https://orcid.org/0000-0002-3552-9153
Abstract
To investigate the effects of non-pharmacological treatments on sarcopenic obesity (SO).
A search for randomized controlled trials (RCTs) on SO was conducted in PubMed, Web of Science, CINAHL, CENTRAL, SPORTDiscus, CNKI, Wanfang and VIP. A meta-analysis was conducted using random-effects models for MDs.
The meta-analysis on 21 RCTs showed that exercise improved PBF (MD: −1.67%, p < .01, I2 = 35%), grip strength (MD: 2.2 kg, p = .03, I2 = 61%), GS (MD: 0.08 m/s, p = .02, I2 = 0%), TCR (MD: 2.22 repetitions, p < .01, I2 = 0%), TUG (MD: −1.48 s, p < .01, I2 = 61%), UE strength (MD: 1.88 kg/kg, p < .01, I2 = 0%) and LE strength (MD: 2.19 kg/kg, p < .01, I2 = 0%). Nutritional interventions improved grip strength (MD: 1.52 kg, p < .01, I2 = 0%). Combine interventions improved PBF (MD: −1.97%, p < .01, I2 = 38%), ASMM (MD: 0.4 kg, p < .01, I2 = 6%), grip strength (MD: 1.83 kg, p < .01, I2 = 38%) and GS (MD: 0.04 m/s, p < .01, I2 = 0%). Combined interventions were more effective than nutrition alone for reducing PBF (MD: −0.8%, p = .05, I2 = 0%).
The effects of exercise and nutrition interventions on SO are limited individually, especially regarding muscle mass, but their combination can yield optimal results. Additionally, physical therapy also demonstrated some potential.
Key Points
Exercise is crucial for sarcopenic obesity (SO) patients.
Nutrition intervention exhibited limited effect in improving SO.
Combining exercise and nutrition can achieve better results in SO management.
Physical therapy showed some potential while requiring more related evidence.
Introduction
Sarcopenic obesity (SO) is characterized by the simultaneous presence of sarcopenia and obesity [1]. Its diagnosis criteria are based on the assessment of muscle and fat mass. Specifically, individuals who are classified as obese (BMI >30 kg/m2 or body fat percentage > 30%) and have a skeletal muscle mass index (SMI) that is two standard deviations below the average SMI of reference groups can be diagnosed with SO [2–4].
To date, the prevalence of SO has reached 10 ~ 27% worldwide [5] and primarily occurs in individuals older than 65 years, possibly due to age-related accumulation of abdominal fat and muscle weakness [1, 6–9]. However, recent evidence has suggested an increasing age range for this condition [10], which has raised alarms for public health. Owing to the cumulative effects of obesity and sarcopenia, SO is distinctively correlated with many chronic diseases, such as osteoporosis [11], type 2 diabetes mellitus [12] and cardiovascular diseases [13], thereby increasing the risk of physical disability and mortality among the affected population [14]. Furthermore, specific clinical cohorts, such as cancer patients [15, 16], or those with orthopaedic disease [17], are prone to SO, leading to impaired recovery and quality of life.
Given the threat of SO, many attempts have been made to explore possible treatment strategies. Currently, there are no approved medications for treating SO, making non-pharmacological interventions primary and recommended option [18–21]. Specifically, exercise and nutrition are the most predominant non-pharmacological interventions [22]. To date, a few systematic reviews have investigated interventions for the overall health of SO patients. However, these reviews have primarily focused on exercise and nutritional interventions and considered primary outcomes of SO, such as muscle mass, fat mass and grip strength [21, 23], while other health aspects of SO patients, such as general physical and physiological outcomes, have been rarely addressed. Considering this, we conducted a systematic review to evaluate the overall effects of non-pharmacological interventions on SO patients, with a focus on approaches beyond exercise and nutritional intervention.
Methods
This systematic review followed the Preferred Reporting Items for Systematic Review and Meta-analysis (PRISMA) guidelines [24] and was registered with PROSPERO (CRD42023468710).
Searching strategy
Web of Science, PubMed, SPORTDiscus (EBSCO), CINAHL, Cochrane Central Register for Controlled Trials (CENTRAL), China National Knowledge Infrastructure (CNKI), Wangfang database, China Science and Technology Journal (VIP) Database were searched for relevant studies published in English and Chinese and up to March 2024, using MeSh terms and free text, including ‘sarcopenic obesity’, ‘sarcopeni*’, ‘obes* or overweight’, ‘adipo*’. We set no restrictions on the interventions used or the publication date.
Study selection: inclusion and exclusion criteria
Two reviewers independently screened the titles and abstracts according to the inclusion and exclusion criteria. Subsequently, the full text of the remaining records was assessed, and all the eligible studies were then independently evaluated by the third reviewer.
The inclusion criteria were based on the ‘PICOS’ (population, intervention, comparator, outcome and study) approach [25]:
Population (P): Patients with SO or sarcopenic overweight (with clear diagnostic evidence) and without other significant diseases. Measurements for sarcopenia include SMI, appendicular muscle index (AMI) or appendicular skeletal muscle mass (ASM). Measurements for obesity include body mass index (BMI), percentage of body fat (PBF).
Intervention (I): All types of non-pharmacological interventions, including, but not limited to, exercise, nutritional interventions and multifactorial interventions.
Comparator (C): placebo, or no intervention (blank control).
Outcome (O): Anthropometric measurements (e.g. skeletal muscle mass, percentage body fat, waist circumstance), physical capacity (e.g. muscle strength, gait speed) and other relevant indicators (e.g. physiological indicators such as blood pressure, biomarkers.)
Study (S): Randomized controlled trials (RCTs) or cluster RCTs published in peer-reviewed journals.
Data extraction
The following data were extracted: (1) Study characteristics: author, publication year, country/region and study design; (2) Participants: sample size and characteristics; (3) intervention: description of the intervention, including dose, frequency and duration; (4) Comparison: description of the control group; (5) Outcomes and their variations: sarcopenia outcomes according to EWGSOP [26] and AWGS [27], mainly including muscle mass, muscle strength and physical capacity. Obesity primary outcomes mainly include body composition and waist circumstance. Additionally, other covariate measures (e.g. serum biomarkers) were also extracted.
Risk of bias
The Physiotherapy Evidence Database (PEDro) [28, 29] scale was utilized to assess the risk of bias. The process was conducted independently by two reviewers. Any discrepancies were resolved by a third reviewer.
Data analysis and synthesis
The data analysis was conducted using Review manager 5 (The Cochrane Collaboration, London, UK). Mean differences with 95% CIs were used to determine the effect size, and random-effects models were employed to pool the data. Heterogeneity was tested using chi-square and I2 statistic. For studies employing several similar interventions within one trial, the data were merged across the groups for comparisons (See Appendix 1 in the Supplementary Data section for the full details of the formulars). Descriptive analysis was performed when the data synthesis was not applicable.
Quality of evidence
The quality of scientific evidence was evaluated by two reviewers using the Grading of Recommendations, Assessment, Development and Evaluation (GRADE) system [30].
Sensitivity analysis
For analyses involving at least three studies and demonstrating substantial heterogeneity, a sensitivity analysis using the leave-one-out (LOO) method was employed to check the robustness of the main results.
Results
Study selection
A total of 18,837 articles were identified through the literature search. After further screening, 21 studies [11, 31–50] were included in the systematic review, of which 18 studies were included in the meta-analysis (Figure 1).
PRISMA Flowchart showing the search and selection of studies.
Characteristics of studies included
Article details are summarized in Table 1 (See Appendix 2 in the Supplementary Data section for the full details of Table 1). The included studies were published between 2014 and 2023 and in the United States [46], Brazil [35, 38, 44, 48], Japan [45], South Korea [37], Germany [39, 50], Canada [34], France [49], Iran [11], Lebanon [33], China mainland [32, 36, 47] and Taiwan [31, 40–43]. A total of 1453 participants (950 females and 503 males) were included, aged from 60 to 90.
The outcomes can be categorized into anthropometric [51], physical capacity [52] and physiological indicators.
The main anthropometric indicators included weight [11, 31, 32, 34, 40, 44, 45, 49], waist circumstance [32, 35, 37, 49], percentage of body fat [11, 31–33, 35–37, 39–44, 46–48, 50], body fat mass [32, 34, 35, 40, 45, 49], appendicular skeletal muscle mass [36, 37, 39, 40, 45, 49], appendicular muscle index [33, 34, 41, 47], appendicular lean mass [41, 43], lean body mass [36, 49], skeletal muscle mass [32, 40, 48], total fat free mass [42, 44] and bone mass density [11, 36, 43, 48].
The main physical capacity indicators included grip strength [32, 37, 40, 42, 43, 45, 46, 49, 50], knee extension strength [35, 38, 40, 45], gait speed [32, 41–43, 45], timed up-and-go test and timed chair rise [41–43], upper extremity and lower extremity [41, 42], short physical performance battery [32, 38, 46] and the Medical Outcomes Study Questionnaire 36-Item Short Form [32, 38, 41].
The main physiological indicators included C-reactive protein [31, 34, 37, 45], triglycerides [31, 34, 37, 45], total cholesterol [34, 37, 45], high-density lipoprotein and low-density lipoprotein [31, 34, 37], systolic blood pressure and diastolic blood pressure [37, 45] and interleukin-6 [34, 45].
Interventions of studies included
Exercise was the most employed intervention (See Appendix 3 in the Supplementary Data section for the full details of table 2), such as resistance training (RT) [11, 31, 34, 35, 38, 40–44, 46, 48], aerobic training (AT) [40] and combined training (CT) [36, 37, 40, 45]. The duration of exercise interventions ranged from 8 weeks [40] to 48 weeks [33], with individual sessions lasting between 40 min [46] to 75 min [41]. Elastic bands were the most popular tool for training [31, 37, 41, 43, 45]. Progressive protocols were used in 12 studies [11, 35–41, 44, 45, 48, 50]. For RT interventions, the percentage of one-repetition maximum [34, 38, 40, 44, 46] and the rate of perceived exertion (RPE) [11, 31, 36, 37, 39, 41–43, 50] were used to evaluate exercise intensity. The intervention typically included 8 to 12 exercises targeting major muscle groups, with each exercise performed in 1 to 3 sets of 8 to 12 repetitions [31, 37, 40–44, 46]. For AT interventions, only one study [36] reported the intensity of exercise, measured by the percentage of maximum heart rate (HRmax). The AT methods included cycling [45], dancing [40] and walking [36, 37].
Nutritional supplementation was also a common intervention [32–34, 39, 45, 47, 49, 50]. Amino acids (or protein) [32, 34, 39, 45, 47, 50] and vitamin D or cholecalciferol [33, 45, 49, 50] were the main supplements. The duration of nutritional interventions ranged from 12 weeks [47, 48] to 48 weeks [33]. The studies either provided nutritional supplementation postexercise or daily. Beside exercise and nutritional supplementation, one study reported the use of electrical acupuncture [47], which was categorized as a form of physical therapy.
Risk of bias
Scores on the PEDro scale ranged from 5 to 10 for the included studies (See Appendix 4 in the Supplementary Data section for the full details of table 3). Two studies [36, 37] demonstrated fair quality; 14 studies [2, 30, 37–47, 49] demonstrated good quality; and five studies [32–35, 49] were of excellent quality.
Effects of non-pharmacological interventions on SO
Exercise vs. control
For anthropometric indicators, exercise interventions only decreased PBF (MD = −1.67%, p < .00001, 95% CI: −2.4–−0.93, I2 = 35%) when compared to control groups (Figure 2). For capacity indicators, exercise interventions increased grip strength (MD = 2.2 kg, p = .03, 95% CI: 0.22–4.19, I2 = 61%), GS (MD = 0.08 m/s, p = .02, 95% CI: 0.01–0.14, I2 = 0%), TCR (MD = 2.22 repetitions, p = .001, 95% CI: 0.89–4.19, I2 = 0%), UE (MD = 1.88 kg/kg, p = .005, 95% CI: 0.57–3.18, I2 = 0%), LE (MD = 2.19 kg/kg, p < .00001, 95% CI: 1.82–2.55, I2 = 0%) and a significant decrease in TUG (MD = −1.48 s, p = .0001, 95% CI: −2.24—−0.72, I2 = 61%) when compared to control groups (Figure 3). For physiological indicators, no significant changes were observed (Figure 4).
The differences in anthropometric indices between the exercise and control groups.
The differences in physical capacity indices between the exercise and control groups.
The differences in physiological indices between the exercise and control groups.
Nutritional intervention vs. control
For anthropometric indicators, nutritional interventions failed to change any of these indicators compared to the control groups (Figure 5). For physical capacity indicators, nutrition interventions significantly improved grip strength (MD = 1.52 kg, p < .0001, 95% CI: 0.98–2.06, I2 = 0%) compared to control groups.
The differences in measured indices between the nutritional intervention and control groups.
Exercise & nutritional intervention vs. control
For anthropometric indicators, exercise & nutritional interventions decreased PBF (MD = −1.97%, p < .0001, 95% CI = −2.68—−1.26, I2 = 38%) and increased ASM (MD = 0.4 kg, p = .005, 95% CI: 0.12–0.67, I2 = 6%), handgrip strength (MD = 1.83 kg, p = .008, 95% CI: 0.48–3.18, I2 = 38%), and gait speed (MD = 0.04 m/s, p = .0001, 95% CI: 0.02–0.06, I2 = 0%) compared to the control groups (See Appendix 5 in the Supplementary Data section for the full details).
Exercise vs. nutritional intervention
Only one study [45] compared the effects of exercise and nutritional intervention (See Appendix 6 in the Supplementary Data section for the full details of Table 4), which reported that the exercise intervention significantly reduced BFM, BFM, AFM, trunk FM, leg FM, walking angle and leptin level, while significantly increased arm muscle mass, leg muscle mass, knee extension strength, stride, step length and step count.
For nutritional intervention, there were significant increases in arm muscle mass, leg muscle mass, knee extension strength and VD level, and significant decreases in BFM, BFM, AFM, trunk FM, leg FM, waking speed and leptin level.
Compared to nutritional intervention, exercise was more beneficial for improving stride ability. Conversely, nutritional intervention was more effective in increasing VD level.
Exercise vs. exercise & nutritional intervention
No significant differences were observed between the exercise and combine interventions (see Appendix 7 in the Supplementary Data section for the full details).
Nutrition vs. exercise & nutritional intervention
Exercise & nutritional interventions increased PBF compared to nutrition interventions (MD = 0.8%, p = .05, 95% CI: 0.00–1.61, I2 = 0%) (see Appendix 8 in the Supplementary Data section for the full details).
Nutritional intervention vs. physical therapy & nutritional intervention
Only one study [47] included nutritional intervention and the combined ‘physical therapy (electrical acupuncture) & nutrition’ intervention. The study showed that both interventions significantly improved PBF and SMI (labelled as ASM/H2 in Figure 2) after 4 weeks of interventions (p < .05). Additionally, the effects appeared to consistently improve throughout the intervention period (p < .001). However, the difference between the groups was not reported in this study.
Effects of different exercises
Three studies [40, 46, 48] compared different exercises. However, a meta-analysis was not applicable due to varied experimental settings.
Balachandran et al. [46] compared the effects of high-speed circuit training and hypertrophy training on the physical capacity in adults with SO. After 15 weeks of training, high-speed circuit training significantly improved SPPB (p < .05), power of leg press and chest press, 1RM of chest press, sit-to-stand speed and pan carry speed. The hypertrophy training resulted in statistically significant improvements (p < .05) in leg and chest press power, leg and chest press 1RM, jacket-on speed, scarf pick-up speed and pan carry speed. However, a statistically significant difference (p < .05) was only observed in leg press power.
Chen et al. [40] compared the effects of RT, AT and CT, and found that AT (40 ± 4.4% to 39 ± 4.6%) and RT (39.7 ± 5.6% to 38.7 ± 6.4%) decreased PBF more significantly (p < .05) than CT. For handgrip strength and knee extension strength, RT increased handgrip strength (20.0 ± 7.0 kg to 23.5 ± 7.3 kg) and knee extension strength more than AT and CT (p < .05), with CT being more effective than AT (p < .05). Regarding IGF-1, CT exhibited a more significant improvement than RT (p < .05).
In the study by Cunha [48], the effects of RT with different sets were compared. The results demonstrated that both 1-set and 3-set RT improved total strength and SMM. However, only 3-set RT successfully decreased PBF. Furthermore, 3-set RT was more effective in improving muscular strength and PBF than AT (p < .05).
Effects of different nutritional interventions
Only one study [33] compared the effects of different nutritional interventions. This study investigated the impact of varying doses of VD supplementation on the improvement of SO. The results demonstrated that subcutaneous adipose tissue area decreased significantly (p < .05) in both the low-dose group (461 ± 41.7 cm2 to 302 ± 46 cm2) and the high-dose group (476 ± 38.1 cm2 to 367 ± 31 cm2). However, ALMI decreased in the high-dose group only (7.7 ± 0.1 kg/m2 to 7.5 ± 0.17 kg/m2).
Assessment of evidence quality
Table 5 (See Appendix 9 in the Supplementary Data section for the full details of Table 5) showed the quality assessment. Due to the nature of exercise interventions, there is relative high risk of bias related to blinding in all the included studies. Consequently, the quality of evidence ranged from ‘very low’ to ‘moderated’.
Sensitivity analysis
The effect of exercise on the grip strength was accompanied by significant heterogeneity (I2 = 61%). The LOO method revealed that the study by Kim et al [45]. was the primary source of heterogeneity. After removing this study, the heterogeneity was eliminated, and the result did not change substantially. The details are provided in Supplementary file: Appendix 10.
Discussion
This systematic review examined the effects of the non-pharmacological interventions on the overall health of SO population. We found that exercise, nutritional intervention, and their combination are the most common interventions. Our core findings suggest that exercise may reduce obesity and improve physical capacity, while nutritional intervention may improve grip strength. Their combined interventions appear to benefit muscle mass. These findings offer insight into the therapy on SO.
Effects on anthropometric indicators
Exercise exhibited a significant advantage in improving PBF, the primary outcome of obesity. According to EASO Physical Activity Working Group, AT, RT and CT can all reduce obesity [53]. However, exercise demonstrated limited efficacy in improving the primary indicators of sarcopenia, such as ASM, SMI or SMM. This aligns with two previous reviews [21, 23] that reported no significant changes in ASM and muscle mass after exercise. Given the current evidence, exercise can help improve obesity status in SO individuals but shows modest effect in managing sarcopenia.
We found no distinct results for nutritional interventions. However, we cannot conclude the ineffectiveness of nutritional interventions, as the included supplements (VD and amino acids) primarily focused on muscle growth and maintenance rather than fat mass reduction. To our knowledge, there are limited nutritional interventions specifically targeting obesity in SO individuals, despite nutrition being vital for both sarcopenia and obesity [54]. Sarcopenia correlates with inadequate nutritional intake, whereas obesity results from excess energy consumption [55]. This difference complicates the design of effective nutrition strategy for SO. Precisely for this reason, we believe that developing nutrition strategies to concurrently address sarcopenia and obesity is critical.
The combination of exercise and nutrition showed a positive impact on ASM, likely due to the improved balance, which is essential for hypertrophy [56]. Evidence has demonstrated that protein supplementation with exercise can enhance net protein balance, promoting muscle growth even in older adults [57]. Furthermore, the combined intervention effectively improved the obesity in SO patients. These findings suggest that the combination of exercise and nutrition is an effective approach for managing SO.
Effects on physical capacity
We compared the effects of exercise on physical capacity indicators with control groups, and found that exercise significantly improved GS, TCR, TUG, UE and LE. These findings extend the results of Hsu et al. [58], who only investigated grip strength and GS. However, it is notable that these improvements are not consistent with the null results in muscle mass mentioned earlier, highlighting a potential disconnect between muscle function and muscle growth. Study by Loenneke et al. suggested that muscle function and muscle size can vary independently [59]. Thus, exercise may enhance physical capacity without increasing muscle mass. It is also notable that the study by Kim et al [45] introduced some heterogeneity, reporting a slight, statistically non-significant decrease in grip strength (−0.1 ± 2.2 kg). Kim et al. suggested that the focus on lower-limb training programs was the main reason for this phenomenon. Nonetheless, this discrepancy did not lead to substantial change in the overall effect.
Nutrition interventions independently improved grip strength in our review, contrasting with Yin, et al [21]. This discrepancy may be explained by differences in the nutritional supplements used. Yin’s study specifically focused on calorie intake, whereas our review included amino acid and VD. Additionally, our results showed that combining exercise and nutrition improved both grip strength and gait speed. These findings highlight the benefits of combining exercise and nutritional strategies to enhance the physical capacity in both upper and lower limbs.
Effects on physiological indicators
Only two RCTs investigated the physiological indicators, with no significant changes observed. The included studies mainly focus on cardiovascular health indicators, such as TC [60], TG [61], SBP and DBP [62], possibly due to the fact that both obesity and sarcopenia in older adults are closely associated with cardiovascular diseases [63]. However, we noticed that the included studies placed little emphasis on factors related to muscle growth (e.g. testosterone, growth hormone and irisin) [64, 65] and fat metabolism (e.g. leptin and adiponectin) [66, 67]. Investigating these indicators may clarify the mechanisms behind improvements in SO. Overall, our results suggest that current research on non-pharmacological interventions for SO’s physiological mechanisms related is insufficient and warrant more targeted outcomes.
Limitation and future directions
The primary limitation of this systematic review is the low quality of evidence. According to the GRADE evaluation, the quality of evidence is from ‘very low’ to ‘moderated’, which undermines our confidence in the robustness of the findings.
Secondly, some RCTs employed various indicators (e.g. ASMM, ALST, ALM and AFFM for muscle mass), resulting in a limited number of studies for meta-analysis. This restricts the strength of evidence and further analysis (e.g. meta-regression). Therefore, cautious must be exercised when interpretating our findings.
Additionally, although some studies [40, 46, 48] suggested that CT or high-volume RT protocols (e.g. 3-set RT protocols by Cunha et al. [48]) may be optimal for SO individuals, we recommend further comparisons of different exercise modalities to provide higher-quality evidence for optimal strategies. Similarly, exploring a wild range of nutritional supplementation is also advised in future studies, as different types may impact outcomes in SO.
Moreover, although this review included 21 studies, fewer than 10 studies were included for meta-analysis. According to the Cochrane Handbook for Systematic Reviews of Interventions (https://training.cochrane.org/zh-hans/cochrane), assessing publication bias is of limited value in such small samples. Therefore, although we tested for publish bias using funnel plots (see Appendix 11 in the Supplementary Data section for the full details), the results cannot be reliably interpreted.
Conclusion
By integrating the existing evidence related to SO, we found that exercise, nutrition and their combination are the most common non-pharmacological interventions. When implemented separately, exercise primarily reduced obesity and improving physical capacity, while nutritional intervention mainly improves grip strength, with both showing limited effects on muscle mass. However, the combination of the two might lead to improvements in muscle mass, making it an optimal choice for SO patients. Specifically, CT or high-volume RT with amino acids or vitamin D may be effective.
Declaration of Conflicts of Interest:
None declared.
Declaration of Sources of Funding:
This study was supported by National Social Science Fund of China (21BTY092) and Chongqing Doctoral Research Innovation Project (CYB240087).
Comments