Next Article in Journal
Noninvasive Ventilation and Rapid Enteral Feeding Advances in Preterm Infants—2-Year Follow-Up of the STENA-Cohort
Next Article in Special Issue
Rehabilitation Nutrition in Older People
Previous Article in Journal
Association between Antibiotic Exposure and Type 2 Diabetes Mellitus in Middle-Aged and Older Adults
Previous Article in Special Issue
Predictive Value of Temporal Muscle Thickness for Sarcopenia after Acute Stroke in Older Patients
 
 
Font Type:
Arial Georgia Verdana
Font Size:
Aa Aa Aa
Line Spacing:
Column Width:
Background:
Article

Effects of Undernutrition on Swallowing Function and Activities of Daily Living in Hospitalized Patients: Data from the Japanese Sarcopenic Dysphagia Database

1
Department of Nutrition, Sapporonishimaruyama Hospital, Sapporo 064-0944, Japan
2
Department of Nutritional Management, Keiju Hatogaoka Integrated Facility for Medical and Long-Term Care, Hosu 927-0023, Japan
3
Department of Geriatric Medicine, Hospital, National Center for Geriatrics and Gerontology, Obu 474-8511, Japan
4
Department of Clinical Nutrition and Food Service, Nagasaki Rehabilitation Hospital, Nagasaki 850-0854, Japan
5
Department of Rehabilitation Medicine, Mie University Graduate School of Medicine, Tsu 514-0001, Japan
6
Department of Rehabilitation, Sapporonishimaruyama Hospital, Sapporo 064-0944, Japan
7
Social Welfare Corporation, Tobetsu Town Council of Social Welfare, Ishikari 064-0234, Japan
8
Department of Rehabilitation Medicine, Tokyo Women’s Medical University Hospital, Tokyo 162-8666, Japan
*
Author to whom correspondence should be addressed.
Nutrients 2023, 15(5), 1291; https://doi.org/10.3390/nu15051291
Submission received: 2 February 2023 / Revised: 27 February 2023 / Accepted: 3 March 2023 / Published: 6 March 2023
(This article belongs to the Special Issue Rehabilitation Nutrition in Older People)

Abstract

:
This retrospective cohort study examined the effects of undernutrition on swallowing function and activities of daily living in hospitalized patients. Data from the Japanese Sarcopenic Dysphagia Database were used, and hospitalized patients aged ≥20 years with dysphagia were included in the analysis. Participants were assigned to the undernutrition or normal nutritional status group based on the Global Leadership Initiative on Malnutrition criteria. The primary outcome was the Food Intake Level Scale change, and the secondary outcome was the Barthel Index change. Among 440 residents, 281 (64%) were classified under the undernutrition group. The undernutrition group had a significantly higher Food Intake Level Scale score at baseline and Food Intake Level Scale change (p = 0.001) than the normal nutritional status group. Undernutrition was independently associated with the Food Intake Level Scale change (B = −0.633, 95% confidence interval = −1.099 to −0.167) and the Barthel Index change (B = −8.414, 95% confidence interval = −13.089 to −3.739). This was defined as the period from the date of admission to the hospital until discharge or 3 months later. Overall, our findings indicate that undernutrition is associated with reduced improvement in swallowing function and the ability to perform activities of daily living.

1. Introduction

Undernutrition is frequent in patients with dysphagia, which results in worse clinical outcomes. Numerous diseases cause dysphagia including cerebrovascular disease (e.g., stroke), neurodegenerative disease (e.g., amyotrophic lateral sclerosis), dementia and head and neck cancer [1]. The prevalence of dysphagia is 11–33% in community-dwelling older adults [2,3], 53% in institutionalized residents [4] and 24–50% in hospitalized patients [5,6]. There are also reports of a high incidence of dysphagia and undernutrition co-occurrence [5,7,8]. Dysphagia patients who are undernourished have longer hospital stays, higher risk of complications [6] and higher mortality rates [9]. Therefore, these patients should be evaluated for undernutrition.
Sarcopenic dysphagia and presbyphagia have recently received attention as causes of dysphagia. Sarcopenic dysphagia is a swallowing disorder caused by sarcopenia of the entire body as well as the swallowing muscle. Low muscle mass, age, undernutrition, lack of independence in daily living and low tongue pressure have recently been identified as risk factors for sarcopenic dysphagia [1]. Since 1992, undernutrition has been recognized as a risk factor for feeding and swallowing difficulties [10]. Undernutrition can reduce overall muscle mass and strength, resulting in a decrease in swallowing-related muscle tone. Undernutrition is caused by starvation, invasion and cachexia, and the dysphagia caused by undernutrition is classified as sarcopenia dysphagia [1]. Furthermore, the concept of presbyphagia refers to age-related sarcopenia of the lingual and supraspinal muscle groups [11]. Hypophagia is not uncommon in patients with presbyphagia owing to decreased muscle mass and function of swallowing-related muscles.
A few studies have assessed patients with dysphagia using the Global Leadership Initiative on Malnutrition (GLIM) criteria, which is a diagnostic method for evaluating undernutrition proposed by several global societies [12]. The GLIM criteria involve the assessment of muscle mass, body mass index and disease effects. Hence, it can be used for the nutritional assessment of adults with dysphagia [13]. However, a survey on nutritional assessment methods among patients admitted to internal medicine departments has found that only 20% of studies used the GLIM criteria [14]. In previous studies, 90% of patients with dysphagia who were admitted to a rehabilitation hospital presented with undernutrition diagnosed using the GLIM criteria [15,16]. In addition, severe undernutrition according to the same criteria was found to be associated with poor improvement in dysphagia [15]. However, previous studies only included patients with sarcopenic dysphagia. Therefore, whether undernutrition diagnosed using the GLIM criteria is a useful prognostic indicator of swallowing and physical function in patients with dysphagia should be examined.
The current study aimed to examine the effects of undernutrition diagnosed by the GLIM criteria on activities of daily living and swallowing function in hospitalized patients with dysphagia.

2. Materials and Methods

2.1. Study Design and Participants

This was a retrospective cohort study. Patients from the Japanese Sarcopenia Dysphagia Database, which was jointly established by the Rehabilitation Nutrition Database Committee of the Japanese Association of Rehabilitation Nutrition and the Japanese Working Group on Sarcopenic Dysphagia, were enrolled in this study [17]. Although whole-body sarcopenia and malnutrition are known risk factors for the development of sarcopenic dysphagia, other risk factors and associated factors remain unknown. Therefore, we created the Japanese Sarcopenic Dysphagia Database, which can be used by many hospitals to collect more information on sarcopenic dysphagia. The Japanese Association of Rehabilitation Nutrition and the Japanese Working Group on Sarcopenic Dysphagia recruited participating facilities. To ensure data accuracy, the REDCap data input manual was distributed to all data entry personnel at the participating facilities. The timing of baseline data entry was at admission. At the baseline and follow-up, entry personnel recorded the patients’ data. The timing of outcome measurement was at discharge or 3 months later. At the follow-up visit, the outcome was classified as discharge to home, transfer to other hospitals/facilities, continuation of hospitalization or home stay or death. Nineteen hospitals, including nine acute-care, eight rehabilitation and two long-term care hospitals, and one home-visit rehabilitation team were registered in this database. The registration period was from April 2018 to March 2021. The inclusion criteria were patients aged >20 years who presented with dysphagia, which was defined as a Food Intake Level Scale [18] score of ≤8. Food Intake Level Scale scores of 1–3 relate to various degrees of nonoral feeding; 4–6 to various degrees of oral food intake and alternative nutrition; 7 and 8 to various degrees of oral food intake alone; 9 to no dietary restriction but medical consideration given and 10 indicates normal oral food intake. The exclusion criteria were patients with missing data. This study was approved by the Ethics Committee of Sapporo Nishi Maruyama Hospital, Keijinkai (1 November 2019). All patients provided informed consent prior to enrolment in the database.

2.2. Data Collection

The following data were included in the database registration: age, sex, body mass index, calf circumference, handgrip strength, C-reactive protein level, serum albumin levels and Charlson Comorbidity Index [19]. Body mass index was calculated by dividing body weight (kg) by height squared (m2). Charlson Comorbidity Index was used to assess comorbidities, with higher scores indicating greater comorbidity severity and risk of mortality. At baseline and follow-up, the Food Intake Level Scale and Barthel Index scores were calculated. The Barthel Index includes 10 items as follows: feeding, moving from a wheelchair to bed and back, grooming, transferring to and from a toilet, bathing, walking on a level surface, going up and down stairs, dressing, bowel continence and bladder continence. The degrees of functional ability for each Barthel Index category vary, with higher scores indicating complete independence and lower scores indicating less physical function. Clinical, rehabilitation-related and nutrition-related data were entered based on the judgement of physicians, rehabilitation-related professionals and ward staff and dieticians, respectively. Registry guidelines were developed for measurement.

2.3. Nutritional Assessment

In this study, nutritional status was diagnosed using the GLIM criteria [20]. The GLIM criteria were developed to standardize the diagnosis of adult undernutrition in clinical practice worldwide. The steps involved in assessments using the GLIM criteria are as follows: The first step is to screen the candidates using a validated screening tool. The Mini Nutritional Assessment Short-Form was used as the screening tool in this study [21]. If the screening indicates that the patient is at risk of malnutrition, the patient moves on to the next step. The second step is to assess each of the three phenotypic and two etiologic criteria. The phenotypic criteria comprise the following three components: unintentional weight loss, low body mass index and loss of muscle mass. The phenotypic criteria included weight loss (≥5% within the last 6 months and ≥10% after >6 months), low body mass index (18.5 kg/m2 in patients aged <70 years and <20.0 kg/m2 in those aged ≥70 years) and reduced muscle mass [22,23]. There are two etiologic criteria: decreased food intake or digestive/absorptive capacity and disease burden/inflammatory involvement. The etiologic criteria used in this study were reduced food intake (1 week or any reduction for >2 weeks), assimilation problems (e.g., dysphagia, vomiting and diarrhea) and disease burden/inflammatory condition (e.g., congestive heart failure, chronic obstructive pulmonary disease, chronic kidney disease and cancer). When one or more of the presenting phenotypic and etiologic criteria apply, undernutrition is diagnosed.

2.4. Outcome

The primary outcome was improvement in the Food Intake Level Scale. The Food Intake Level Scale is a 10-point scale for assessing dysphagia [18]. Food Intake Level Scale scores of 1–3 indicated parenteral intake; 4–6 indicated oral food intake and alternative nutrition; 7 and 8 indicated oral food intake alone; 9 indicated no dietary restrictions but with medical considerations and 10 indicated no issues with swallowing. The Food Intake Level Scale change was calculated by subtracting the Food Intake Level Scale score at baseline from that at follow-up. A larger increase in Food Intake Level Scale change indicated a greater improvement in dysphagia. The secondary outcome was the Barthel Index change, a widely used measure of activities of daily living [24]. The Barthel Index comprises 10 items: bathing, grooming, eating, dressing, defecation, bladder, toilet movement, stairs, transferring and moving. Bathing and grooming were rated on a scale of 0 or 5. Eating, dressing, defecation, bladder, toilet movement and stairs were rated on a scale of 0, 5 or 10. Transferring and moving were rated using a four-point scale (0, 5, 10 or 15). The highest Barthel Index score was 100, with higher scores indicating a better ability to perform activities of daily living. The Barthel Index gain was calculated by subtracting the Barthel Index score at baseline from that at follow-up. A larger increase in Barthel Index change indicated a greater improvement in performing activities of daily living [25].

2.5. Statistical Analyses

Data analysis was performed using the Statistical Package for the Social Sciences software version 26 (IBM; Armonk, New York, the USA). Parametric data are expressed as mean ± standard deviation and nonparametric data as median and interquartile range. Categorical data are presented as n (%). The Student’s t-test, Mann–Whitney U test, chi-square test and Fisher’s exact test were used to analyze differences between the undernutrition and normal nutritional status groups. The Food Intake Level Scale gain and Barthel Index gain were compared between the undernutrition and normal nutritional status groups in the univariate analysis. In addition, multiple regression analysis was performed with the Food Intake Level Scale gain and Barthel Index gain as the objective variables and undernutrition as the explanatory variable. The covariates were age, sex, Charlson Comorbidity Index and setting at the time of the survey. A p-value of <0.05 was considered statistically significant. The follow-up was performed at discharge or 3 months after admission, at which time changes were calculated.

3. Results

The total number of registered patients in the Japanese Sarcopenic Dysphagia Database was 467. Among them, 27 patients with missing data were excluded. Finally, 440 registered patients were included in the analysis (Figure 1). Rehabilitation hospitals were the most common prehospitalization facilities (47.5%), followed by acute-care hospitals (42.5%), long-term care hospitals (9.3%) and others (0.7%).
Table 1 displays the demographic characteristics of the participants at baseline. The mean age of the patients was 80.2 ± 10.9 years. Furthermore, 281 (64%) patients were classified as undernourished according to the GLIM criteria and were included in the undernutrition group. Compared with the normal nutritional status group, the undernutrition group was significantly older and had a high C-reactive protein level and Charlson Comorbidity Index (p < 0.001). The undernutrition group had a significantly lower serum albumin level, body mass index, calf circumference and handgrip strength than the normal nutritional status group (p < 0.001).
Table 2 presents the results of analysis using the GLIM criteria for the undernutrition and normal nutritional status groups. The results of the phenotypic criteria are given below. The percentage of unintentional weight loss was significantly higher in the undernutrition group (41 (9.4%)) than in the normal nutritional status group (7 (1.6%); p < 0.001). The percentage of low body mass index was significantly higher in the undernutrition group (158 (36.0%)) than in the normal nutrition status group (53 (12.1%); p < 0.001). The percentage of decreased muscle mass was significantly greater in the undernutrition group (276 (63.0%)) than in the normal nutritional status group (118 (26.9%); p < 0.001). In terms of etiological criteria, the percentage of decreased food intake or assimilation was significantly higher in the undernutrition group (160 (36.4%)) than in the normal nutritional status group (8 (1.8%); p < 0.001). The rate of disease burden/inflammation was significantly higher in the undernutrition group (170 (38.7%)) than in the normal nutrition status group (13 (3.0%); p < 0.001).
Table 3 displays the results of univariate analysis of Food Intake Level Scale and Barthel Index for the undernutrition and normal nutrition status groups. The median Food Intake Level Scale score at baseline was significantly higher (p < 0.001) in the undernutrition group (median, 7; interquartile range, 5–8) than in the normal nutrition status group (median, 7; interquartile range, 2–7). At follow-up, the median Food Intake Level Scale score for the undernutrition group (median, 8; interquartile range, 7–8) was not significantly different from that for the normal nutritional status group (median, 8; interquartile range, 7–8). The median rate of increase in a Food Intake Level Scale score was significantly higher (p < 0.001) in the undernutrition group (median, 1; interquartile range, 0–5) than in the normal nutrition status group (median, 0; interquartile range, 0–2). The median Barthel Index score at baseline for the undernutrition group (median, 30; interquartile range, 10–50) was not significantly different from that for the normal nutrition status group (median, 25; interquartile range, 5–50). The median Barthel Index score at follow-up was significantly lower (p < 0.001) in the undernutrition group (median, 50; interquartile range, 20–70) than in the normal nutrition status group (median, 60; interquartile range, 30–90). The median rate of increase in Barthel Index score was significantly lower (p < 0.001) in the undernutrition group (median, 10; interquartile range, 0–28) than in the normal nutrition status group (median, 20; interquartile range, 5–40). Compared with the normal nutrition status group, the undernutrition group had significantly lower increases in the Barthel Index at baseline and at follow-up (p < 0.001).
Table 4 displays the results of regression analysis for determining improvements in the Food Intake Level Scale and Barthel Index scores adjusted for age, sex, Charlson Comorbidity Index and prehospitalization facilities. Undernutrition diagnosed using the GLIM criteria was independently associated with the Food Intake Level Scale gain (partial regression coefficient (B) = −0.633, 95% confidence interval (CI) = −1.099 to −0.167) and Barthel Index gain (B = −8.414, 95% CI = −13.089 to −3.739).

4. Discussion

This multicenter, retrospective cohort study of patients with dysphagia revealed the following points: First, compared with normal nutritional status, undernutrition diagnosed using the GLIM criteria was associated with poor improvement in swallowing function. Second, undernutrition affected the improvement in activities of daily living. The current study is among the few that examined improvement in swallowing function and activities of daily living in patients with dysphagia and undernutrition diagnosed using the GLIM criteria.
Multivariate analysis revealed that undernutrition negatively affects the gain on the Food Intake Level Scale. Previous studies have shown that undernutrition negatively affects the improvement in swallowing function. Deteriorated nutritional status affects the improvement in dysphagia [26]. Furthermore, it increases the risk of weight loss, low BMI and decreased skeletal muscle mass [27]. Thus, undernutrition leads to a decrease in overall muscle mass (sarcopenia), and swallowing-related muscles, and may result in dysphagia.
Worse improvement in swallowing function could be attributed to the loss of muscle mass and strength that were assessed by the GLIM criteria. Undernutrition causes dysphagia due to a decrease in total body skeletal muscle mass and muscle strength related to swallowing [1,8]. In this study, compared with the normal nutritional status group, the undernutrition group had a significantly lower body mass index and calf circumference, a measure of muscle mass and handgrip strength and a measure of muscle strength. Grip strength is correlated with tongue muscle strength [28] and low tongue pressure with poor improvement in swallowing function [16]. Furthermore, body mass index and reduced skeletal muscle mass are considered risk factors of dysphagia in older hospitalized adult patients [1,29]. Thus, the patients with undernutrition, who had a lower muscle mass and strength, may have poor improvement in swallowing function. Poor muscle mass and strength in undernourished patients may also attribute to the development of dysphagia in sarcopenia.
Moreover, undernutrition affects improvement in activities of daily living. In rehabilitative patients, undernutrition was associated with poor activities of daily living [27,30]. Undernutrition inhibits improvement in activities of daily living due to muscle weakness, wasting and physical frailty and complications during hospitalization [27]. Another study showed that undernutrition was associated with poor functional outcomes and a higher percentage of weight loss [31]. In this study, undernutrition was associated with a significantly higher percentage of weight loss compared with normal nutritional status. Weight loss can decrease the capability to perform activities of daily living, including physical components such as mobility limitations [32,33]. Therefore, the association of GLIM-criteria-defined undernutrition, including loss of muscle mass, with improvement in activities of daily living seems plausible and supports the findings from a previous study.
Nutritional status and rehabilitation are important in improving the swallowing function and activities of daily living in patients with dysphagia and undernutrition. Much of feeding and swallowing problems affected by sarcopenia may be avoidable [34,35]. Given the pathogenesis mechanism, nutritional management that considers muscle mass and function is critical. Undernutrition and sarcopenia can be accurately assessed to identify subjects at risk of developing the disease. The GLIM criteria are useful for detecting malnutrition. To put it another way, in patients with sarcopenic dysphagia, both nutritional management and physical intervention can improve general muscle strength and function, including swallowing muscles [36]. Furthermore, individualized, high-frequency nutritional support with the multidisciplinary intervention was associated with better nutritional status, physical function and dysphagia in poststroke survivors with undernutrition [37]. These reports showed the importance of improving nutritional status and rehabilitation in patients with dysphagia and undernutrition.
Rehabilitation nutrition has been shown to improve swallowing function and activities of daily living in patients with dysphagia and malnutrition [38]. Rehabilitation nutrition is a combination of rehabilitation and nutritional therapy. Although there are few clinical studies examining the efficacy of nutritional support for dysphagia in sarcopenia, multidisciplinary feeding and swallowing rehabilitation, as well as nutritional care, may be beneficial in the treatment of sarcopenia dysphagia [38,39,40].
The current study had some limitations. First, the severity of undernutrition diagnosed by the GLIM criteria was not evaluated. Therefore, the degree of improvement in swallowing function and activities of daily living according to undernutrition severity is unknown. Second, this study only included patients with the Food Intake Level Scale ≤8. Therefore, the generalizability of the study results must be examined in patients with dysphagia assessed by gold-standard methods (e.g., videofluorography). Third, research is needed to compare the differences in prevention, treatment and nutritional management between sarcopenia eating and swallowing disorders and other eating and swallowing disorders. Because dysphagia is a complex condition caused by a variety of factors, factors other than nutritional management must be considered.

5. Conclusions

Patients with dysphagia who presented undernutrition diagnosed by the GLIM criteria demonstrated inadequate improvement in swallowing function and ability to perform activities of daily living than those who presented with normal nutritional status. Nevertheless, further studies are needed to examine the effects of rehabilitation nutrition in patients with dysphagia who presented with undernutrition. The significance of this study is that it evaluated the predictive validity of the GLIM criteria, which may help improve activities of daily living in patients with dysphagia.

Author Contributions

Conceptualization, S.A., Y.K., K.M., S.N. and H.W.; methodology, S.A., Y.K., K.M., S.N. and H.W.; validation, S.A., Y.K., K.M., S.N., H.M., Y.T., S.S., K.S., N.E. and H.W.; formal analysis, S.A., K.M., S.N., H.M., Y.T., S.S., K.S., N.E. and H.W.; investigation, S.A., H.M., Y.T., S.S., K.S., N.E. and H.W.; data curation, S.A., H.M., Y.T., S.S., K.S., N.E. and H.W.; writing—original draft preparation, S.A. and Y.K.; writing—review and editing, S.A., Y.K., K.M., S.N., R.M., H.M., Y.T., S.S., K.S., N.E. and H.W.; visualization, S.A., Y.K. and H.W.; supervision, H.W.; project administration, H.W. All authors have read and agreed to the published version of the manuscript.

Funding

The research received no external funding.

Institutional Review Board Statement

The study was conducted in accordance with the Declaration of Helsinki and approved by the Ethics Committee of Sapporo Nishi Maruyama Hospital, Keijinkai (1 November 2019).

Informed Consent Statement

All participants provided informed consent prior to enrolment and were allowed to withdraw from the study at any time (opt out).

Data Availability Statement

Not applicable.

Conflicts of Interest

The authors declare no conflict of interest.

References

  1. Fujishima, I.; Fujiu-Kurachi, M.; Arai, H.; Hyodo, M.; Kagaya, H.; Maeda, K.; Mori, T.; Nishioka, S.; Oshima, F.; Ogawa, S.; et al. Sarcopenia and dysphagia: Position paper by four professional organizations. Geriatr. Gerontol. Int. 2019, 19, 91–97. [Google Scholar] [CrossRef] [PubMed] [Green Version]
  2. Holland, G.; Jayasekeran, V.; Pendleton, N.; Horan, M.; Jones, M.; Hamdy, S. Prevalence and symptom profiling of oropharyngeal dysphagia in a community dwelling of an elderly population: A self-reporting questionnaire survey. Dis. Esophagus. 2011, 24, 476–480. [Google Scholar] [CrossRef] [PubMed]
  3. Roy, N.; Stemple, J.; Merrill, R.M.; Thomas, L. Dysphagia in the elderly: Preliminary evidence of prevalence, risk factors, and socioemotional effects. Ann. Otol. Rhinol. Laryngol. 2007, 116, 858–865. [Google Scholar] [CrossRef]
  4. Park, Y.H.; Han, H.R.; Oh, B.M.; Lee, J.; Park, J.A.; Yu, S.J.; Chang, H. Prevalence and associated factors of dysphagia in nursing home residents. Geriatr. Nurs. 2013, 34, 212–217. [Google Scholar] [CrossRef] [PubMed]
  5. Peñalva-Arigita, A.; Prats, R.; Lecha, M.; Sansano, A.; Vila, L. Prevalence of dysphagia in a regional hospital setting: Acute care hospital and a geriatric sociosanitary care hospital: A cross-sectional study. Clin. Nutr. ESPEN 2019, 33, 86–90. [Google Scholar] [CrossRef] [PubMed]
  6. Bomze, L.; Dehom, S.; Lao, W.P.; Thompson, J.; Lee, N.; Cragoe, A.; Luceno, C.; Crawley, B. Comorbid dysphagia and malnutrition in elderly hospitalized patients. Laryngoscope 2021, 131, 2441–2447. [Google Scholar] [CrossRef]
  7. Sura, L.; Madhavan, A.; Carnaby, G.; Crary, M.A. Dysphagia in the elderly: Management and nutritional considerations. Clin. Interv. Aging 2012, 7, 287–298. [Google Scholar]
  8. Tran, T.P.; Nguyen, L.T.; Kayashita, J.; Shimura, F.; Yamamoto, S. Nutritional status and feeding practice among dysphagic older adult inpatients in Vietnam. J. Nutr. Sci. Vitaminol. 2020, 66, 224–228. [Google Scholar] [CrossRef]
  9. Veldee, M.S.; Peth, L.D. Can protein-calorie malnutrition cause dysphagia? Dysphagia 1992, 7, 86–101. [Google Scholar] [CrossRef]
  10. Wakabayashi, H. Presbyphagia and sarcopenic dysphagia: Association between aging, sarcopenia, and deglutition disorders. J. Frailty Aging 2014, 3, 97–103. [Google Scholar] [CrossRef]
  11. Ueshima, J.; Shimizu, A.; Maeda, K.; Uno, C.; Shirai, Y.; Sonoi, M.; Motokawa, K.; Egashira, F.; Kayashita, J.; Kudo, M.; et al. Nutritional management in adult patients with dysphagia: Position paper from Japanese working group on integrated nutrition for dysphagic people. J. Am. Med. Dir. Assoc. 2022, 23, 1676–1682. [Google Scholar] [CrossRef] [PubMed]
  12. Jensen, G.L.; Cederholm, T.; Correia, M.I.T.D.; Gonzalez, M.C.; Fukushima, R.; Higashiguchi, T.; de Baptista, G.A.; Barazzoni, R.; Blaauw, R.; Coats, A.J.S.; et al. GLIM criteria for the diagnosis of malnutrition: A consensus report from the global clinical nutrition community. JPEN J. Parenter. Enteral. Nutr. 2019, 43, 32–40. [Google Scholar] [CrossRef] [Green Version]
  13. Ueshima, J.; Momosaki, R.; Shimizu, A.; Motokawa, K.; Sonoi, M.; Shirai, Y.; Uno, C.; Kokura, Y.; Shimizu, M.; Nishiyama, A.; et al. Nutritional assessment in adult patients with dysphagia: A scoping review. Nutrients 2021, 13, 778. [Google Scholar] [CrossRef] [PubMed]
  14. Riso, S.; Para, O.; Collo, A.; Campanini, M.; Rotunno, S.; Giorgetti, G.; Zanetti, M.; Manfellotto, D. FADOI and SINPE Clinical nutrition in internal medicine: An Italian survey by the scientific societies FADOI and SINPE. Nutrition 2022, 98, 111623. [Google Scholar] [CrossRef] [PubMed]
  15. Taguchi, K.; Wakabayashi, H.; Fujimoto, M.; Obayashi, S.; Yamamoto, M.; Nishioka, S.; Momosaki, R. Association between malnutrition severity and swallowing function in convalescent rehabilitation wards: A multi-center cohort study in malnourished patients with sarcopenic dysphagia. J. Nutr. Health Aging 2022, 26, 469–476. [Google Scholar] [CrossRef] [PubMed]
  16. Shimizu, A.; Fujishima, I.; Maeda, K.; Wakabayashi, H.; Nishioka, S.; Ohno, T.; Nomoto, A.; Shigematsu, T.; Kayashita, J. Japanese Working Group on Sarcopenic Dysphagia Effect of low tongue pressure on nutritional status and improvement of swallowing function in sarcopenic dysphagia. Nutrition 2021, 90, 111295. [Google Scholar] [CrossRef]
  17. Mizuno, S.; Wakabayashi, H.; Fujishima, I.; Kishima, M.; Itoda, M.; Yamakawa, M.; Wada, F.; Kato, R.; Furiya, Y.; Nishioka, S.; et al. Construction and quality evaluation of the Japanese sarcopenic dysphagia database. J. Nutr. Health Aging 2021, 25, 926–932. [Google Scholar] [CrossRef] [PubMed]
  18. 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. [Google Scholar] [CrossRef]
  19. Charlson, M.E.; Pompei, P.; Ales, K.L.; MacKenzie, C.R. A new method of classifying prognostic comorbidity in longitudinal studies: Development and validation. J. Chronic Dis. 1987, 40, 373–383. [Google Scholar] [CrossRef]
  20. Cederholm, T.; Jensen, G.L.; Correia, M.I.T.D.; Gonzalez, M.C.; Fukushima, R.; Higashiguchi, T.; Baptista, G.; Barazzoni, R.; Blaauw, R.; Coats, A.J.S. GLIM criteria for the diagnosis of malnutrition—A consensus report from the global clinical nutrition community. J. Cachexia Sarcopenia Muscle 2019, 10, 207–217. [Google Scholar] [CrossRef] [Green Version]
  21. Kaiser, M.J.; Bauer, J.M.; Ramsch, C.; Uter, W.; Guigoz, Y.; Cederholm, T.; Thomas, D.R.; Anthony, P.; Charlton, K.E.; Maggio, M.; 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, 13, 782–788. [Google Scholar] [CrossRef] [PubMed]
  22. Chen, L.K.; Woo, J.; Assantachai, P.; Auyeung, T.W.; Chou, M.Y.; Iijima, K.; Jang, H.C.; Kang, L.; Kim, M.; Kim, S.; et al. Asian Working Group for Sarcopenia: 2019 Consensus update on sarcopenia diagnosis and treatment. J. Am. Med. Dir. Assoc. 2020, 21, 300–307.e2. [Google Scholar] [CrossRef] [PubMed]
  23. Kawakami, R.; Murakami, H.; Sanada, K.; Tanaka, N.; Sawada, S.S.; Tabata, I.; Higuchi, M.; Miyachi, M. Calf circumference as a surrogate marker of muscle mass for diagnosing sarcopenia in Japanese men and women. Geriatr. Gerontol. Int. 2015, 15, 969–976. [Google Scholar] [CrossRef] [PubMed]
  24. Mahoney, F.I.; Barthel, D.W. Functional evaluation: The Barthel index. Md. State Med. J. 1965, 14, 61–65. [Google Scholar]
  25. Collin, C.; Wade, D.T.; Davies, S.; Horne, V. The Barthel ADL Index: A reliability study. Int. Disabil Stud. 1988, 10, 61–63. [Google Scholar] [CrossRef]
  26. Nishioka, S.; Okamoto, T.; Takayama, M.; Urushihara, M.; Watanabe, M.; Kiriya, Y.; Shintani, K.; Nakagomi, H.; Kageyama, N. Malnutrition risk predicts recovery of full oral intake among older adult stroke patients undergoing enteral nutrition: Secondary analysis of a multicentre survey (the APPLE study). Clin. Nutr. 2017, 36, 1089–1096. [Google Scholar] [CrossRef] [PubMed]
  27. Nishioka, S.; Wakabayashi, H. Interaction between malnutrition and physical disability in older adults: Is there a malnutrition-disability cycle? Nutr. Rev. 2023, 10, 191–205. [Google Scholar] [CrossRef]
  28. Butler, S.G.; Stuart, A.; Leng, X.; Wilhelm, E.; Rees, C.; Williamson, J.; Kritchevsky, S.B. The relationship of aspiration status with tongue and handgrip strength in healthy older adults. J. Gerontol. A Biol. Sci. Med. Sci. 2011, 66, 452–458. [Google Scholar] [CrossRef] [PubMed] [Green Version]
  29. 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, 72, 1290–1294. [Google Scholar] [CrossRef]
  30. Wojzischke, J.; van Wijngaarden, J.; van den Berg, C.; Cetinyurek-Yavuz, A.; Diekmann, R.; Luiking, Y.; Bauer, J. Nutritional status and functionality in geriatric rehabilitation patients: A systematic review and meta-analysis. Eur. Geriatr. Med. 2020, 11, 195–207. [Google Scholar] [CrossRef] [Green Version]
  31. Kokura, Y.; Momosaki, R. Prevalence of malnutrition assessed by the GLIM criteria and association with Activities of Daily Living in older residents in an integrated facility for medical and long-term care. Nutrients 2022, 14, 3656. [Google Scholar] [CrossRef] [PubMed]
  32. Kalm, L.M.; Semba, R.D. They starved so that others be better fed: Remembering Ancel Keys and the Minnesota experiment. J. Nutr. 2005, 135, 1347–1352. [Google Scholar] [CrossRef] [PubMed] [Green Version]
  33. Kurkcu, M.; Meijer, R.I.; Lonterman, S.; Muller, M.; de van der Schueren, M.A.E. The association between nutritional status and frailty characteristics among geriatric outpatients. Clin. Nutr. ESPEN 2018, 23, 112–116. [Google Scholar] [CrossRef] [PubMed]
  34. Shimizu, A.; Fujishima, I.; Maeda, K.; Wakabayashi, H.; Nishioka, S.; Ohno, T.; Nomoto, A.; Kayashita, J.; Mori, N. the Japanese Working Group on Sarcopenic Dysphagia Nutritional management enhances the recovery of swallowing ability in older patients with sarcopenic dysphagia. Nutrients 2021, 11, 596. [Google Scholar] [CrossRef]
  35. Hudson, H.M.; Daubert, C.R.; Mills, R.H. The interdependency of protein-energy malnutrition, aging, and dysphagia. Dysphagia 2000, 15, 31–38. [Google Scholar] [CrossRef]
  36. Shimazu, S.; Yoshimura, Y.; Kudo, M.; Nagano, F.; Bise, T.; Shiraishi, A.; Sunahara, T. Frequent and personalized nutritional support leads to improved nutritional status, activities of daily living, and dysphagia after stroke. Nutrition 2021, 83, 111091. [Google Scholar] [CrossRef]
  37. Wakabayashi, H. Rehabilitation nutrition in general and family medicine. J. Gen. Fam Med. 2017, 18, 153–154. [Google Scholar] [CrossRef] [Green Version]
  38. Maeda, K.; Akagi, J. Treatment of sarcopenic dysphagia with rehabilitation and nutritional support: A comprehensive approach. J. Acad. Nutr. Diet. 2016, 116, 573–577. [Google Scholar] [CrossRef]
  39. Wakabayashi, H.; Uwano, R. Rehabilitation nutrition for possible sarcopenic dysphagia after lung cancer surgery: A case report. Am. J. Phys. Med. Rehabil. 2016, 95, e84–e89. [Google Scholar] [CrossRef]
  40. Zanetti, G.; Merati, G. Interaction between photosystem I and ferredoxin. Identification by chemical cross-linking of the polypeptide which binds ferredoxin. Eur. J. Biochem. 1987, 169, 143–146. [Google Scholar] [CrossRef]
Figure 1. A flowchart of participant selection.
Figure 1. A flowchart of participant selection.
Nutrients 15 01291 g001
Table 1. Demographic characteristics of the participants at baseline.
Table 1. Demographic characteristics of the participants at baseline.
All Patients
n = 440
Patients with Undernutrition Diagnosed Using the GLIM Criteria
n = 281
Patients with Normal Nutritional Status
n = 159
p-Value
Age, years, mean ± SD80.2 ± 10.981.8 ± 10.577.3 ± 11.0<0.001 (a)
Sex, female, n (%)224 (50.9)152 (54.1)72 (45.3)0.091 (b)
Prehospitalization facilities, n (%) 0.223 (c)
Acute-care hospitals187 (42.5)125 (44.5)62 (39.0)
Rehabilitation hospitals209 (47.5)124 (44.1)85 (53.5)
Long-term care hospitals41 (9.3)30 (10.7)11 (6.9)
Others3 (0.7)2 (0.7)1 (0.6)
Body mass index (kg/m2), mean ± SD20.2 ± 3.719.6 ± 3.521.4 ± 3.8<0.001 (a)
Calf circumference (cm), median (IQR)28 (25, 31)27 (25, 30)30 (26, 33)<0.001 (d)
Handgrip strength (kg), median (IQR)12.0 (6.3, 19.0)11.0 (6.0, 17.5)14.2 (8.1, 22.1)<0.001 (d)
C-reactive protein levels (mg/dL), median (IQR)0.7 (0.2, 2.9)1.0 (0.3, 5.2)0.2 (0.1, 0.7)<0.001 (d)
Serum albumin levels (g/dL), median (IQR)3.4 (3.0, 3.7)3.3 (2.9, 3.6)3.5 (3.3, 3.9)<0.001 (d)
Charlson Comorbidity Index, median (IQR)2 (0, 4)2 (1, 4)2 (0, 3)<0.001 (d)
SD, standard deviation; IQR, interquartile range; (a) Student’s t-test; (b) Chi-square test; (c) Fisher’s exact test; (d) Mann–Whitney U test.
Table 2. Global Leadership Initiative on Malnutrition criteria.
Table 2. Global Leadership Initiative on Malnutrition criteria.
Patients with Undernutrition Diagnosed Using the GLIM Criteria
n = 281
Patients with Normal Nutritional Status
n = 159
p-Value
Phenotypic criteria, presence, n (%)
Weight loss 41 (9.4)7 (1.6)<0.001 (a)
Low body mass index158 (36.0)53 (12.1)<0.001 (a)
Reduced muscle mass 276 (63.0)118 (26.9)<0.001 (a)
Etiologic criteria, presence, n (%)
Reduced food intake or assimilation 160 (36.4)8 (1.8)<0.001 (a)
Disease burden/inflammation 170 (38.7)13 (3.0)<0.001 (a)
(a) Chi-square test.
Table 3. Univariate analysis of Functional Intake Level Scale score and Barthel Index.
Table 3. Univariate analysis of Functional Intake Level Scale score and Barthel Index.
Patients with Undernutrition Diagnosed Using the GLIM Criteria
n = 281
Patients with Normal Nutritional Status
n = 159
p-Value
Functional Intake Level Scale score, median (IQR)
Admission7 (5, 8)7 (2, 7)<0.001 (a)
Follow-up8 (7, 8)8 (7, 8)0.262 (a)
Change1 (0, 5)0 (0, 2)<0.001 (a)
Barthel Index, median (IQR)
Admission30 (10, 50)25 (5, 50)0.224 (a)
Follow-up50 (20, 70)60 (30, 90)<0.001 (a)
Change10 (0, 28)20 (5, 40)<0.001 (a)
IQR, interquartile range; (a) Mann–Whitney U test.
Table 4. Multiple regression analysis of changes in the Functional Intake Level Scale score and Barthel Index score.
Table 4. Multiple regression analysis of changes in the Functional Intake Level Scale score and Barthel Index score.
Change in the Functional Intake Level Scale ScoreChange in the Barthel Index Score
B95% Confidence Intervalp-ValueB95% Confidence Intervalp-Value
LowerUpper LowerUpper
Age−0.051−0.072−0.029<0.001−0.201−0.4160.0140.067
Sex−0.392−0.8490.0640.092−0.277−4.8574.3030.905
Charlson Comorbidity Index−0.098−0.2200.0240.116−1.859−3.085−0.633<0.003
Prehospitalization facilities−1.159−1.497−0.821<0.001−0.547−3.9382.8440.751
Undernutrition diagnosed using the GLIM criteria−0.633−1.099−0.167<0.008−8.414−13.089−3.739<0.001
B, partial regression coefficient; GLIM, Global Leadership Initiative on Malnutrition.
Disclaimer/Publisher’s Note: The statements, opinions and data contained in all publications are solely those of the individual author(s) and contributor(s) and not of MDPI and/or the editor(s). MDPI and/or the editor(s) disclaim responsibility for any injury to people or property resulting from any ideas, methods, instructions or products referred to in the content.

Share and Cite

MDPI and ACS Style

Abe, S.; Kokura, Y.; Maeda, K.; Nishioka, S.; Momosaki, R.; Matsuoka, H.; Tomii, Y.; Sugita, S.; Shimizu, K.; Esashi, N.; et al. Effects of Undernutrition on Swallowing Function and Activities of Daily Living in Hospitalized Patients: Data from the Japanese Sarcopenic Dysphagia Database. Nutrients 2023, 15, 1291. https://doi.org/10.3390/nu15051291

AMA Style

Abe S, Kokura Y, Maeda K, Nishioka S, Momosaki R, Matsuoka H, Tomii Y, Sugita S, Shimizu K, Esashi N, et al. Effects of Undernutrition on Swallowing Function and Activities of Daily Living in Hospitalized Patients: Data from the Japanese Sarcopenic Dysphagia Database. Nutrients. 2023; 15(5):1291. https://doi.org/10.3390/nu15051291

Chicago/Turabian Style

Abe, Sayaka, Yoji Kokura, Keisuke Maeda, Shinta Nishioka, Ryo Momosaki, Hiroki Matsuoka, Yasuomi Tomii, Shinnosuke Sugita, Kenta Shimizu, Nanami Esashi, and et al. 2023. "Effects of Undernutrition on Swallowing Function and Activities of Daily Living in Hospitalized Patients: Data from the Japanese Sarcopenic Dysphagia Database" Nutrients 15, no. 5: 1291. https://doi.org/10.3390/nu15051291

APA Style

Abe, S., Kokura, Y., Maeda, K., Nishioka, S., Momosaki, R., Matsuoka, H., Tomii, Y., Sugita, S., Shimizu, K., Esashi, N., & Wakabayashi, H. (2023). Effects of Undernutrition on Swallowing Function and Activities of Daily Living in Hospitalized Patients: Data from the Japanese Sarcopenic Dysphagia Database. Nutrients, 15(5), 1291. https://doi.org/10.3390/nu15051291

Note that from the first issue of 2016, this journal uses article numbers instead of page numbers. See further details here.

Article Metrics

Back to TopTop