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. 2018 May 31;22(8):1003–1009. doi: 10.1007/s12603-018-1055-z

Systematic Review and Meta-Analysis of the Association Between Sarcopenia and Dysphagia

W-T Zhao 1,2, M Yang 1,2, H-M Wu 1,2, L Yang 3, Xue-mei Zhang 1,2, Y Huang 1,2
PMCID: PMC12876361  PMID: 30272106

Abstract

Objectives

Sarcopenia, an age-related decrease in muscle mass and function, is associated with several potential adverse health outcomes. Its association with another age-related syndrome, dysphagia remains unclear. This systematic review and meta-analysis aims to explore the association between sarcopenia and dysphagia.

Methods

PubMed, Embase, Scopus and CINAHL were searched for cross-sectional, case-control and cohort studies that investigated the association between sarcopenia and dysphagia. First author, publication year, study type, sample size, inclusion and exclusion criteria, participant demographics, definition and measurement for evaluation of sarcopenia and dysphagia, main outcomes were retrieved. The association between sarcopenia and dysphagia were expressed by odds ratio (OR) and 95% confidence interval (CI).

Results

9 studies are eligible in the systematic review, and 5 cross-sectional studies comprising 913 participants which showed dichotomous classification of sarcopenia and dysphagia were included in the meta-analysis. The crude odds ratios (ORs) were extracted from 5 studies, and 4 of them also provide adjusted ORs. The crude ORs between sarcopenia and dysphagia is 6.17 (95% CI, 3.81-10.00), after adjusting for some confounders, such as age, sex, Barthel Index score, nutritional status, sarcopenia is also have an association with dysphagia (adjusted ORs, 4.06; 95% CI, 2.27-7.29). The subgroup analysis showed that there was no significant difference between different sarcopenia diagnostic criteria, assessment tools of skeletal muscle mass and dysphagia.

Conclusion

Sarcopenia was positively associated with dysphagia. Prevention and screening of dysphagia is essential among sarcopenic old patients. The causal relationship requires more prospective cohort study for confirmation.

Key words: Sarcopenia, dysphagia, aging, order people

Introduction

Dysphagia is a medical term for the symptom of difficulty in swallowing (1). It has been estimated that 13%-35% of elderly individuals who live independently report dysphagia symptoms (2). Dysphagia is regarded as an important and serious current and future issue in geriatric medicine for the reason that it increases the risk of malnutrition and clinical complications, such as aspiration pneumonia, choking, dehydration and mortality (3, 4, 5). Recently, a possible association has been reported between sarcopenia and dysphagia (6, 7). Sarcopenia is a geriatric syndrome, which is characterized by progressive and generalized loss of muscle mass and strength (8). This term was first coined by Rosenberg in 1989 to describe agerelated decrease in muscle mass (9). The decline of muscle mass has been documented as a physiologic phenomenon, being approximately 3-8% per decade after 30 years old, and with further decline after 60 years old (10). The prevalence of sarcopenia varies from 0.9% to 85.4% in the elderly population based on its different definitions, measuring tools and cut-off values (11). Sarcopenia is categorized as primary and secondary sarcopenia based on its etiology (10). The dominant reason of primary sarcopenia is aging, while the reasons for secondary sarcopenia are inactivity, malnutrition and some diseases, such as stroke and Alzheimer's disease (12). It also has been associated with several potential adverse health outcomes, including disability, mortality, increased incidence of falls, longer hospitalization and increased need for rehabilitation care after hospital discharge (13, 14).

In recent years, some studies indicated that there has been an observed association between sarcopenia and dysphagia, due to a generalized decline of muscle mass and muscle strength in elder people, which can coincide with weakening of the muscles related to swallowing (12). However, the association among various studies were varied as the different targeted people as well as methods in assessing sarcopenia and dysphagia, and there has been no systematic review or metaanalysis study published in the literature. Therefore, this metaanalysis aims to explore the association between sarcopenia and dysphagia.

Method

Search strategy and inclusion criteria

PubMed, Embase, Scopus and CINAHL were searched for cross-sectional, case-control and cohort studies that investigated the association between sarcopenia and dysphagia published between the earliest record and January 2018. Old adults aged 60 years or older were eligible. Sarcopenia was defined as an age-related loss of muscle mass and/or reduced muscle strength and/or impaired physical performance. The assessment of dysphagia by a validated diagnostic method or scale was required in each enrolled study. Studies were excluded if they were review articles, randomized controlled trials, case report or conference abstracts. The combination of key terms for literatures search was listed as follows: (sarcopenia OR muscle atrophy OR muscle mass) AND (dysphagia OR swallowing disorders OR deglutition disorders OR swallowing difficulties). The references lists of the retrieved articles were manually retrieved for other potentially eligible studies. Additionally, only articles published in English or Chinese were included, and the abstracts that lacked of available full texts were discarded.

Data extraction and outcome of interest

Two researchers independently evaluated the studies and extracted the information and data using a standardized form that included first author, publication year, study type (crosssectional studies, case-control studies or cohort studies), sample size, average age, inclusion and exclusion criteria, participant demographics, definition and measurement for evaluation of sarcopenia and dysphagia. Any disagreement in abstracted data was discussed with a third reviewer. The outcomes of interest was the association between sarcopenia and dysphagia, expressed by odds ratio (OR) and 95% confidence interval (CI). The crude ORs were derived from the individual numbers of dysphagia in the sarcopenia and non-sarcopenia groups, which was often presented in the tables describing the demographic characteristics of participants.

Quality assessment

The methodological quality of the enrolled studies was independently scored by two authors, the quality of studies included was assessed using a standardized critical appraisal instrument, the Joanna Briggs Institute Meta-Analysis of Statistics Assessment and Review Instrument (JBI-MAStARI) (15, 16). It is widely used for the evaluation of randomized controlled trails and non-randomized controlled trails with respect to selection, comparability and outcome/exposure of the enrolled studies. The item would be scored “0 if it was answered “NO if it was answered “UNCLEAR it scored “1 if the item was answered “YES, it would be scored “2. A higher score indicated a better methodology quality. If the general score is more than 70% of the total, the risk of bias is low. Discrepancies between both reviewers were resolved by discussion or evaluated by the corresponding author.

Statistical analysis

Mata-analysis was attempted for the cross-sectional studies which presented dysphagia and sarcopenia categories. Heterogeneity across the studies was examined by χ2 test. The degree of the heterogeneity was assessed using I2 statistic. Significant heterogeneity was defined as P>0.1 or I2<50% (17). The OR and the 95% CI was analyzed using the random effect model when heterogeneity was high and fixed effects model when heterogeneity was moderate or low (18). The subgroup analysis was conducted based on the different measuring tools of skeletal muscle mass, diagnostic criteria of sarcopenia and assessment tools of dysphagia. We will use funnel plot and Egger test to evaluate the potential publication bias if the number of enrolled studies is more than 10. All the analyses were performed by Comprehensive Meta-Analysis version 2.0 (Biostat, Englewood, NJ, USA), Review Manager 5 (V.5.3., Copenhagen: The Nordic Cochrane Center, The Cochrane Collaboration and StatsDirect) and STATA version 11 (StataCorp LP, College Station, TX, USA).

Results

Results of literature search

The initial literature search identified 323 articles consisting of 58 duplicates, which were discarded. After reading the titles and abstracts, we retained 25 articles for the full-text review. Of these, 1 study had a mistake in the result data, but we haven't get the correct data from the author. 1 study only included the participants who were suspected of having reduced tongue strength due to sarcopenia, 2 studies only enrolled patients with dysphagia, another 11 articles were considered ineligible for lacking of a proper measurement or assessment of sarcopenia, skeletal muscle mass or dysphagia, 1 is a review article. Finally, a total of 9 articles (6, 7, 19, 20, 21, 22, 23, 24, 25) (8 cross-sectional studies (6, 7, 19, 20, 22, 23, 24, 25), 1 cohort study (21)) were included in this systematic review, among which, 5 cross-sectional studies provided the dichotomous classification of sarcopenia and dysphagia were included for the meta-analysis (6, 7, 19, 20, 22) A PRISMA flow diagram of the study selection is presented in Figure 1.

Figure 1.

Figure 1

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Preferred Reporting Items for Systematic Reviews and Meta- Analyses (PRISMA) flow diagram for the study selection process

Characteristics of included studies and participants

The 9 included studies comprised 2033 participants with the mean age ranging from 71.0 to 86.5 years. The proportion of male participants range from 14.29% to 60.24%. As for the targeted population, 5 studies recruited hospitalized older people (6, 7, 19, 21, 23), 1 study recruited cancer patients who require rehabilitation (19) 1 recruited community elderly who require long-term care (20), 1 enrolled community elder patients with Alzheimer's disease (22), 1 study focused on the old people living in a geriatric health services facility (24), and 1 study enrolled home-bound elderly (25). In terms of the measurement of skeletal muscle mass, 8 studies used bioelectrical impedance analysis (BIA) (6, 7, 20, 21, 22, 23, 24, 25), 1 study used the abdominal computed tomography (CT) (19). Regarding the diagnostic algorithm of sarcopenia, skeletal muscle loss was used to diagnose sarcopenia in 4 studies (20, 21, 22, 25), 5 studies adopted European Working Group on Sarcopenia in Older People (EWGSOP) (8) or Asian Working Group for Sarcopenia (AWGS) criteria (26), add low handgrip strength and/or low physical performance as a part of the diagnosed criteria (6, 7, 19, 23, 24). With regards to the assessment tool for dysphagia, 2 studies adopted the Functional Oral Intake Scale (FOIS) (6, 21), 2 studies used the modified water swallowing test (MWST) (20, 22), 1 study used 10-item Eating Assessment Tool (EAT-10) (19), 1 study used Food Intake Level Scale (FILS) (23), 1 study used the video fluoroscopic studies(VFSS) (7), 1 study used the dysphagia severity scale (DSS), the repetitive saliva swallowing Test (RSST) and other assessment tools (24) and 1 study assessed the dysphagia by cervical auscultation (25). The result of the quality assessment for the included studies is listed in Table 1.

Table 1.

Results for the critical appraisal of included studies using the JBI-MAStARI

CitationCross-sectional studies Q1 Q2 Q3 Q4 Q5 Q6 Q7 Q8 Total (%)
Keisuke Maeda (2016) Y Y Y Y Y Y Y Y 100.00
Hidetaka Wakabayashi (2017) Y Y Y Y Y Y Y Y 100.00
Silvia Carrion (2016) Y Y Y Y U U Y Y 87.50
Kohji Murakami (2015) Y Y Y Y Y Y Y Y 100.00
Daisuke Takagi (2015) Y Y Y Y Y Y Y Y 100.00
Yoshihiro Yoshimura (2017) Y Y Y Y Y Y Y Y 100.00
Hiroyasu Shiozu (2015) U Y Y Y U U Y Y 81.25
Keiichiro Sagawa (2015) Y U Y U U U Y Y 75.00
Citation
Cohort studies Q1 Q2 Q3 Q4 Q5 Q6 Q7 Q8 Q9 Q10 Q11 Total (%)
Keisuke Maeda, (2017) Y Y Y Y Y Y Y U Y N Y 86.36
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Y, yes; U, unclear; N, no; NA, not applicable.

Association between sarcopenia and dysphagia

1 cohort study and 3 cross-sectional studies which lack of a dichotomous classification of sarcopenia or dysphagia were retrieved for qualitative synthesis (21, 23, 24, 25). Participants with sarcopenia were shown to have a higher risk of dysphagia or lower swallowing function than those without sarcopenia. One study indicated that participants with lower muscle mass and muscle strength had a lower FILS scores, which is used to classify the severity of dysphagia (23). Another study indicated that swallowing function were significantly lower in the sarcopenia group than in the non-sarcopenia group (24). All these 4 studies presented evidence in favor of a positive association between sarcopenia and dysphagia.

Figure 2 presents the results of comparison of dysphagia incidence between sarcopenia and non-sarcopenia groups. Pooled data of 5 studies (6, 7, 19, 20, 22) with 913 participants showed the risk of dysphagia is higher in sarcopenia groups than that in the non-sarcopenia group. The crude OR of the association between sarcopenia and dysphagia was 6.17 (95% CI, 3.81- 10.00), pooled from all the 5 studies. After adjusting for potential confounders, such as age, sex, Barthel Index score, nutritional status, sarcopenia also have a positive association with dysphagia (adjusted OR, 4.06; 95% CI, 2.27-7.29). Low between-study heterogeneity was noted both for the crude ORs (P = 0.31 and I2 = 15.97%) and the adjusted ORs (P = 0.90 and I2 = 0%), indicating that the finding of studies were highly consistent. We could not evaluate publication bias of these 5 articles, because of the small number of enrolled studies.

Figure 2.

Figure 2

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Forest plot of the (A) crude and (B) adjusted association between sarcopenia and dysphagia

The subgroup analysis showed that the group diagnosed sarcopenia by skeletal muscle loss tended to have a higher crude association (OR, 7.00; 95%CI, 3.82-12.86) than those adopted the EWGSOP or AWGS, diagnosed by loss of muscle mass and reduced muscle strength and/or impaired physical performance (OR, 4.98; 95%CI, 2.25-11.00), and trend remained following adjustment for potential confounders (Figure 3). In terms of the measurements of skeletal muscle mass, the group using BIA to measure the skeletal muscle mass tended to have a stronger association (OR, 7.11; 95%CI, 4.21- 12.02) than the study using abdominal CT (OR, 2.88; 95%CI, 0.85-9.76), and trend remained after controlling for confounders (Figure 4). In addition, the group using FOIS as an assessment tool for dysphagia tended to have a stronger association (OR, 9.68; 95%CI, 2.90-32.33) than those using MWST (OR, 7.00; 95%CI, 3.82-12.86), EAT-10 (OR, 2.88; 95%CI, 0.85-9.76) or VFSS (OR, 3.39; 95%CI, 0.42-27.11), and the trend also remained by the results of adjusted ORs. (Figure 5). But all of the subgroup differences were not statistically significant.

Figure 3.

Figure 3

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Forest plot of the (A) crude association and (B) adjusted association between sarcopenia and dysphagia by subgroup analysis based on diagnostic algorithm of sarcopenia

Figure 4.

Figure 4

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Forest plot of the (A) crude association and (B) adjusted association between sarcopenia and dysphagia by subgroup analysis based on measurement for skeletal muscle mass

Figure 5.

Figure 5

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Forest plot of the (A) crude association and (B) adjusted association between sarcopenia and dysphagia by subgroup analysis based on assessment tool for dysphagia

In addition, sensitivity analysis showed that removing any single study did not alter the results. First, we eliminated a study enrolled cancer patients, it didn't alter the positive association between sarcopenia and dysphagia (crude OR, 7.11; 95%CI, 4.21-12.02; adjusted OR, 4.17; 95%CI, 2.18-7.97). Second, we eliminated a study enrolled patients with Alzheimer's disease, and effect size also didn't change significantly (crude OR, 5.09; 95%CI, 2.98-8.68; adjusted OR, 3.93; 95%CI, 2.08-7.41).

Discussion

The present systematic review was conducted to determine the association between sarcopenia and dysphagia using published studies. The result have shown that sarcopenia was positively associated with dysphagia both in the qualitative synthesis and quantitative analysis. The subgroup analysis further indicated that the studies adopted skeletal muscle loss as the diagnostic criteria of sarcopenia tended to have a higher ORs than those adopted the EWGSOP or AWGS criteria. And the group using bioelectrical impedance analysis to measure the skeletal muscle mass tended to have a stronger association than the study using abdominal CT. In addition, the group using FOIS as an assessment tool for dysphagia tended to have a stronger association than those using MWST, EAT-10 and other tools. Although all of these subgroup differences were not statistically significant.

Sarcopenia has been associated with several potential adverse health outcomes, including cognitive impairment, disability, physical inactivity, depression and mortality (11, 13, 14), the association between sarcopenia and dysphagia has been recognized recently. In 1992, Veldee et al (27) first indicated that malnutrition could change the neuromuscular function in our body, and these changes is associated with dysphagia and aspiration, but the term “sarcopenia was not mentioned. In 1995, Robbins et al (28) found that aging could influence lingual strength and pressure, and the decreased lingual strength and pressure was a risk factor of dysphagia. On the base of the previous stage of research, in 2005, they further indicated that sarcopenia may influence lingual strength, and cause dysphagia accordingly (29). Since then, studies on association between sarcopenia and dysphagia have increased. Keisuke Maeda et al (6) reported that sarcopenia was an independent risk factor for dysphagia among hospitalized older individuals. Nevertheless, Hidetaka Wakabayashi et al (19) later investigate the relationship between sarcopenia and dysphagia in cancer patients, but the power of this study was too low to observe a significant association between them. Thus, based on the inconsistent results among studies and the significance of both health issues, a systematic review and meta-analysis was conducted to investigate the association between sarcopenia and dysphagia.

Our result have shown that sarcopenia was positively associated with dysphagia, according to the results from qualitative synthesis and meta-analysis. It is not surprising that sarcopenia is concomitant with dysphagia, for the reason that there are many known factors relevant to both of them. Aging plays an important role in sarcopenia and dysphagia. On one hand, the structure and function of neuromuscular system suffer from a degenerative change with age, thereby leading to sarcopenia. On the other hand, the swallowing mechanism and function change in older adults with age, leading to dysphagia (12). In addition, inactivity is also a risk factor related to sarcopenia and dysphagia. Physical inactivity can cause disuse atrophy of skeletal muscle as well as swallowing muscles, which can increase the risk of sarcopenia and dysphagia (12, 30). Moreover, malnutrition caused by reduced food intake, poor appetite and reduced nutrient absorption is a significant risk factor for low muscle mass and sarcopenia (10). Type II fibers are affected by malnutrition more easily than type I fibers, therefore, malnutrition could affect swallowing muscles which have moderate to high percentage of type II fibers, leading to dysphagia (12, 28). Some diseases that can cause sarcopenia also can increase the risk of dysphagia, such as Alzheimer's disease and cancer (12, 31).

In the sensitivity analysis, we discarded a study targeting cancer patients, the effect size didn't change significantly. We also eliminated a study enrolled patients with Alzheimer's disease, it also didn't alter the positive association between sarcopenia and dysphagia. As we mentioned above, Alzheimer's disease and cancer can cause sarcopenia also can increase the risk of dysphagia, they can strength the association between sarcopenia and dysphagia. Therefore, the result of sensitivity analysis further improved the credibility of our results and strengthened the possible application of our results to the general population and implied the observation in certain disease groups.

Among the enrolled studies, the group diagnosed sarcopenia by skeletal muscle loss tended to have a higher association than those adopted the EWGSOP or AWGS diagnostic criteria, which diagnose sarcopenia by skeletal muscle loss and reduced muscle strength and/or impaired physical performance, but the difference was not statistically significant. In 2010, EWGSOP presented a practical clinical definition and diagnostic criteria for sarcopenia. They indicated that the parameters of sarcopenia are the amount of muscle and its function, the measurable variables include mass, strength and physical performance (8). Some studies showed that low handgrip strength and nonambulatory status was associated with dysphagia (32, 33), so the association between sarcopenia and dysphagia should be stronger in the group diagnosed sarcopenia by EWGSOP or AWGS diagnostic algorithm. But our result is contradict to these facts, the possible reasons are the different participant characteristics and assessment tools for dysphagia and skeletal muscle mass in each study.

The subgroup analysis also showed that different measurements of skeletal muscle mass might vary the association between sarcopenia and dysphagia, although the difference was also not statistically significant. CT and MRI are golden standards for measuring skeletal muscle mass, but they are used only occasionally because of its high expense and radiation exposure (34). Bioelectrical impedance analysis (BIA) is widely used in medical researches with the advantages of low cost and strong operability, it has been mostly used in body composition analysis as an alternative to CT and MRI (35). Our result indicated that the group using BIA to measure the skeletal muscle mass tended to have a stronger association than the study using abdominal CT. One possible reason is that the skeletal muscle mass measured by BIA is through calculation from an equation stored in the instrument in advance. This equation includes body mass index (BMI), reactance, electric resistance and some other parameters of body. In the equation, the skeletal muscle mass is proportional to BMI. Therefore, the patients with a lower BMI tend to have a decreased skeletal muscle mass measured by BIA, and they are prone to be categorized as sarcopenia (36). A lower BMI is also a possible risk factor and feature of dysphagia (37). Therefore, more participants with dysphagia were diagnosed with sarcopenia. This probably explains why the association between sarcopenia and dysphagia was stronger in the group using BIA to measure the skeletal muscle mass. The study using the abdominal CT had an extraordinary low ORs, we believe that CT is not the only cause of the outlier value, we should take the participant characteristics, diagnostic criteria of sarcopenia and assessment tools for dysphagia into account. Besides, there was only one study using abdominal CT to measure the skeletal muscle mass, the small number is not representative.

In our result, we didn't find significant difference in the ORs among the studies using the different assessment tools for dysphagia, although there were some differences between them. As for the assessment tools for dysphagia, videofluoroscopy swallowing study (VFSS) is considered the gold standard for diagnosing and assessing swallowing disorders (38). Furthermore, screening tests are designed to be faster, relatively noninvasive, and pose little risk to patients, while identifying the signs or symptoms of dysphagia needed for diagnosis, such as the Eating Assessment Tool (EAT-10) and 3-ounce water swallow test (39, 40). Besides, there are also some tools focus on the functional impact of dysphagia symptoms on the oral intake of food and liquid, such as Functional Oral Intake Scale (FOIS) and Food Intake Level Scale (FILS) (41). In our results, the group using EAT-10 had an extraordinary lower OR, we think that EAT-10 is not the main cause of the lower value because the study in this group also diagnosed sarcopenia by AWGS diagnostic algorithm and used abdominal CT to measure the skeletal muscle mass. And the group using FOIS tended to have a stronger association than those using the other tools, for the reason that one study in this group enrolled hospitalized patients who had restricted oral intake, nil per os is a risk factor for sarcopenia and dysphagia (42), so it can strengthen the association between them.

Our meta-analysis also pooled the adjusted OR, which indicated the independent association between sarcopenia and dysphagia. Although aging and malnutrition are the common risk factors of sarcopenia and dysphagia, our results showed that dysphagia in old patients with sarcopenia could not be entirely explained by aging or malnutrition, sarcopenia may cause dysphagia directly. The possible reason is the generalized decline of muscle mass and muscle strength in elder people with sarcopenia, which can coincide with weakening of the muscles related to swallowing, such as tongue muscle, mylohyoid muscle, genioglossus muscle, palatopharyngeus muscle, and so on. These may contribute to decreased tongue strength, reduced range of tongue motion, weak contractility of pharyngeal muscle and reduced endurance of muscles related to swallowing (6, 43), all of these changes might increase the risk of dysphagia.

We acknowledge that the meta-analysis had several limitations. First, all of the enrolled studies are cross-sectional design, we could not clarify the causal relationship between sarcopenia and dysphagia. Second, only 5 studies incorporated in meta-analysis, and the included studies used different diagnostic criteria of sarcopenia and various assessment tools for dysphagia and skeletal muscle mass, these lead to betweenstudy heterogeneity and poor comparability in subgroup analysis. Third, publication bias could not be measured due to the small number of enrolled studies. Fourth, the potential confounders adjusted in each study were varied. So, uniform variables were suggested to use in future researches.

In conclusion, our systematic review and meta-analysis showed that dysphagia was significantly more prevalent in participants with sarcopenia compared with those without sarcopenia, and their association still remained after controlling for potential confounders like age, sex, malnutrition and activities of daily living. However, the causal relationship requires more prospective cohort study for confirmation.

Conflicts of interest

There is no potential conflicts of interest with respect to the research, authorship, and publication of this article.

Ethical standard

The study was approved by the Research Ethics Committee for Sichuan University.

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