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Associations between tongue strength and skeletal muscle mass under dysphagia rehabilitation for geriatric out patients
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Original article
Associations between tongue strength and skeletal muscle mass under dysphagia rehabilitation for geriatric out patients Yujiro Nakazawaa , Takeshi Kikutania,b,* , Kumi Igarashia , Yuri Yajimab , Fumiyo Tamurab a
Division of Clinical Oral Rehabilitation, The Nippon Dental University, Graduate School of Life Dentistry, 1-9-20, Fujimi, Chiyoda, Tokyo 102-0071, Japan Division of Rehabilitation for Speech and Swallowing Disorders, The Nippon Dental University, Tama Oral Rehabilitation Clinic, 4-44-19, Koganei, Tokyo 1840011, Japan b
A R T I C L E I N F O
A B S T R A C T
Article history: Received 18 August 2018 Received in revised form 5 July 2019 Accepted 9 July 2019 Available online xxx
Purpose: The purpose of this study was to examine how skeletal muscle mass influences the effectiveness of dysphagia rehabilitation. Methods: The cross-sectional study and the prospective cohort study were conducted in a clinic, specialized in rehabilitation of patients with dysphagia, located in Tokyo, Japan. Skeletal muscle mass measurement by bioelectrical impedance analysis and tongue strength measurement were performed on 178 outpatients with dysphagia. In addition, the Barthel Index, Mini Nutritional Assessment-Short Form, and Functional Oral Intake Scale values were measured. Dysphagia rehabilitation was performed, and 88 of the patients who were available for follow-up one year later were included in a follow-up study. In the cross-sectional study, the associations between tongue strength and other factors were examined. In the follow-up study, factors associated with rehabilitation effectiveness, shown by tongue strength, were examined. Results: Tongue strength and skeletal muscle mass were correlated, and both decreased as eating and swallowing function level decreased. After one year of dysphagia rehabilitation, tongue strength and skeletal muscle mass increased. The factors associated with the amount of increase in tongue strength were initial tongue strength and skeletal muscle mass. Conclusions: For patients with dysphagia, maintenance of skeletal muscle mass was associated with improvement of tongue strength in rehabilitation. This indicates that prevention of sarcopenia in dysphagia patients contributes to the effect of rehabilitation. © 2019 Japan Prosthodontic Society. Published by Elsevier Ltd. All rights reserved.
Keywords: Tongue strength Skeletal muscle mass Dysphagia Rehabilitation Sarcopenia
1. Introduction Patients with dysphagia are known to have low energy intake and protein levels and fall into malnutrition [1]. Swallowing muscles are not an exception; muscle strength in the muscles related to swallowing has also been shown to decrease with malnutrition [2]. Kuroda and Kuroda [3] demonstrated that there is a relationship between eating and swallowing function and upper arm circumference in older inpatients with dysphagia. The cause of this may be related to a decrease in lean body mass that includes swallowing muscles, and the presence of dysphagia due to sarcopenia was suggested. Associations between dysphagia and a decrease in whole body muscle mass or the presence of
* Corresponding author at: Division of Rehabilitation for Speech and Swallowing Disorders, The Nippon Dental University, Tama Oral Rehabilitation Clinic, 4-44-19, Koganei, Tokyo 184-0011, Japan. E-mail address: [email protected] (T. Kikutani).
sarcopenia have been observed in patients with cancer [4], after surgery for major cardiovascular diseases [5], and with Alzheimer’s disease [6]. Tongue strength, which is often used as an indicator of the muscles related to swallowing, decreases with aging [7]. Moreover, tongue strength has been shown to be lower in people with dysphagia than those without [8], and a study of inpatients showed an association between tongue strength and the development of pneumonia [9]. These findings suggest that there is a strong relationship between tongue strength and eating and swallowing function. Maeda and Akagi measured tongue strength in 104 inpatients without a history of cerebrovascular diseases or neurodegenerative diseases, and they reported that a decrease in tongue strength was associated with the presence or absence of sarcopenia and dysphagia from sarcopenia [10]. Many studies have shown that grip and other forms of muscle strength are closely associated with nutritional status and skeletal muscle mass. Meanwhile, eating and swallowing function can be divided into several different levels, such as complete inability to take food orally, partial oral intake
https://doi.org/10.1016/j.jpor.2019.07.004 1883-1958/ © 2019 Japan Prosthodontic Society. Published by Elsevier Ltd. All rights reserved.
Please cite this article in press as: Y. Nakazawa, et al., Associations between tongue strength and skeletal muscle mass under dysphagia rehabilitation for geriatric out patients, J Prosthodont Res (2019), https://doi.org/10.1016/j.jpor.2019.07.004
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ability, or ability to take food orally by meal modification. However, no studies have fully examined the associations between tongue strength and eating and swallowing function, level of eating and swallowing function, physical functioning, and skeletal muscle mass. Moreover, many studies have supported the importance of maintaining eating and swallowing function to prevent malnutrition and pneumonia in older adults. Many studies have verified the importance of resistance training for improving eating and swallowing function, and the effectiveness of resistance training has been said to be stronger in people with a better nutritional status [11]. Studies have shown that poorer nutritional status or low skeletal muscle mass have more difficulty conducting activities of daily living (ADL) after rehabilitation [2]. However, what effects maintenance of nutritional status and skeletal muscle mass for improvement of eating and swallowing function have on rehabilitation remain unclear. In this study, we carried out based on the hypothesis that maintaining skeletal muscle affects the prognosis of dysphagia rehabilitation. 2. Materials and methods 2.1. Design and patient sample 2.1.1. Cross-sectional study A total of 588 of the 4441 outpatients who were examined at the Nippon Dental University Oral Rehabilitation Tama Clinic during the period from April 2014 to March 2017, excluding 1276 patients who were under 65 years of age and 2577 home care patients, were evaluated. Excluding patients who did not have dysphagia as a chief complaint, patients with oral cancer who had undergone an extensive glossectomy, and patients who could not have their tongue strength measured due to reduced cognitive functioning, one-hundred seventy-eight patients participated in a cross-sectional study. Patients with neuromuscular disease were excluded for follow-up studies. Furthermore, we excluded those who had data loss and those who came to the hospital only to evaluate their swallowing function. One hundred people were enrolled as followup study. At the start of the intervention, eating and swallowing function tests including videofluorography were performed on each participant. Tongue strength related to feeding swallowing function and skeletal muscle mass associated with sarcopenia were
examined. Based on those results, resistance training was performed to improve tongue strength, and comprehensive swallowing function training was performed according to each individual’s functioning level. In resistance training, we instructed the training to be performed twice a day for a total of 30 times with the goal of applying about 80% resistance, referring to the pressure of each person’s tongue. Depending on their nutritional status, the patients were given nutritional counseling from a registered dietitian. Of those who were available for follow-up one year later, 88 patients were included in a follow-up study (Fig.1) 2.2. Instrument Oral intake status was assessed with the Functional Oral Intake Scale (FOIS) [12]. Tongue strength was measured with the JMS tongue strength measurement device (JM-TPM; JMS Co., Ltd., Hiroshima, Japan) three times [13], and the average was used for the analysis. Nutritional status was assessed with the Mini Nutritional Assessment-Short Form (MNA-SF) [14]. ADL were measured using the Barthel Index [15], which is a basic ADL scale. For skeletal muscle mass, the InBody S10 (Inbody, Seoul, Korea) was used to take measurements, and the skeletal muscle mass index (SMI) was calculated [16]. The cut-off values for SMI to define sarcopenia for men and women were <7.0 kg/m2 and <5.7 kg/m2, respectively [17]. 2.3. Analysis Spearman’s rank correlation coefficients were used to examine the associations between tongue strength, SMI, and other factors. Factors with a probability of less than 10% on univariate analysis were set as independent variables, and the multiple regression analysis was performed. SPSS statistics 24 software (IBM, Tokyo, Japan) was used for all statistical analyses. The t-test was used to examine the comparison on between baseline and after year. The level of statistical significance was set at p < 0.05. 2.4. Ethics This study was conducted in compliance with the Declaration of Helsinki, after obtaining proper informed consent from each subject or his/her legal representatives, such as family members.
Outpatients n=4441 ・Under 65 years of age: n=1276 ・Home care patient: n=2577 n=588
Participants (cross-sectional study)
・No dysphagic complaint, Oral cancer, Dementia: n=410
n=178
Participants
・Neuromuscular disease: n=26
(enllored as follow-up study)
・Only evaluation: n=13
n=100
・Data missing: n=39
Fainal participants (follow-up study)
・Drop out due to hospitalization or death : n=12
n=88 Fig. 1. Study flowchart describing the exclusion of participants in the study.
Please cite this article in press as: Y. Nakazawa, et al., Associations between tongue strength and skeletal muscle mass under dysphagia rehabilitation for geriatric out patients, J Prosthodont Res (2019), https://doi.org/10.1016/j.jpor.2019.07.004
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Table 1. The characteristics of the subjects. Cross-sectional study (at the baseline)
Follow-up study (at the after a year)
Characteristic
Over all, n = 178
Men, n = 103
Women, n = 75
Over all, n = 88
Men, n = 55
Women, n = 33
Age, mean SD SMI, mean SD MNA-SF, mean SD Barthel Index, mean SD Tongue strength, KPa, mean SD FOIS Level 1, n(%) Level 2, n(%) Level 3, n(%) Level 4, n(%) Level 5, n(%) Level 6, n(%) Level 7, n(%)
79.44 7.20 5.98 1.00 9.75 2.78 83.68 22.00 21.01 9.03 5 (2.81) 5 (2.81) 2 (1.12) 44 (24.72) 41 (23.03) 69 (38.76) 12 (6.74)
79.12 6.73 6.49 0.09 9.58 3.06 82.23 21.59 21.04 9.66 4 (3.9) 3 (2.9) 2 (1.9) 26 (25.2) 22 (21.4) 40 (38.8) 6 (5.8)
79.88 7.82 5.29 0.72 9.97 2.34 85.67 22.55 20.96 8.13 1 (1.3) 2 (2.7) 0 (0) 18 (24.0) 19 (25.3) 29 (38.7) 6 (8.0)
79.36 6.90 5.99 1.01 9.91 2.66 84.94 20.40 21.22 9.42 2 (2.27) 2 (2.27) 0 (0) 22 (25) 23 (26.14) 38 (43.18) 1 (1.14)
79.35 6.81 6.50 0.82 9.82 2.87 85.09 19.16 20.36 10.49 2 (3.6) 1 (1.8) 0 (0) 13 (23.6) 15 (27.3) 24 (43.6) 0 (0)
79.39 7.15 5.15 0.69 10.06 2.30 84.70 22.64 22.66 7.23 0 (0) 1 (3.0) 0 (0) 9 (27.3) 8 (24.2) 14 (42.4) 1 (3.0)
SD: standard deviation; SMI: Skeletal Muscle Mass Index; MNA-SF: Mini Nutritional Assessment-Short Form; FOIS: Functional Oral Intake Scale.
Table 2. The relationships between the measurements in the cross-sectional study (correlation matrix table). Tongue strength Tongue strength Age SMI MNA-SF Barthel Index FOIS
Age
SMI
MNA-SF
Barthel Index
1 0.331*** 0.134* 0.207***
1 0.334*** 0.277***
1 0.288***
1 0.176** 0.287*** 0.380*** 0.277*** 0.393***
1 0.133* 0.272*** 0.286*** 0.080
Coefficients of correlation were calculated with Pearson’s correlation coefficient. SMI: Skeletal Muscle Mass Index; MNA-SF: Mini Nutritional Assessment-Short Form; FOIS: Functional Oral Intake Scale. * p-Value < 0.1. ** p-Value < 0.05. *** p-Value < 0.01.
3. Results
4. Discussion
The final number of participants in the cross-sectional study was 178 (103 men, mean age: 79.12 6.73 years; 75 women, mean age: 79.88 7.82 years). Twenty-six patients (79.4 7.2 years) were excluded for having a progressive neuromuscular disease that caused dysphagia in follow-up study. A further 13 patients (80.2 9.4 years) discontinued outpatient visits based on personal wishes and could not participate. Twenty-nine patients (78.4 7.8 years) were excluded because of missing data. For the follow-up study, one-hundred patients (63 men, mean age: 79.4 6.8 years; 37 women, mean age: 80.0 7.0 years) were enrolled. Twelve patients (mean age: 81.4 6.7 years) were withdrawn during follow-up period due to hospitalization or death. Finaly in the follow-up study it was 88 (55 men, mean age: 79.35 6.81 years; 33 women, mean age: 79.39 7.15 years). (Fig. 1). There were no significant differences in these subjects’ age, tongue strength, SMI, eating function level, or MNA-SF score at the time of initial registration. However, Barthel Index scores differed significantly (p < 0.01). The characteristics of the subjects in the cross-sectional study and the follow-up study are shown in Table 1. Table 2 shows the relationship between each measurement item in the cross-sectional study. In addition, tongue strength was significantly associated with SMI, MNA-SF score, and eating and swallowing level (Table 3). SMI was significantly associated with tongue strength, MNA-SF score, eating and swallowing level, and sex (Table 4). In the follow-up study, after one year of rehabilitation, tongue strength and SMI were significantly increased compared to the start of intervention (Table 5). The factors that were significantly associated with the amount of increase in tongue strength after a year were initial tongue strength and initial SMI (Table 6). The patients maintaining SMI had significantly increased tongue muscle strength compared to those who had decreased SMI (maintaining SMI patients: 6.85 7.64 kPa, low SMI patients: 4.07 5.07 kPa, p < 0.05).
In the present study, the tongue strength was associated with skeletal muscle mass, nutritional status, and eating function. Tamura et al. [18] found that tongue thicknesswas associated with skeletal muscle mass. Similarly, Furuya et al. [19] reported tongue muscle mass and tongue strength by ultrasound and found both to be strongly correlated with skeletal muscle mass and the effect of aging was particularly strong in men. Maeda et al. [20] found that decreased tongue strength is associated with the presence or absence of sarcopenia, including a decrease in skeletal muscle mass. The present association between tongue strength and skeletal muscle mass therefore supports past findings. Meanwhile, the present study also showed an association between tongue strength and level of eating function shown by FOIS, and poorer eating function was associated with lower tongue strength. Tongue strength and nutritional status were also correlated. Buehring found that the tongue strength of inpatients at a sub-acute care hospital was correlated with nutritional status [21]. Moreover, a study by Sakai et al. [22] also showed that lip pressure and tongue strength are correlated with nutritional status. These studies
Table 3. Multiple regression analysis values with the tongue strength and the dependent variables.
Sex Age SMI MNA-SF Barthel Index FOIS
β
Standard error
95% Confidence interval of β
p Value
1.295 0.069 1.701 0.631 0.037 1.851
1.615 0.088 0.844 0.255 0.030 0.501
1.929 0.242 0.035 0.127 0.022 0.861
0.437 0.432 0.045 0.014 0.222 <0.001
4.447 0.104 3.366 1.135 0.096 2.841
Each variable was adjusted for age and sex (0, female; 1, male). SMI: Skeletal Muscle Mass Index; MNA-SF: Mini Nutritional Assessment-Short Form; FOIS: Functional Oral Intake Scale.
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Table 4. Multiple regression analysis values with the SMI and the dependent variables.
Sex Age Tongue strength MNA-SF Barthel Index FOIS
β
Standard error
95% Confidence interval of β
1.262 0.002 0.014 0.106 0.001 0.095
0.108 0.008 0.007 0.022 0.003 0.046
1.475 0.013 0.000 0.062 0.004 0.004
p Value <0.001 0.782 0.045 <0.001 0.741 0.040
1.048 0.018 0.027 0.149 0.006 0.186
Each variable was adjusted for age and sex (0, female; 1, male). SMI: Skeletal Muscle Mass Index; MNA-SF: Mini Nutritional Assessment-Short Form; FOIS: Functional Oral Intake Scale.
Table 5. Comparison between baseline and after a year.
Tongue strength, KPa, mean SD SMI, mean SD
Baseline
After a year
p Value
21.22 9.42 5.99 1.01
26.17 9.68 6.06 1.06
<0.001 0.04
SD: standard deviation; SMI: Skeletal Muscle Mass Index.
suggest that maintenance of both skeletal muscle mass and nutritional status is important for maintaining tongue strength, which is strongly associated with eating and swallowing function. In the present study, tongue strength increased significantly, as did skeletal muscle mass following dysphagia rehabilitation. Robbins [23] found that resistance training may increase tongue strength and improve eating and swallowing function. However, Wakabayashi et al. [24] tested the effects of resistance training in a randomized interventional study in elderly living in the community in the maintenance phase and found no improvement in tongue strength. One of the reasons for the lack of improvement is the poor adherence to training. Compared to the convalescent phase, we commonly see that the effects of rehabilitation are limited in the maintenance phase. While it is inevitable that the function declines with age, it is said that maintenance of functions is an important outcome in rehabilitation for older adults in the maintenance phase, even if there is no improvement in the function [25]. In the present study, it is of great significance that tongue strength improved and skeletal muscle mass increased following dysphagia rehabilitation. In this study, we were unable to measure adherence to training, so we could not consider this effect. On the other hand, it is known that combining the two with oral function training alone or nutrition instruction alone is more effective [26]. The fact that this intervention was comprehensive
swallowing function training including nutritional counseling may have worked effectively on the results of this study. As effects of one year of dysphagia rehabilitation, tongue strength and skeletal muscle mass increased significantly. In particular, tongue strength improved more notably in subjects who were maintaining skeletal muscle mass at the time of intervention. Maeda and Akagi found [1] that the reduction in skeletal muscle mass may be a risk factor for development of dysphagia and stressed the importance of nutritional management and rehabilitation before hospital admission. Maeda et al. also conducted a follow-up study of inpatients hospitalized for pneumonia and found that lower skeletal muscle mass was a predictor of mortality [20]. These reports indicate that whole-body sarcopenia causes dysphagia and worsens dysphagia. Prevention of sarcopenia, that is, maintenance of skeletal muscle mass, is important to enhance the effects of swallowing function training that includes improving tongue strength. For that reason, when starting rehabilitation, it is important to measure skeletal muscle mass to know the presence or absence of sarcopenia. In addition, it may be necessary to implement a program to improve sarcopenia. Nutritional supplements and resistance training are effective in increasing skeletal muscle mass [27]. In addition to resistance training for tongue strength, adding resistance training for the whole body and nutritional supplements may help boost tongue strength. This study has limitations. The first limitation of the present study is that the method of intervention was a comprehensive method and the degree of the subject’s adherence to the resistance training instruction is unknown. Similarly, since nutritional counseling was tailored for each individual’s nutritional status and level of competence in daily activities, there was large variance in actual nutritional intake. This problem makes it difficult to
Table 6. The relationships between the change of the tongue strength and the other factors in the follow-up study. (1) Correlation matrix table. (2) Multiple regression analysis values with the change of the tongue strength and the dependent variables. Change of the tongue strength Change of the tongue strength Age SMI MNA-SF Barthel Index Tongue strength FOIS
Sex Age SMI Tongue strength
Age
SMI
MNA-SF
Barthel Index
Tongue strength
1 0.267** 0240** 0.242** 0.168
1 0.314*** 0.400*** 0.149
1 0.356*** 0.340***
1 0.358***
1 0.044 0.189* 0.049 0.095 0.285*** 0.005
1 0.168 0.216** 0.240** 0.214** 0.085
β
Standard error
95% Confidence interval of β
1.471 0.063 2.112 0.258
1.788 0.092 0.887 0.073
2.085 0.246 0.348 0.403
p Value 5.027 0.120 3.875 0.113
0.413 0.497 0.020 0.001
Coefficients of correlation were calculated with Pearson’s correlation coefficient. SMI: Skeletal Muscle Mass Index; MNA-SF: Mini Nutritional Assessment-Short Form; FOIS: Functional Oral Intake Scale. Each variable was adjusted for age and sex (0, female; 1, male). SMI: Skeletal Muscle Mass Index; MNA-SF: Mini Nutritional Assessment-Short Form; FOIS: Functional Oral Intake Scale. * p-Value < 0.1. ** p-Value < 0.05. *** p-Value < 0.01.
Please cite this article in press as: Y. Nakazawa, et al., Associations between tongue strength and skeletal muscle mass under dysphagia rehabilitation for geriatric out patients, J Prosthodont Res (2019), https://doi.org/10.1016/j.jpor.2019.07.004
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investigate which aspects of nutrition affect the increase in tongue strength and skeletal muscle mass that were observed in the present study. The second limitation was that there were many more dropouts in the follow-up study than in the cross-sectional study. The possibility cannot be dismissed that only those with a good prognosis who showed good effects from the rehabilitation participated in the follow-up study. In the present study, in which elderly outpatients participated, the large number of dropouts may be permissible. Moreover, as shown in the results, aside from the ADL indicator, there were no significant differences in initial tongue strength, skeletal muscle mass, or nutritional status data among those with a poor prognosis requiring counseling or hospitalization, those who ceased visiting the clinic, and those who actually participated in the follow-up study. The possibility of effects of the intervention cannot be dismissed. 5. Conclusion For patients with dysphagia, maintaining skeletal muscle mass has a positive impact on the increase in tongue strength obtained by rehabilitation. This indicates that prevention of sarcopenia in dysphagia patients contributes to the effect of rehabilitation. The results of this study provided one guide in rehabilitation for patients with dysphagia in sarcopenia. Conflict of interest There is no conflict of interest regarding the publication of the study results. References [1] Maeda K, Akagi J. Sarcopenia is an independent risk factor of dysphagia in hospitalized older people. Geriatr Gerontol Int 2016;515–21. [2] Wakabayashi H, Sashika H. Malnutrition is associated with poor rehabilitation outcome in elderly inpatients with hospital-associated deconditioning a prospective cohort study. J Rehabil Med 2014;277–82. [3] Kuroda Y, Kuroda R. Relationship between thinness and swallowing function in Japanese older adults: implications for sarcopenic dysphagia. J Am Geriatr Soc 2012;1785–6. [4] Wakabayashi H, Matsushima M, Uwano R, Watanabe N, Oritsu H, Shimizu Y. Skeletal muscle mass is associated with severe dysphagia in cancer patients. J Cachexia Sarcopenia Muscle 2015;351–7. [5] Wakabayashi H, Takahashi R, Watanabe N, Oritsu H, Shimizu Y. Prevalence of skeletal muscle mass loss and its association with swallowing function after cardiovascular surgery. Nutrition 2017;70–3. [6] Takagi D, Hirano H, Watanabe Y, Edahiro A, Ohara Y, Yoshida H, et al. Relationship between skeletal muscle mass and swallowing function in patients with Alzheimer’s disease. Geriatr Gerontol Int 2017;402–9.
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[7] 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;286–90. [8] Yoshida M, Kikutani T, Tsuga K, Utanohara Y, Hayashi R, Akagawa Y. Decreased tongue pressure reflects symptom of dysphagia. Dysphagia 2006;61–5. [9] 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 2016e0165837. [10] Maeda K, Akagi J. Decreased tongue pressure is associated with sarcopenia and sarcopenic dysphagia in the elderly. Dysphagia 2015;80–7. [11] Rabadi MH, Coar PL, Lukin M, Lesser M, Blass JP. Intensive nutritional supplements can improve outcomes in stroke rehabilitation. Neurology 2008;1856–61. [12] Crary MA, Mann GD, Groher ME. Initial psychometric assessment of a functional oral intake scale for dysphagia in stroke patients. Arch Phys Med Rehabil 2005;1516–20. [13] 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;e1078–85. [14] Kaiser MJ, Bauer JM, Ramsch C, Uter W, Guigoz Y, Cederholm T, et al. Validation of the Mini Nutritional Assessment Short-Form (MNA-SF): a practical tool for identification of nutritional status. J Nutr Health Aging 2009;782–8. [15] Mahoney FI, Barthel DW. Functional evaluation: the Barthel index. Md State Med J 1965;61–5. [16] Baumgartner RN, Koehler KM, Gallagher D, Romero L, Heymsfield SB, Ross RR, et al. Epidemiology of sarcopenia among the elderly in New Mexico. Am J Epidemiol 1998;755–63. [17] Chen LK, Liu LK, Woo J, Assantachai P, Auyeung TW, Bahyah KS, et al. Sarcopenia in Asia: consensus report of the Asian working group for sarcopenia. J Am Med Dir Assoc 2014;95–101. [18] Tamura F, Kikutani T, Tohara T, Yoshida M, Yaegaki K. Tongue thickness relates to nutritional status in the elderly. Dysphagia 2012;556–61. [19] Furuya H, Tamura F, Yoshida M, Hirano H, Iijima K, Kikutani T. Tongue muscle mass and strength relate to whole-body muscle in the community-dwelling elderly. J Jpn Assoc Oral Rehabil 2016;1–9. [20] Maeda K, Takaki M, Akagi J. Decreased skeletal muscle mass and risk factors of sarcopenic dysphagia: a prospective observational cohort study. J Gerontol A Biol Sci Med Sci 2017;1290–4. [21] Buehring B, Hind J, Fidler E, Krueger D, Binkley N, Robbins J. Tongue strength is associated with jumping mechanography performance and handgrip strength but not with classic functional tests in older adults. J Am Geriatr Soc 2013;418–22. [22] Sakai K, Nakayama E, Tohara H, Takahashi O, Ohnishi S, Tsuzuki H, et al. Diagnostic accuracy of lip force and tongue strength for sarcopenic dysphagia in older inpatients: a cross-sectional observational study. Clin Nutr 2019;303–9. [23] Robbins J. New frontiers in dysphagia rehabilitation. Semin Speech Lang 2006;217–8. [24] Wakabayashi H, Matsushima M, Momosaki R, Yoshida S, Mutai R, Yodoshi T, et al. The effects of resistance training of swallowing muscles on dysphagia in older people: a cluster, randomized, controlled trial. Nutrition 2018;111–6. [25] World Health Organization. Rehabilitation in health systems. Geneva: WHO; 2017 Rehabilitation in health systems. https://www.who.int/disabilities/ rehabilitation_health_systems/en/. 2018. [Accessed 27 June 2018]. [26] Kikutani T, Enomoto R, Tamura F, Oyaizu K, Suzuki A, Inaba S. Effects of oral functional training for nutritional improvement in Japanese older people requiring long-term care. Gerodontology 2006;93–8. [27] Yamada M, Arai H, Yoshimura K, Kajiwara Y, Sonoda T, Nishiguchi S, et al. Nutritional supplementation during resistance training improved skeletal muscle mass in community-dwelling frail older adults. J Frailty Aging 2012;64–70.
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Original article
Associations between tongue strength and skeletal muscle mass under dysphagia rehabilitation for geriatric out patients Yujiro Nakazawaa , Takeshi Kikutania,b,* , Kumi Igarashia , Yuri Yajimab , Fumiyo Tamurab a
Division of Clinical Oral Rehabilitation, The Nippon Dental University, Graduate School of Life Dentistry, 1-9-20, Fujimi, Chiyoda, Tokyo 102-0071, Japan Division of Rehabilitation for Speech and Swallowing Disorders, The Nippon Dental University, Tama Oral Rehabilitation Clinic, 4-44-19, Koganei, Tokyo 1840011, Japan b
A R T I C L E I N F O
A B S T R A C T
Article history: Received 18 August 2018 Received in revised form 5 July 2019 Accepted 9 July 2019 Available online xxx
Purpose: The purpose of this study was to examine how skeletal muscle mass influences the effectiveness of dysphagia rehabilitation. Methods: The cross-sectional study and the prospective cohort study were conducted in a clinic, specialized in rehabilitation of patients with dysphagia, located in Tokyo, Japan. Skeletal muscle mass measurement by bioelectrical impedance analysis and tongue strength measurement were performed on 178 outpatients with dysphagia. In addition, the Barthel Index, Mini Nutritional Assessment-Short Form, and Functional Oral Intake Scale values were measured. Dysphagia rehabilitation was performed, and 88 of the patients who were available for follow-up one year later were included in a follow-up study. In the cross-sectional study, the associations between tongue strength and other factors were examined. In the follow-up study, factors associated with rehabilitation effectiveness, shown by tongue strength, were examined. Results: Tongue strength and skeletal muscle mass were correlated, and both decreased as eating and swallowing function level decreased. After one year of dysphagia rehabilitation, tongue strength and skeletal muscle mass increased. The factors associated with the amount of increase in tongue strength were initial tongue strength and skeletal muscle mass. Conclusions: For patients with dysphagia, maintenance of skeletal muscle mass was associated with improvement of tongue strength in rehabilitation. This indicates that prevention of sarcopenia in dysphagia patients contributes to the effect of rehabilitation. © 2019 Japan Prosthodontic Society. Published by Elsevier Ltd. All rights reserved.
Keywords: Tongue strength Skeletal muscle mass Dysphagia Rehabilitation Sarcopenia
1. Introduction Patients with dysphagia are known to have low energy intake and protein levels and fall into malnutrition [1]. Swallowing muscles are not an exception; muscle strength in the muscles related to swallowing has also been shown to decrease with malnutrition [2]. Kuroda and Kuroda [3] demonstrated that there is a relationship between eating and swallowing function and upper arm circumference in older inpatients with dysphagia. The cause of this may be related to a decrease in lean body mass that includes swallowing muscles, and the presence of dysphagia due to sarcopenia was suggested. Associations between dysphagia and a decrease in whole body muscle mass or the presence of
* Corresponding author at: Division of Rehabilitation for Speech and Swallowing Disorders, The Nippon Dental University, Tama Oral Rehabilitation Clinic, 4-44-19, Koganei, Tokyo 184-0011, Japan. E-mail address: [email protected] (T. Kikutani).
sarcopenia have been observed in patients with cancer [4], after surgery for major cardiovascular diseases [5], and with Alzheimer’s disease [6]. Tongue strength, which is often used as an indicator of the muscles related to swallowing, decreases with aging [7]. Moreover, tongue strength has been shown to be lower in people with dysphagia than those without [8], and a study of inpatients showed an association between tongue strength and the development of pneumonia [9]. These findings suggest that there is a strong relationship between tongue strength and eating and swallowing function. Maeda and Akagi measured tongue strength in 104 inpatients without a history of cerebrovascular diseases or neurodegenerative diseases, and they reported that a decrease in tongue strength was associated with the presence or absence of sarcopenia and dysphagia from sarcopenia [10]. Many studies have shown that grip and other forms of muscle strength are closely associated with nutritional status and skeletal muscle mass. Meanwhile, eating and swallowing function can be divided into several different levels, such as complete inability to take food orally, partial oral intake
https://doi.org/10.1016/j.jpor.2019.07.004 1883-1958/ © 2019 Japan Prosthodontic Society. Published by Elsevier Ltd. All rights reserved.
Please cite this article in press as: Y. Nakazawa, et al., Associations between tongue strength and skeletal muscle mass under dysphagia rehabilitation for geriatric out patients, J Prosthodont Res (2019), https://doi.org/10.1016/j.jpor.2019.07.004
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ability, or ability to take food orally by meal modification. However, no studies have fully examined the associations between tongue strength and eating and swallowing function, level of eating and swallowing function, physical functioning, and skeletal muscle mass. Moreover, many studies have supported the importance of maintaining eating and swallowing function to prevent malnutrition and pneumonia in older adults. Many studies have verified the importance of resistance training for improving eating and swallowing function, and the effectiveness of resistance training has been said to be stronger in people with a better nutritional status [11]. Studies have shown that poorer nutritional status or low skeletal muscle mass have more difficulty conducting activities of daily living (ADL) after rehabilitation [2]. However, what effects maintenance of nutritional status and skeletal muscle mass for improvement of eating and swallowing function have on rehabilitation remain unclear. In this study, we carried out based on the hypothesis that maintaining skeletal muscle affects the prognosis of dysphagia rehabilitation. 2. Materials and methods 2.1. Design and patient sample 2.1.1. Cross-sectional study A total of 588 of the 4441 outpatients who were examined at the Nippon Dental University Oral Rehabilitation Tama Clinic during the period from April 2014 to March 2017, excluding 1276 patients who were under 65 years of age and 2577 home care patients, were evaluated. Excluding patients who did not have dysphagia as a chief complaint, patients with oral cancer who had undergone an extensive glossectomy, and patients who could not have their tongue strength measured due to reduced cognitive functioning, one-hundred seventy-eight patients participated in a cross-sectional study. Patients with neuromuscular disease were excluded for follow-up studies. Furthermore, we excluded those who had data loss and those who came to the hospital only to evaluate their swallowing function. One hundred people were enrolled as followup study. At the start of the intervention, eating and swallowing function tests including videofluorography were performed on each participant. Tongue strength related to feeding swallowing function and skeletal muscle mass associated with sarcopenia were
examined. Based on those results, resistance training was performed to improve tongue strength, and comprehensive swallowing function training was performed according to each individual’s functioning level. In resistance training, we instructed the training to be performed twice a day for a total of 30 times with the goal of applying about 80% resistance, referring to the pressure of each person’s tongue. Depending on their nutritional status, the patients were given nutritional counseling from a registered dietitian. Of those who were available for follow-up one year later, 88 patients were included in a follow-up study (Fig.1) 2.2. Instrument Oral intake status was assessed with the Functional Oral Intake Scale (FOIS) [12]. Tongue strength was measured with the JMS tongue strength measurement device (JM-TPM; JMS Co., Ltd., Hiroshima, Japan) three times [13], and the average was used for the analysis. Nutritional status was assessed with the Mini Nutritional Assessment-Short Form (MNA-SF) [14]. ADL were measured using the Barthel Index [15], which is a basic ADL scale. For skeletal muscle mass, the InBody S10 (Inbody, Seoul, Korea) was used to take measurements, and the skeletal muscle mass index (SMI) was calculated [16]. The cut-off values for SMI to define sarcopenia for men and women were <7.0 kg/m2 and <5.7 kg/m2, respectively [17]. 2.3. Analysis Spearman’s rank correlation coefficients were used to examine the associations between tongue strength, SMI, and other factors. Factors with a probability of less than 10% on univariate analysis were set as independent variables, and the multiple regression analysis was performed. SPSS statistics 24 software (IBM, Tokyo, Japan) was used for all statistical analyses. The t-test was used to examine the comparison on between baseline and after year. The level of statistical significance was set at p < 0.05. 2.4. Ethics This study was conducted in compliance with the Declaration of Helsinki, after obtaining proper informed consent from each subject or his/her legal representatives, such as family members.
Outpatients n=4441 ・Under 65 years of age: n=1276 ・Home care patient: n=2577 n=588
Participants (cross-sectional study)
・No dysphagic complaint, Oral cancer, Dementia: n=410
n=178
Participants
・Neuromuscular disease: n=26
(enllored as follow-up study)
・Only evaluation: n=13
n=100
・Data missing: n=39
Fainal participants (follow-up study)
・Drop out due to hospitalization or death : n=12
n=88 Fig. 1. Study flowchart describing the exclusion of participants in the study.
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Table 1. The characteristics of the subjects. Cross-sectional study (at the baseline)
Follow-up study (at the after a year)
Characteristic
Over all, n = 178
Men, n = 103
Women, n = 75
Over all, n = 88
Men, n = 55
Women, n = 33
Age, mean SD SMI, mean SD MNA-SF, mean SD Barthel Index, mean SD Tongue strength, KPa, mean SD FOIS Level 1, n(%) Level 2, n(%) Level 3, n(%) Level 4, n(%) Level 5, n(%) Level 6, n(%) Level 7, n(%)
79.44 7.20 5.98 1.00 9.75 2.78 83.68 22.00 21.01 9.03 5 (2.81) 5 (2.81) 2 (1.12) 44 (24.72) 41 (23.03) 69 (38.76) 12 (6.74)
79.12 6.73 6.49 0.09 9.58 3.06 82.23 21.59 21.04 9.66 4 (3.9) 3 (2.9) 2 (1.9) 26 (25.2) 22 (21.4) 40 (38.8) 6 (5.8)
79.88 7.82 5.29 0.72 9.97 2.34 85.67 22.55 20.96 8.13 1 (1.3) 2 (2.7) 0 (0) 18 (24.0) 19 (25.3) 29 (38.7) 6 (8.0)
79.36 6.90 5.99 1.01 9.91 2.66 84.94 20.40 21.22 9.42 2 (2.27) 2 (2.27) 0 (0) 22 (25) 23 (26.14) 38 (43.18) 1 (1.14)
79.35 6.81 6.50 0.82 9.82 2.87 85.09 19.16 20.36 10.49 2 (3.6) 1 (1.8) 0 (0) 13 (23.6) 15 (27.3) 24 (43.6) 0 (0)
79.39 7.15 5.15 0.69 10.06 2.30 84.70 22.64 22.66 7.23 0 (0) 1 (3.0) 0 (0) 9 (27.3) 8 (24.2) 14 (42.4) 1 (3.0)
SD: standard deviation; SMI: Skeletal Muscle Mass Index; MNA-SF: Mini Nutritional Assessment-Short Form; FOIS: Functional Oral Intake Scale.
Table 2. The relationships between the measurements in the cross-sectional study (correlation matrix table). Tongue strength Tongue strength Age SMI MNA-SF Barthel Index FOIS
Age
SMI
MNA-SF
Barthel Index
1 0.331*** 0.134* 0.207***
1 0.334*** 0.277***
1 0.288***
1 0.176** 0.287*** 0.380*** 0.277*** 0.393***
1 0.133* 0.272*** 0.286*** 0.080
Coefficients of correlation were calculated with Pearson’s correlation coefficient. SMI: Skeletal Muscle Mass Index; MNA-SF: Mini Nutritional Assessment-Short Form; FOIS: Functional Oral Intake Scale. * p-Value < 0.1. ** p-Value < 0.05. *** p-Value < 0.01.
3. Results
4. Discussion
The final number of participants in the cross-sectional study was 178 (103 men, mean age: 79.12 6.73 years; 75 women, mean age: 79.88 7.82 years). Twenty-six patients (79.4 7.2 years) were excluded for having a progressive neuromuscular disease that caused dysphagia in follow-up study. A further 13 patients (80.2 9.4 years) discontinued outpatient visits based on personal wishes and could not participate. Twenty-nine patients (78.4 7.8 years) were excluded because of missing data. For the follow-up study, one-hundred patients (63 men, mean age: 79.4 6.8 years; 37 women, mean age: 80.0 7.0 years) were enrolled. Twelve patients (mean age: 81.4 6.7 years) were withdrawn during follow-up period due to hospitalization or death. Finaly in the follow-up study it was 88 (55 men, mean age: 79.35 6.81 years; 33 women, mean age: 79.39 7.15 years). (Fig. 1). There were no significant differences in these subjects’ age, tongue strength, SMI, eating function level, or MNA-SF score at the time of initial registration. However, Barthel Index scores differed significantly (p < 0.01). The characteristics of the subjects in the cross-sectional study and the follow-up study are shown in Table 1. Table 2 shows the relationship between each measurement item in the cross-sectional study. In addition, tongue strength was significantly associated with SMI, MNA-SF score, and eating and swallowing level (Table 3). SMI was significantly associated with tongue strength, MNA-SF score, eating and swallowing level, and sex (Table 4). In the follow-up study, after one year of rehabilitation, tongue strength and SMI were significantly increased compared to the start of intervention (Table 5). The factors that were significantly associated with the amount of increase in tongue strength after a year were initial tongue strength and initial SMI (Table 6). The patients maintaining SMI had significantly increased tongue muscle strength compared to those who had decreased SMI (maintaining SMI patients: 6.85 7.64 kPa, low SMI patients: 4.07 5.07 kPa, p < 0.05).
In the present study, the tongue strength was associated with skeletal muscle mass, nutritional status, and eating function. Tamura et al. [18] found that tongue thicknesswas associated with skeletal muscle mass. Similarly, Furuya et al. [19] reported tongue muscle mass and tongue strength by ultrasound and found both to be strongly correlated with skeletal muscle mass and the effect of aging was particularly strong in men. Maeda et al. [20] found that decreased tongue strength is associated with the presence or absence of sarcopenia, including a decrease in skeletal muscle mass. The present association between tongue strength and skeletal muscle mass therefore supports past findings. Meanwhile, the present study also showed an association between tongue strength and level of eating function shown by FOIS, and poorer eating function was associated with lower tongue strength. Tongue strength and nutritional status were also correlated. Buehring found that the tongue strength of inpatients at a sub-acute care hospital was correlated with nutritional status [21]. Moreover, a study by Sakai et al. [22] also showed that lip pressure and tongue strength are correlated with nutritional status. These studies
Table 3. Multiple regression analysis values with the tongue strength and the dependent variables.
Sex Age SMI MNA-SF Barthel Index FOIS
β
Standard error
95% Confidence interval of β
p Value
1.295 0.069 1.701 0.631 0.037 1.851
1.615 0.088 0.844 0.255 0.030 0.501
1.929 0.242 0.035 0.127 0.022 0.861
0.437 0.432 0.045 0.014 0.222 <0.001
4.447 0.104 3.366 1.135 0.096 2.841
Each variable was adjusted for age and sex (0, female; 1, male). SMI: Skeletal Muscle Mass Index; MNA-SF: Mini Nutritional Assessment-Short Form; FOIS: Functional Oral Intake Scale.
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Table 4. Multiple regression analysis values with the SMI and the dependent variables.
Sex Age Tongue strength MNA-SF Barthel Index FOIS
β
Standard error
95% Confidence interval of β
1.262 0.002 0.014 0.106 0.001 0.095
0.108 0.008 0.007 0.022 0.003 0.046
1.475 0.013 0.000 0.062 0.004 0.004
p Value <0.001 0.782 0.045 <0.001 0.741 0.040
1.048 0.018 0.027 0.149 0.006 0.186
Each variable was adjusted for age and sex (0, female; 1, male). SMI: Skeletal Muscle Mass Index; MNA-SF: Mini Nutritional Assessment-Short Form; FOIS: Functional Oral Intake Scale.
Table 5. Comparison between baseline and after a year.
Tongue strength, KPa, mean SD SMI, mean SD
Baseline
After a year
p Value
21.22 9.42 5.99 1.01
26.17 9.68 6.06 1.06
<0.001 0.04
SD: standard deviation; SMI: Skeletal Muscle Mass Index.
suggest that maintenance of both skeletal muscle mass and nutritional status is important for maintaining tongue strength, which is strongly associated with eating and swallowing function. In the present study, tongue strength increased significantly, as did skeletal muscle mass following dysphagia rehabilitation. Robbins [23] found that resistance training may increase tongue strength and improve eating and swallowing function. However, Wakabayashi et al. [24] tested the effects of resistance training in a randomized interventional study in elderly living in the community in the maintenance phase and found no improvement in tongue strength. One of the reasons for the lack of improvement is the poor adherence to training. Compared to the convalescent phase, we commonly see that the effects of rehabilitation are limited in the maintenance phase. While it is inevitable that the function declines with age, it is said that maintenance of functions is an important outcome in rehabilitation for older adults in the maintenance phase, even if there is no improvement in the function [25]. In the present study, it is of great significance that tongue strength improved and skeletal muscle mass increased following dysphagia rehabilitation. In this study, we were unable to measure adherence to training, so we could not consider this effect. On the other hand, it is known that combining the two with oral function training alone or nutrition instruction alone is more effective [26]. The fact that this intervention was comprehensive
swallowing function training including nutritional counseling may have worked effectively on the results of this study. As effects of one year of dysphagia rehabilitation, tongue strength and skeletal muscle mass increased significantly. In particular, tongue strength improved more notably in subjects who were maintaining skeletal muscle mass at the time of intervention. Maeda and Akagi found [1] that the reduction in skeletal muscle mass may be a risk factor for development of dysphagia and stressed the importance of nutritional management and rehabilitation before hospital admission. Maeda et al. also conducted a follow-up study of inpatients hospitalized for pneumonia and found that lower skeletal muscle mass was a predictor of mortality [20]. These reports indicate that whole-body sarcopenia causes dysphagia and worsens dysphagia. Prevention of sarcopenia, that is, maintenance of skeletal muscle mass, is important to enhance the effects of swallowing function training that includes improving tongue strength. For that reason, when starting rehabilitation, it is important to measure skeletal muscle mass to know the presence or absence of sarcopenia. In addition, it may be necessary to implement a program to improve sarcopenia. Nutritional supplements and resistance training are effective in increasing skeletal muscle mass [27]. In addition to resistance training for tongue strength, adding resistance training for the whole body and nutritional supplements may help boost tongue strength. This study has limitations. The first limitation of the present study is that the method of intervention was a comprehensive method and the degree of the subject’s adherence to the resistance training instruction is unknown. Similarly, since nutritional counseling was tailored for each individual’s nutritional status and level of competence in daily activities, there was large variance in actual nutritional intake. This problem makes it difficult to
Table 6. The relationships between the change of the tongue strength and the other factors in the follow-up study. (1) Correlation matrix table. (2) Multiple regression analysis values with the change of the tongue strength and the dependent variables. Change of the tongue strength Change of the tongue strength Age SMI MNA-SF Barthel Index Tongue strength FOIS
Sex Age SMI Tongue strength
Age
SMI
MNA-SF
Barthel Index
Tongue strength
1 0.267** 0240** 0.242** 0.168
1 0.314*** 0.400*** 0.149
1 0.356*** 0.340***
1 0.358***
1 0.044 0.189* 0.049 0.095 0.285*** 0.005
1 0.168 0.216** 0.240** 0.214** 0.085
β
Standard error
95% Confidence interval of β
1.471 0.063 2.112 0.258
1.788 0.092 0.887 0.073
2.085 0.246 0.348 0.403
p Value 5.027 0.120 3.875 0.113
0.413 0.497 0.020 0.001
Coefficients of correlation were calculated with Pearson’s correlation coefficient. SMI: Skeletal Muscle Mass Index; MNA-SF: Mini Nutritional Assessment-Short Form; FOIS: Functional Oral Intake Scale. Each variable was adjusted for age and sex (0, female; 1, male). SMI: Skeletal Muscle Mass Index; MNA-SF: Mini Nutritional Assessment-Short Form; FOIS: Functional Oral Intake Scale. * p-Value < 0.1. ** p-Value < 0.05. *** p-Value < 0.01.
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investigate which aspects of nutrition affect the increase in tongue strength and skeletal muscle mass that were observed in the present study. The second limitation was that there were many more dropouts in the follow-up study than in the cross-sectional study. The possibility cannot be dismissed that only those with a good prognosis who showed good effects from the rehabilitation participated in the follow-up study. In the present study, in which elderly outpatients participated, the large number of dropouts may be permissible. Moreover, as shown in the results, aside from the ADL indicator, there were no significant differences in initial tongue strength, skeletal muscle mass, or nutritional status data among those with a poor prognosis requiring counseling or hospitalization, those who ceased visiting the clinic, and those who actually participated in the follow-up study. The possibility of effects of the intervention cannot be dismissed. 5. Conclusion For patients with dysphagia, maintaining skeletal muscle mass has a positive impact on the increase in tongue strength obtained by rehabilitation. This indicates that prevention of sarcopenia in dysphagia patients contributes to the effect of rehabilitation. The results of this study provided one guide in rehabilitation for patients with dysphagia in sarcopenia. Conflict of interest There is no conflict of interest regarding the publication of the study results. References [1] Maeda K, Akagi J. Sarcopenia is an independent risk factor of dysphagia in hospitalized older people. Geriatr Gerontol Int 2016;515–21. [2] Wakabayashi H, Sashika H. Malnutrition is associated with poor rehabilitation outcome in elderly inpatients with hospital-associated deconditioning a prospective cohort study. J Rehabil Med 2014;277–82. [3] Kuroda Y, Kuroda R. Relationship between thinness and swallowing function in Japanese older adults: implications for sarcopenic dysphagia. J Am Geriatr Soc 2012;1785–6. [4] Wakabayashi H, Matsushima M, Uwano R, Watanabe N, Oritsu H, Shimizu Y. Skeletal muscle mass is associated with severe dysphagia in cancer patients. J Cachexia Sarcopenia Muscle 2015;351–7. [5] Wakabayashi H, Takahashi R, Watanabe N, Oritsu H, Shimizu Y. Prevalence of skeletal muscle mass loss and its association with swallowing function after cardiovascular surgery. Nutrition 2017;70–3. [6] Takagi D, Hirano H, Watanabe Y, Edahiro A, Ohara Y, Yoshida H, et al. Relationship between skeletal muscle mass and swallowing function in patients with Alzheimer’s disease. Geriatr Gerontol Int 2017;402–9.
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Please cite this article in press as: Y. Nakazawa, et al., Associations between tongue strength and skeletal muscle mass under dysphagia rehabilitation for geriatric out patients, J Prosthodont Res (2019), https://doi.org/10.1016/j.jpor.2019.07.004