good contribution for this subtype of patients.

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Reviewer #2: No

Reviewer #3: Yes: Vanessa Cano-Nigenda

Acceptance letter

Wisit Cheungpasitporn

26 May 2021

PONE-D-21-05820R1

Relationship between tongue pressure and dysphagia diet in patients with acute stroke

Dear Dr. Nakamori:

I'm pleased to inform you that your manuscript has been deemed suitable for publication in PLOS ONE. Congratulations! Your manuscript is now with our production department.

If your institution or institutions have a press office, please let them know about your upcoming paper now to help maximize its impact. If they'll be preparing press materials, please inform our press team within the next 48 hours. Your manuscript will remain under strict press embargo until 2 pm Eastern Time on the date of publication. For more information please contact onepress@plos.org.

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Thank you for submitting your work to PLOS ONE and supporting open access.

Kind regards,

PLOS ONE Editorial Office Staff

on behalf of

Dr. Wisit Cheungpasitporn

Academic Editor

PLOS ONE

Associated Data

    This section collects any data citations, data availability statements, or supplementary materials included in this article.

    Supplementary Materials

    S1 Data. All relevant data of the study.

    (XLSX)

    Click here for additional data file. (14.3KB, xlsx)
    Attachment

    Submitted filename: response_to_reviewer_submission.docx

    Click here for additional data file. (48KB, docx)

    Data Availability Statement

    All relevant data are within the manuscript and its Supporting information files.

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