Abstract
Head lifting strength can be easily measured without special equipment. The relationship between head lifting strength and dysphagia is well-established. However, its association with Pharyngeal residuals—a risk factor for aspiration—has not yet been explored. This study aimed to determine the association between head lifting strength and Pharyngeal residuals, as assessed through a Videofluoroscopic swallowing study (VFSS), in older inpatients with suspected dysphagia. A total of 50 patients who underwent VFSS for suspected dysphagia were included. Head lifting strength was measured as the number of repetitions of maximum head lifting and the time to maintain maximum head lifting. The Normalized Residue Ratio Scale (NRRS) was scored at the valleculae (NRRSv) and piriform sinus (NRRSp) while swallowing 3 ml of a moderately thick liquid during the VFSS. Univariate and multiple regression analyses examined the relationship between head lifting strength and NRRSv and NRRSp. The time to maintain maximum head lifting and the number of repetitions of maximum head lifting were significantly negatively correlated with the NRRSv and NRRSp. However, in the adjusted multiple regression analysis model, only the number of repetitions of maximum head lifting was related to NRRSv and NRRSp. This study implies that a simple head lifting strength test can be implemented in the clinic to determine the risk of pharyngeal residuals after swallowing and, consequently, the possibility of aspiration.
Keywords: Head Lifting Strength, Pharyngeal Residuals, The Normalized Residue Ratio Scale, Videofluoroscopic Swallowing Study
Introduction
The number of older adults in Japan with impaired feeding and dysphagia continues to increase [1]. Swallowing difficulties may lead to various complications, including nutritional disorders, muscle weakness, impaired mobility, poor wound healing, dehydration, aspiration, choking, pneumonia, and decreased quality of life [2]. Therefore, an accurate assessment of dysphagia is crucial for planning effective interventions.
The videofluoroscopic swallowing study (VFSS) is considered the gold standard for evaluating dysphagia [3], where patients swallow a contrast medium, allowing clinicians to observe swallowing dynamics. Pharyngeal residuals that exceed a specific threshold in the valleculae may lead to aspiration during subsequent swallowing [4]. Some researchers have suggested that the head-turn-plus-chin-down maneuver may help eliminate vallecular residue [5], while the chin-tuck maneuver may reduce pyriform sinus residue [6]. Since the optimal approach varies based on the location of pharyngeal residue, predicting pharyngeal residue accurately is essential in clinical practice.
Maximum tongue pressure and jaw-opening force have garnered attention as methods for assessing swallowing difficulties. Decreased maximum tongue pressure, commonly seen in older individuals and patients with dysphagia, is linked to swallowing challenges during meals, pharyngeal residuals, and coughing while eating [7–12]. Similarly, the jaw-opening force also declines in older adults, correlating with increased risk of aspiration and pharyngeal residuals [13, 14]. However, these methods are limited by their dependence on specialized measurement equipment.
Swallowing-related muscle strength, which does not require specialized equipment to measure, can be assessed using head lifting strength. Methods for measuring head lifting strength include manual muscle testing (MMT), measurement of the number of repetitions of maximum head lifting [15], and measurement of the time to maintain maximum head lifting [15, 16]. MMT evaluates strength of individual muscle groups on a six-point scale. The number of repetitions of maximum head lifting assesses how many times a participant can lift their head from a supine position, while the time to maintain maximum head lifting measures the duration for which the head can be held raised from a supine position.
A previous study reported that decreased head lifting strength, as assessed by MMT, is associated with dysphagia and malnutrition [17]. However, in that study, only two groups were compared: those with MMT scores of 3 or higher and those with scores of 2 or lower for neck flexor muscles. Additionally, in clinical settings, dysphagia is often observed even in patients with an MMT score of 5 for neck flexor muscles, though its prevalence in these cases remains unclear. Consequently, elucidating the relationship between dysphagia and alternative assessments of head lifting strength is essential to address these limitations.
The evaluation method — whether the number of repetitions of maximum head lifting or the time to maintain maximum head lifting — that is more related to dysphagia remains unclear. This study aimed to determine the association between the number of repetitions of maximum head lifting or the time to maintain maximum head lifting and pharyngeal residuals in older hospitalized patients using VFSS.
Materials and Methods
This study is a prospective observational study targeting individuals suspected of dysphagia who underwent VFSS at Hyogo Medical University Hospital between June 2022 and October 2023. Individuals with cognitive decline or aphasia that prevented the measurement of swallowing-related muscle strength, patients with neck injuries, and those with a tracheal cannula were excluded. Given practical constraints, we aimed to enroll as many eligible participants as possible within this timeframe. This study was approved by the Institutional Ethics Committee of Hyogo Medical University, and all patients provided written informed consent.
Overall Experimental Procedure
Swallowing-related muscle strength was evaluated within seven days before or after the VFSS. To minimize participant fatigue, a rest period of approximately three to five minutes was provided between each test. Notably, the number of repetitions of maximum head lifting and the duration of maximum head lift maintenance were measured on separate days to avoid the effects of cumulative fatigue on the results.
Number of Repetitions of Maximum Head Lifting
The number of repetitions for maximum head lifting was measured following the method outlined in the study of Maeda and Fujishima [15]. Prior to evaluating head lifting strength, the head was manually raised from the supine position to measure the full range of motion. Participants were positioned in a supine position on a horizontal bed with their shoulders in contact with the bed, instructed to raise their heads to the maximum range of motion, and lower them as many times as possible. Specifically, the head was raised and lowered at intervals of approximately one second each. Before commencing the exercise, participants were advised not to hold their breath. The evaluator was positioned on the side of the participant and visually checked the amount of head elevation. In this study, one repetition was counted each time the participant’s head was lifted beyond half the maximum range of motion. The exercise was terminated if their head did not reach beyond half of the maximum range of motion for three consecutive repetitions (Fig. 1).
Fig. 1.
Number of repetitions of maximum head lifting and time to maintain maximum head lifting
Time to Maintain Maximum Head Lifting
The time to maintain maximum head lifting was measured following the method outlined in previous studies [15, 16]. Participants lying in a supine position on a flat bed were instructed to lift their heads with their shoulders resting on the bed. The exercise was concluded when the participant’s head returned to the bed or when the head position noticeably dropped below half of the maximum range of motion. The duration for which head elevation was maintained is referred to as the time taken to maintain maximum head elevation.
Maximum Tongue Pressure
The maximum tongue pressure was measured using a JMS tongue pressure measuring device (JMS Corporation, Hiroshima). To measure anterior tongue pressure, participants were instructed to gently hold the rigid ring of the probe between their upper and lower incisors and to use their tongue to press the balloon against the palate with maximal force. The measurement duration was seven seconds, and the average of three measurements was used to determine the maximum tongue pressure [8]. A rest period of approximately five to ten seconds was provided between each measurement.
Jaw-Opening Force
The jaw-opening force was measured using a jaw-opening sthenometer (Livet Inc., Tokyo, Japan). The participants’ heads and chins were firmly fixed in place with a specialized belt, and they were instructed to open their mouths as strongly as possible. In this study, after instructing the participants to achieve maximum mouth opening, we confirmed that the value displayed on the LCD screen reached its peak within approximately three seconds, and we recorded this peak value. The maximum value from three attempts was recorded as the jaw-opening force [13, 14]. A rest period of approximately five to ten seconds was provided between each measurement.
Data Collection
Basic demographic and health information were assessed, including age, sex, height, weight, body mass index (BMI), skeletal mass index (SMI), grip strength, presence of sarcopenia, Functional Oral Intake Scale (FOIS), and cognitive function. The SMI was calculated using InBody S10 (InBody Japan, Tokyo, Japan) to estimate limb muscle mass adjusted for height. The Asian Working Group for Sarcopenia 2019 criteria [18] were applied to evaluate sarcopenia. FOIS was used to evaluate oral intake status, which is rated on a 7-point scale ranging from ‘nothing by mouth’ (Level 1) to ‘total oral diet with no restrictions’ (Level 7) [19]. Cognitive function was assessed using the Revised Hasegawa’s Dementia Scale (HDS-R) [20].
Videofluoroscopic Swallowing Study
The patients underwent VFSS in the sitting position. They were asked to swallow a test solution consisting of 3 ml of a moderately thick liquid. Although other test materials (e.g., thin liquids, nectar-like liquids, jelly, and rice porridge) were also used depending on each patient’s swallowing function in the clinical setting, only a single swallow of 3 mL moderately thick liquid was used for analysis in this study. This solution was prepared by combining barium sulfate powder (Varitop P®, 99% w/w; Kaigen Pharma Corporation, Osaka, Japan) with water to achieve a 40% weight/volume concentration of barium sulfate. Subsequently, 200 mL of the diluted solution was mixed with a xanthan gum thickener (3 g; Tsururinko Quickly; Morinaga Dairy Clinic, Tokyo, Japan) to create a moderately thick solution. The viscosity of the test solution was assessed using the International Dysphagia Diet Standardization Initiative (IDDSI) flow test [21] and confirmed to be IDDSI level three (moderate concentration). The VFSS was recorded at 30 frames per second using an HDD recorder (DIGA DMR-XP200; Panasonic Corporation, Japan). Subsequently, two speech therapists analyzed the VFSS using image analysis software (Image J; National Institutes of Health, USA).
Pharyngeal residuals were evaluated using the Normalized Residue Ratio Scale (NRRS) [22] and calculated at the valleculae (NRRSv) and piriform sinus (NRRSp), respectively. The NRRS score was calculated as the ratio of the residual volume to the pharyngeal cavity, normalized by the size of the cervical spine. After the swallowing was completed, the NRRS analyzed the frame when the hyoid descended to its lowest position (Fig. 2). The NRRS was calculated by two speech therapists, and the average value was used. To assess inter-rater reliability, the intraclass correlation coefficient (ICC [1, 2]) was calculated using a two-way random-effects model with absolute agreement. The ICC was 0.786 for NRRSv and 0.821 for NRRSp, indicating excellent and good reliability, respectively.
Fig. 2.
The assessment process by NRSS. NRRS was calculated as the ratio of residual volume to the pharyngeal cavity and normalized by the size of the cervical spine. NRRS analyzed the frame when swallowing was completed, and the hyoid descended to its lowest position
Statistical Analysis
Categorical variables are presented as number and percentages. Quantitative variables are presented as mean ± standard deviation or median (interquartile range [IQR], 25–75 percentile), depending on the normality of their distribution. The correlation coefficients between jaw-opening force and both the number of repetitions of maximum head lifting and the time to maintain maximum head lifting were calculated using Spearman’s rank correlation coefficient. Associations between swallowing-related muscle strength (number of repetitions of maximum head lifting, time to maintain maximum head lifting, maximum tongue pressure, and jaw-opening force) and NRRSv and NRRSp obtained from the VFSS were assessed using Spearman’s rank correlation coefficient. A multiple regression analysis was conducted with NRRSv and NRRSp as outcome variables, and head lifting strength (number of repetitions of maximum head lifting and time to maintain maximum head lifting), age, and sex as explanatory variables. Since the purpose of this study was to examine the relationship with head lifting strength, variables related to muscle strength and muscle mass were not included as adjustment variables. Statistical significance was set at p < 0.05. All statistical analyses were performed using the R version 4.3.1 (The R Foundation for Statistical Computing, Vienna, Austria).
Results
Between June 2022 and October 2023, 103 individuals aged 65 and older, who were either hospitalized or visiting outpatient clinics at Hyogo Medical University Hospital, underwent a VFSS. Of these, 36 individuals were excluded from the analysis due to difficulty understanding instructions caused by cognitive decline, and 17 were excluded due to having neck injuries or tracheostomy tubes, making it impossible to measure head lift strength. The remaining 50 individuals were included in the analysis. Table 1 presents patient demographics. The mean age of the 50 analyzed participants was 76.5 ± 5.3 years, with 37 (74.0%) of the participants being male. The mean BMI was 18.7 ± 3.8 kg/m2, mean SMI was 6.1 ± 1.2 kg/m2, and mean grip strength was 18.7 ± 9.2 kg. Sarcopenia was detected in 30 (60.0%) participants. There were thirteen patients (26.0%) at FOIS level 7, seven patients (14.0%) at level 6, fifteen patients (30.0%) at level 5, three patients (6.0%) at level 4, 1 (2.0%) at level 3, six patients (12.0%) at level 2, and five patients (10.0%) at level 1. The median HDS-R score was 26 (IQR, 14–28). The diseases included malignant neoplasms in twenty-two patients (44.0%), neuromuscular diseases in thirteen patients (26.0%), respiratory diseases in eight patients (16.0%), disuse syndrome in six patients (12.0%), and cerebrovascular diseases in one patient (2.0%). The median number of repetitions of maximum head lifting was 6.5 (IQR, 0–11.5), median time to maintain maximum head lifting was 12.8 s (IQR, 0.0–27.7), mean maximum tongue pressure was 24.7 ± 7.9 kPa, and mean jaw-opening force was 5.3 ± 2.2 kg. In the VFSS, aspiration was observed in two patients with 3 ml of moderately thickened water. The median NRRSv obtained with the VFSS was 0.03 (IQR, 0.00–0.23), and the median NRRSp was 0.01 (IQR, 0.00–0.26).
Table 1.
Characteristics of the participants
| Characteristics | N=50 |
|---|---|
| Age, year (SD) | 76.5 (5.3) |
| Male, n (%) | 37 (74.0%) |
| BMI, kg/m2 (SD) | 18.7 (3.8) |
| SMI, kg/m2 (SD) | 6.1 (1.2) |
| Grip strength, kg (SD) | 18.7 (7.9) |
| Sarcopenia, n (%) | 30 (60.0%) |
| FOIS, n (%) | |
| 7 | 13 (26.0%) |
| 6 | 7 (14.0%) |
| 5 | 15 (30.0%) |
| 4 | 3 (6.0%) |
| 3 | 1 (2.0%) |
| 2 | 6 (12.0%) |
| 1 | 5 (10.0%) |
| HDS-R, score (IQR) | 26 (14–28) |
| Diagnosis of diseases, n (%) | |
| Cancer | 22 (44.0%) |
| Neuromuscular diseases | 13 (26.0%) |
| Respiratory diseases | 8 (16.0%) |
| Disuse syndrome | 6 (12.0%) |
| Cerebrovascular diseases | 1 (2.0%) |
| Number of repetitions of maximum head lifting, counts (IQR) | 6.5 (0–11.5) |
| Time to maintain maximum head lifting, seconds (IQR) | 12.8 (0.0–27.7) |
| Maximum Tongue Pressure, kPa (SD) | 24.7 (7.9) |
| Jaw-opening force, kg (SD) | 5.2 (2.2) |
| NRRSv (IQR) | 0.03 (0.00–0.23) |
| NRRSp (IQR) | 0.01 (0.00–0.26) |
BMI, Body Mass Index; SMI, Skeletal Muscle Mass Index; FOIS, Functional Oral Intake Scale; HDS-R, Revised Hasegawa’s Dementia Scale; NRRSv, Normalized Residue Ratio Scale for the valleculae; NRRSp, Normalized Residue Ratio Scale for the piriform sinus; SD, Standard deviation; IQR, Interquartile Range
We also calculated the correlation coefficients between jaw-opening force and both the number of repetitions of maximum head lifting and the time to maintain maximum head lifting. The results demonstrated significant correlations between jaw-opening force and the number of repetitions of maximum head lifting (ρ = 0.478, p < 0.001) as well as the time to maintain maximum head lifting (ρ = 0.471, p < 0.001).
Table 2 presents the rank correlation coefficients between swallowing-related muscle strength (number of repetitions of maximum head lifting, time to maintain maximum head lifting, maximum tongue pressure, and jaw-opening force) and NRRSv and NRRSp. The number of repetitions of maximum head lifting showed significant negative correlations with NRRSv (ρ = −0.41, p = 0.003) and NRRSp (ρ = −0.44, p = 0.001). Time to maintain maximum head lifting was significantly associated with NRRSv (ρ = −0.46, p < 0.001) and NRRSp (ρ = −0.37, p = 0.008). Maximum tongue pressure was significantly correlated with NRRSp (ρ = −0.37, p = 0.009). The jaw-opening force was not significantly associated with NRRSv or NRRSp.
Table 2.
The rank correlation coefficients between swallowing-related muscle strength and NRRSv and NRRSp
| NRRSv | NRRSp | |
|---|---|---|
| Number of repetitions of maximum head lifting (times) | −0.41* | −0.44* |
| Time to maintain maximum head lifting (seconds) | −0.46* | −0.37* |
| Maximum tongue pressure (kPa) | −0.25 | −0.38* |
| Jaw-opening force (kg) | −0.17 | −0.25 |
*p < 0.05
NRRSv, Normalized Residue Ratio Scale for the valleculae; NRRSp, Normalized Residue Ratio Scale for the piriform sinus
Multiple regression analyses were performed with NRRSv and NRRSp as dependent variables and head lifting strength (number of repetitions of maximum head lifting and time to maintain maximum head lifting), age, and sex as independent variables. The results showed that NRRSv (β = −0.32, p = 0.03) and NRRSp (β = −0.31, p = 0.03) were significantly associated with the number of repetitions of maximum head lifting (β = −0.32, p = 0.04) (Table 3).
Table 3.
Association between head lifting strength and pharyngeal residuals
| Independent variables | β | 95% CI | P-value | |
|---|---|---|---|---|
| A. NRRSv | ||||
| Number of repetitions of maximum head lifting | −0.32 | −0.61 | −0.03 | 0.03* |
| Time to maintain maximum head lifting | −0.31 | −0.60 | −0.03 | 0.03* |
| B. NRRSp | ||||
| Number of repetitions of maximum head lifting | −0.32 | −0.61 | −0.01 | 0.04* |
| Time to maintain maximum head lifting | −0.25 | −0.51 | 0.08 | 0.10 |
*p < 0.05
Adjusted for age and sex
β, standardized partial regression coefficient
NRRSv, Normalized Residue Ratio Scale for the valleculae; NRRSp, Normalized Residue Ratio Scale for the piriform sinus
Discussion
This study aimed to determine the association between head lifting strength and pharyngeal residuals using VFSS. The results showed that the number of repetitions of maximum head lifting was independently correlated with NRRSv and NRRSp, even after adjusting for age and sex. This study represents the first evidence of a link between head lifting strength and the NRRSv and NRRSp, indicators of pharyngeal residuals.
Association between Head Lifting Strength and Pharyngeal Residuals
The primary muscles involved in raising the head include the suprahyoid and infrahyoid muscle groups involved in swallowing, as well as the sternocleidomastoid muscle, an auxiliary respiratory muscle [23]. In particular, the suprahyoid muscle group play a role in pulling the hyoid bone and larynx anteriorly and superiorly. Furthermore, these muscles contribute to the relaxation and opening of the upper esophageal sphincter (UES) [24–26]. Head lifting exercises have been reported to increase the anterior excursion of the larynx and the anteroposterior diameter of the upper esophageal sphincter opening [27]. If the suprahyoid muscle weaken, the movement of the hyoid and larynx will become insufficient to open the esophageal inlet, resulting in pharyngeal residue and aspiration [13]. This suggests that our method provides a valid approximation of suprahyoid muscle strength, even though it does not measure maximal strength directly. It should be noted that the assessment of head-lifting strength in this study differs from conventional measures of maximal muscle strength, such as maximum voluntary contraction, which evaluates single-instance maximal force generation. Instead, our method employs endurance-based parameters —namely, the number of repetitions for maximum head lifting and the time to maintain maximum head lifting. Rather than absolute strength, these measures primarily reflect muscular endurance. However, previous research has established a strong correlation between endurance performance and maximal muscle strength [28, 29]. Therefore, although our method does not directly measure single-instance maximal muscle strength, it serves as a reasonable proxy for suprahyoid muscle strength in clinical settings. As a result, the number of repetitions of maximum head lifting emerged as an independent predictor of pharyngeal residuals. Future research may benefit from considering the number of repetitions of the maximum head lifting as an important evaluation item when assessing patients with suspected dysphagia. However, it has been revealed that the sternocleidomastoid muscle fatigues before other muscles during head lifting exercises [30]. Therefore, careful consideration is necessary when interpreting the results of this study.
Differences in the Number of Repetitions of Maximum Head Lifting and the time To Maintain Maximum Head Lifting
In the adjusted model, the number of repetitions of maximum head lifting was independently associated with NRRSv and NRRSp. In contrast, the time for which the head is maintained in a raised position for as long as possible was independently related to NRRSv only. A reduced range of hyoid and laryngeal elevations is a risk factor for aspiration and pharyngeal residuals [31]. Therefore, the hyoid and laryngeal elevations are important aspects of swallowing. Both hyoid and laryngeal elevations during swallowing are isotonic movements. The maximum number of head lifting repetitions represents an isotonic movement, whereas the time to maintain maximum head lifting is characterized as an isometric movement [26]. Thus, the number of repetitions of maximum head lifting, an isotonic movement pattern similar to the swallowing movement, may be more sensitive in detecting swallowing dynamics and dysphagia. In this study, both the number of repetitions of maximum head lifting and the time taken to maintain maximum head lifting showed significant correlations with pharyngeal residue, as measured by NRRSv and NRRSp. However, in multiple regression analysis, only the time to maintain maximum head lifting was not a significant predictor of NRRSp. Despite this, the overall trend of association between these head-lift measures and pharyngeal residue was relatively similar. Therefore, we plan to increase the sample sizes in future studies to validate these associations and to enhance the statistical power to detect the independent contribution of each head-lift parameter to pharyngeal residue.
Association between jaw-opening Force and Pharyngeal Residuals
In this study, jaw-opening force was not significantly associated with NRRSv or NRRSp. It has been shown that jaw-opening force is related to the cross-sectional area of the geniohyoid muscle [32]. Additionally, a study examining the relationship between jaw-opening force and pharyngeal residue in the vallecula and pyriform sinuses using the fiberoptic endoscopic evaluation of swallowing test reported a significant difference in jaw-opening force between groups with and without pharyngeal residue in these areas [14]. However, in previous studies, pharyngeal residue was assessed at three levels (trace or none, mild, and severe), and only severe cases were considered as having pharyngeal residue, focusing on participants with substantial pharyngeal residue.
In contrast, this study used the NRRS, a continuous scale, to assess pharyngeal residue. The median amount of pharyngeal residue among participants was low, with NRRSv at 0.03 (IQR, 0.00–0.23) and NRRSp at 0.01 (IQR, 0.00–0.26). These differences in the patient population may have influenced the results of this study.
Mouth opening involves the suprahyoid muscles, specifically the anterior belly of the digastric muscle, the geniohyoid muscle, and the mylohyoid muscle, as well as the lateral pterygoid muscle [13]. In contrast, head lifting involves the suprahyoid muscles, the infrahyoid muscles, and the sternocleidomastoid muscle [23]. These movements share common muscle groups, and in fact, this study confirmed a moderate correlation between jaw-opening force and head-lifting strength. However, jaw-opening force was measured under isometric conditions, which may not fully capture the dynamic muscle contractions required during swallowing. This methodological differences, along with the differences in specific muscle involvement, may have contributed to the lack of significant association between jaw-opening force and pharyngeal residue.
Nevertheless, given the limited existing evidence, this remains a hypothesis. Further research is needed to clarify the relationship between individual swallowing-related muscle strength and swallowing function.
Limitation
This study had several limitations. First, the study was conducted at a single institution, necessitating caution when generalizing the findings. Second, the safety of the evaluation method was not ascertained. Third, the sample size of 50 participants may have resulted in relatively wide confidence intervals, potentially affecting the precision of our estimates and the generalizability of the findings. Fourth, this study focused on hospitalized older patients with suspected dysphagia, which may limit the generalizability of the findings to older patients in outpatient settings. Additionally, the underlying diseases in hospitalized patients could have affected the assessment of head lifting strength. Fifth, the same evaluator who assessed head lifting strength also measured the NRRS, meaning that blinding was not achieved. However, to mitigate potential bias, the NRRS was calculated by two individuals, and the average value was used. Sixth, the method of evaluating head lifting strength used in this study does not strictly distinguish between muscle strength and endurance, and it is thought that it includes elements of endurance. However, the maximum number of repetitions and the duration of maintenance— both reflecting muscle strength—provide a clinically feasible and non-invasive approach, which represents a notable strength of our study. We aim to address these limitations by continuing data collection, enabling the addition of disease-specific subgroup analyses, and considering their application in clinical evaluation on a case-by-case basis.
Conclusion
The number of repetitions of maximum head lifting was independently associated with NRRSv and NRRSp, even after adjusting for age and sex. The number of repetitions of maximum head lifting may be a predictive marker for pharyngeal residuals.
Acknowledgements
We gratefully acknowledge the work of past and present staffs of the Department of Rehabilitation, Hyogo Medical University Hospital. This study was partly supported by the Japan Society for the Promotion of Science [KAKENHI (24H02712)].
Author Contributions
Kazuki Eimoto: Conceptualization, Data curation, formal analysis, Investigation, Methodology, Visualization, Writing of the Original Draft. Koutatsu Nagai: Conceptualization, Data curation, Methodology, Writing, reviewing, and editing. Yuta Nakao: Conceptualization, Writing, reviewing, and editing. Yuki Oshima: Conceptualization, Data curation, formal analysis. Takahiro Matsufuji: Conceptualization, Data curation. Takuya Hamana: Conceptualization, Data curation. Megumi Takato: Conceptualization, Data curation. Tomoyuki Ogino: Conceptualization, Writing, reviewing, and editing. Naoki Sasanuma: Conceptualization, Writing, reviewing, and editing. Yuki Uchiyama: Project administration, writing, Review & Editing. Kazuhisa Domen: Project administration, Supervision, Writing, reviewing, and editing.
Funding
This work was supported by JSPS KAKENHI Grant Number JP24 K02712.
Data Availability
Owing to the nature of this research, the participants of this study did not agree to share their data publicly; therefore, supporting data are not available.
Declarations
Conflict of interest
This work was supported by JSPS KAKENHI Grant Number JP24H02712.
Research Involving Human Participants
All procedures performed in studies involving human participants were in accordance with the ethical standards of the institutional and/or national research committee and with the 1964 Helsinki declaration and its later amendments or comparable ethical standards.
Ethics Approval
This study was reviewed and approved by the Medical Ethics Review Committee of Hyogo Medical University (No. 3304). All participants were provided with comprehensive information regarding the study’s objectives through written and verbal means, and their written consent was obtained.
Ethical Considerations
This study underwent review and received approval by the Medical Ethics Review Committee of Hyogo Medical University (No. 3304). All research participants were provided with comprehensive information regarding the study’s objectives through written and verbal means, and their consent was obtained in written form.
Footnotes
Publisher’s Note
Springer Nature remains neutral with regard to jurisdictional claims in published maps and institutional affiliations.
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Associated Data
This section collects any data citations, data availability statements, or supplementary materials included in this article.
Data Availability Statement
Owing to the nature of this research, the participants of this study did not agree to share their data publicly; therefore, supporting data are not available.