The relationship between muscle strength and quality with functional performance in women mid- to long-term after Roux-en-Y gastric bypass

Abstract

BACKGROUND:

The reduction of muscle mass and strength commonly observed after bariatric surgery might negatively affect the individual physical function. Muscle quality is also of functional relevance in different populations, but its significance in patients who underwent bariatric surgery has yet to be explored.

OBJECTIVE:

To examine the association between muscle strength and quality with physical function in women mid- to long-term after Roux-en-Y gastroplasty (RYGB).

METHODS:

In this cross-sectional study, 133 women (43.7 $\pm$ 9.9 years) who have undergone RYGB at least two years before the study were included. All participants underwent body composition evaluation using DEXA and knee extensors peak moment (PM) using an isokinetic dynamometer. Muscle quality (MQ) was obtained through the ratio between absolute PM and dominant leg fat-free mass. Physical function was measured through the 30-second sit-to-stand (30-STS), 6-minute walking (6-MWT), and timed up-and-go (TUG) tests.

RESULTS:

Differences between PM tertiles were observed for 30-STS and 6-MWT tests. However, statistical significance disappeared when adjusting for age. Regarding PM relative to body weight, all functional tests were significantly different between tertiles. Comparing functional performance according to MQ tertiles, differences were found for 30-STS and 6-MWT tests, but significance disappeared when adjusting for age. Absolute PM was correlated to the 30-STS performance and 6-MWT, while PM relative to body mass and MQ were correlated with all functional tests.

CONCLUSIONS:

Muscle strength and quality seem to be associated with physical function in women mid-to-long-term after RYGB, but strength relative to bodyweight outperformed absolute strength and MQ.

Keywords

Obesity bariatric surgery physical function skeletal muscle

1. Introduction

Obesity is a multifactorial condition well documented to be associated with a wide range of negative clinical outcomes, reduced physical function, and mortality [1, 2, 3, 5]. Despite a plethora of evidence demonstrating the urgent need for effective preventive and therapeutic strategies, the obesity pandemic is rapidly increasing worldwide [6, 7] and is currently responsible for a large fraction of public healthcare costs [8]. Lifestyle modifications are usually the first-line treatment for people with overweight and obesity while pharmacologic therapy may be used in selected patients as an adjunct. However, given the relatively low success rate of nonpharmacological and pharmacological therapies in patients with severe obesity, the number of bariatric surgeries has rapidly increased over the last decades [1, 2, 3, 4]. Of note, one of the most commonly implemented surgery techniques in recent years is the Roux-en-Y gastric bypass (RYGB), a restrictive and malabsorptive procedure [4, 6, 9].

Surgical intervention is indicated for patients with severe obesity (i.e., BMI $>$ 40 kg/m²), or those with BMI greater than 35 kg/m² with comorbidities, when lifestyle changes and pharmacological therapy have failed to induce weight loss [4, 6, 10]. Bariatric surgery is widely considered the most effective intervention for obesity treatment, given the fact it induces large and persistent weight loss and reduces obesity-related comorbidities and mortality, independent of the performed surgical technique [4, 6, 10, 11, 12, 13]. However, the profound weight loss observed as result of bariatric surgery is not solely from fat mass, since a substantial loss of fat-free mass (FFM), particularly skeletal muscle, is also observed [2, 9, 14]. In this regard, a recent meta-analysis revealed that more than 8 kg of lean body mass on average is lost within one-year post-surgery [2]. When accompanied by muscle strength reduction, it raises the concern as to whether lean body mass loss would negatively affect patients’ functional performance [15, 16]. In fact, Alba et al. (2018) reported that, when compared to preoperative values, both lean mass and handgrip strength are significantly reduced 12 months after RYGB [9]. Moreover, these authors demonstrated that individuals with greater absolute or relative muscle strength had faster gait speed and five times sit-to-stand performance.

While reduced muscle strength has been traditionally associated with poor functional performance, recent evidence indicates that muscle quality is also of important functional relevance [17, 18, 19, 20]. It has been demonstrated that fat accumulation within skeletal muscle, a marker of poor muscle quality, is associated with reduced muscle strength and function [20, 21, 22]. A recent report showed that individuals with obesity present a high prevalence of poor muscle quality [23]. Muscle quality has been typically defined as muscle moment per unit of muscle mass, and the ratio of muscle moment to mass (i.e., specific moment) and has been used as a measure of muscle quality in numerous studies [22]. Nevertheless, Shaffer et al. (2017) found that muscle quality did not outperform muscle strength measures in the prediction of physical function in older individuals [22]. The functional significance of muscle quality in individuals after bariatric surgery, however, has yet to be determined, particularly in the mid- to long-term follow-up, a period for which scarce data exist [24, 25]. Thus, it is unclear whether muscle quality, a measure that relies on expensive image equipment, such as dual-energy x-ray absorptiometry (DXA), is more strongly associated with functional performance than muscle strength in this population. Therefore, the purpose of the present study was to examine the association between muscle strength and quality with functional performance in women mid- to long-term after RYGB surgery.

2. Materials and methods

2.1 Subjects

This is a cross-sectional study, where adult women (18–60 years) who were at least two years post-RYGB were eligible for the present study and were invited to participate through posters and social media announcements. All individuals answered a face-to-face questionnaire addressing medical history, co-morbidities, medications use, and lifestyle habits. Patients with diabetes mellitus, heart disease, hormones or appetite regulator use, severe psychiatric disorders, recent elective surgery, and current pregnancy or breastfeeding were excluded. Individuals who used protein supplementation regularly and those who engaged in physical exercise for at least 2 months before the study were also excluded. After exclusion criteria were applied, a total of 133 women underwent all the study assessments and were thus enrolled in the analyses. Written informed consent was obtained from each participant and the study procedures were approved by the institutional review board of the University of Brasilia (protocol # 2052734/2019).

2.2 Muscle strength assessment

Quadriceps PM was assessed using an isokinetic dynamometer (Biodex 3, Biodex Medical, Inc., Shirley, NY, USA) as a measure of muscle strength. In brief, after a warm-up involving two sets of 10 repetitions at sub-maximal effort, the testing protocol consisted of two sets of four knee extensors contractions at 60^∘s^{- 1} with 60 s rest intervals between sets. The recorded value was the single quadriceps contraction that elicited the highest PM throughout the protocol, which was analyzed in absolute values and relative to body weight.

Following a detailed explanation of the procedures, patients were carefully positioned at the dynamometer seat so that the rotation axis of the equipment arm was aligned with the lateral condyle of participants’ dominant femur. Arms were positioned crossed over the chest and velcro belts were used at the trunk, pelvis, and thigh to avoid possible compensatory movements. Patients were instructed to perform the test with their maximal effort while verbal encouragement was systematically provided. Calibration of the equipment was performed according to the manufacturer’s specifications before every testing session.

2.3 Body composition evaluation

Standard procedures were used to gauge weight with 0.1kg precision, and height was measured at the nearest 0.1 cm with a stadiometer. Body mass index (BMI) was derived as body weight divided by height squared (kg/m²). Body composition was assessed using DXA (lunar model 8743, GE Medical Systems, USA). For the procedure, patients laid face up on the DXA table with body carefully centered. Besides whole-body composition, regional measurements (arms, legs, and trunk) were determined based on bone landmarks, with vertical boundaries separating the arms from the body at the shoulder, and angled boundaries separating the legs from the trunk at the hips. Of note, dominant leg FFM was subsequently used to calculate muscle quality (please see below). All measurements were carried out by the same trained technician and the equipment was daily calibrated according to the manufacturer’s specifications. Coefficients of variation were 0.9% for FFM and 1.9% for fat mass in our laboratory.

2.4 Muscle quality

The strength generated per unit of muscle mass (i.e., specific moment) was derived and considered as the measure of muscle quality. In this regard, the PM of the dominant side quadriceps was taken as the muscle strength variable while FFM of the same limb was the variable of muscle mass. Thus, muscle quality was evaluated as the ratio between quadriceps PM (in Nm) and leg FFM (in kg) and expressed in Nm/kg.

2.5 Physical function assessment

For physical function evaluation the timed up-and-go test (TUG), 6-min walk test (6-MWT), and 30-s sit-to-stand test (30-STS) were performed by all participants. The same trained researcher implemented the tests and fully explained the procedures before the assessment. For the TUG, after a familiarization trial, patients were seated in a standard chair with a height of 46 cm, both arms resting alongside the body, and both feet completely resting on the floor at approximately the same distance from their shoulders and were instructed to, on the word “go,” get up and walk 3 m forward, as fast as possible (but without running), turn around a cone, return to the chair and sit down again. The best performance of three attempts was recorded, with 60 s of rest between attempts.

The 6-MWT was conducted using a circuit of 45.72 m in length, with cones placed every 4.57 m. Patients were instructed to walk at their own pace to cover as much distance as possible in 6 min, without running. The covered distance, in meters, was considered for the analyses. Finally, for the 30-STS, patients were instructed to, with their arms crossed over their chest, fully stand up and sit down as many times as possible within 30 seconds. The test was implemented using a standard chair (46 cm) and only the complete repetitions were recorded.

2.6 Statistical analyses

Descriptive data are expressed as mean and standard deviation unless otherwise noted. Data distribution was examined using the Kolmogorov-Smirnov test. Pearson correlation coefficients were used to verify the relationship between independent (i.e., muscle strength and quality) and dependent variables (i.e., functional performance). Also, tertiles were calculated for muscle strength (both absolute and relative to body weight) and quality, and patients were grouped according to these tertiles. One way ANOVA adjusted for age was performed to compare physical function performance among tertile groups. If significant contrasts between tertiles were noted, Tukey’s multiple comparisons tests were performed to identify differences between specific pairs of groups. The significance level was set at $p<$ 0.05, and all analyses were conducted using the Statistical Package for Social Sciences (SPSS 26.0, IBM Corp., Armonk, NY, USA).

Table 1
Descriptive characteristics of the sample

Variables
N	133
Age (year)	43.7 $\pm$ 9.9
Body wight (kg)	80.3 $\pm$ 15.6
Height (m)	1.60 $\pm$ 0.1
BMI (kg/m²)	31.4 $\pm$ 6.1
BMI status, $n$ (%)
Eutrophy	13 (9,8)
Overweight	51 (38.3)
Obesity	69 (51.9)
Higher pre-surgical weight (kg)	111.4 $\pm$ 18.2
Lower post-surgical weight (kg)	70.3 $\pm$ 13.0
Total weight loss (%)	39.0 $\pm$ 22.4
Time from surgery (years)	6.3 $\pm$ 3.4
Total FFM (g)	39.7 $\pm$ 5.6
Right leg FFM (kg)	6.5 $\pm$ 1.2
Percent body fat (%)	46.5 $\pm$ 6.5
Fat mass (kg)	37.5 $\pm$ 11.3
Quadriceps PM 60^∘/s (Nm)	121.4 $\pm$ 30.1
Relative quadriceps PM 60^∘s (Nm/kg)	1.5 $\pm$ 0.4
Muscle quality (Nm/kg)	18.9 $\pm$ 4.2
Sit-to-stand 30’ (rep)	14.1 $\pm$ 3.3
Six-minute walk test (m)	558.4 $\pm$ 93.0
Timed up and go (sec)	6.3 $\pm$ 1.0

BMI: Body mass index; FFM: Fat-free mass; PT: Peak moment; rep: Number of repetitions; sec: Seconds. Data are expressed as mean $\pm$ standard deviation unless otherwise noted.

3. Results

The descriptive characteristics of the patients are outlined in Table 1, including body composition, muscle strength, quality, and mean performance on the functional tests.

Table 2
Correlations between muscle strength, muscle quality and functional performance ( $n=$ 133)

Variables	Sit-to-stand 30’ (rep)		Six-minute walk test (m)		Timed up and go (sec)
	$r$	$p$	$r$	$p$	$r$	$p$
Quadríceps PM	0.21	0.02	0.34	$<$ 0.01	$-$ 0.16	0.07
Quadriceps PM_bw	0.39	$<$ 0.01	0.52	$<$ 0.01	$-$ 0.37	$<$ 0.01
Muscle quality	0.21	0.01	0.28	0.01	$-$ 0.17	0.05

PT: Peak moment; rep: Number of repetitions; sec: Seconds.

Table 2 presents the correlations between muscle strength and quality measures with patients‘ performance on functional tests. The absolute PM was significantly, but negligibly correlated to the 30-STS performance ( $r=$ 0.21; $p=$ 0.02) and the 6-MWT ( $r=$ 0.34; $p<$ 0.01), while the bodyweight normalized PM (PM_bw) and MQ were correlated with all the conducted functional tests (all $p<$ 0.05). Notably, the correlation coefficients were always higher for the PM_bw.

Table 3

Physical performance according to muscle strength and quality tertiles

Physical tests	T1	T2	T3	$p$ values	Adjusted $p$ values^*
Quadriceps PM (Nm) tertile groups
Sit-to-stand 30’ (rep)	12.9 $\pm$ 2.6	14.6 $\pm$ 3.3	14.6 $\pm$ 3.6	0.015	0.571
Six-minute walk test (m)	517.5 $\pm$ 83.7	565.5 $\pm$ 85.1	593.0 $\pm$ 94.0	0.001	0.566
Timed up and go (sec)	6.5 $\pm$ 1.2	6.2 $\pm$ 0.9	6.2 $\pm$ 0.9	0.264	0.921
Relative quadriceps PM (Nm/kg) tertile groups
Sit-to-stand 30’ (rep)	12.4 $\pm$ 2.9	13.6 $\pm$ 2.6	15.6 $\pm$ 3.4	$<$ 0.001	$<$ 0.001
Six-minute walk test (m)	490.0 $\pm$ 79.5	563.8 $\pm$ 68.6	602.4 $\pm$ 97.0	$<$ 0.001	$<$ 0.001
Timed up and go (sec)	6.9 $\pm$ 1.2	6.2 $\pm$ 0.8	6.0 $\pm$ 0.8	$<$ 0.001	$<$ 0.001
Quadriceps quality (Nm/kg of leg FFM) tertile groups
Sit-to-stand 30’ (rep)	12.9 $\pm$ 2.6	14.8 $\pm$ 3.7	14.5 $\pm$ 3.2	0.001	0.078
Six-minute walk test (m)	528.9 $\pm$ 79.1	561.7 $\pm$ 100.4	583.2 $\pm$ 91.8	0.021	0.793
Timed up and go (sec)	6.5 $\pm$ 1.1	6.3 $\pm$ 0.9	6.1 $\pm$ 0.9	0.160	0.911

BMI: Body mass index; FFM: Fat-free mass; PT: Peak moment; rep: Number of repetitions; sec: Seconds. Data are expressed as mean $\pm$ standard deviation unless otherwise noted. ^*p values for comparisons adjusted for age and time from surgery.

Table 3 presents physical function performance according to muscle strength (PM and PM_bw) and quality tertile groups. Regarding PM, significant differences between groups were observed for the 30-STS and the 6-MWT. As for the PM_bw, significant between groups differences were noted for all the conducted physical function tests. Regarding muscle quality tertile groups, significant between groups differences were observed for the 30-STS and the 6-MWT test results. However, after adjustment for confounders, statistical significances were sustained only for the PM_bw.

Figure 1.

Post hoc analyses for comparisons among relative PM tertile groups. rep: Number of repetitions; sec: Seconds.

Post hoc analyses for comparisons of the PM_bw among tertile groups are illustrated in Fig. 1. For the 30-STS test, differences were driven by better performance for the upper tertile group, with significant differences when compared to the middle and the lowest groups. For the 6-MWT and TUG tests, poorer performance was noted for the lower tertile group, with significant differences when compared to the middle and upper tertile groups.

4. Discussion

To our knowledge, this is the first study to explore muscle strength and quality in relation to physical function in women mid- to long-term after RYGB, a period from which scarce data exist. The salient findings provide support for the concept that skeletal muscle capacity is related to performance in tests that mimic activities of daily life, with muscle strength expressed relative to bodyweight being the variable that presented the most consistent relationship. Specifically, relative strength had been shown to be related to all examined function tests independently from age and time from surgery (i.e., TUG, 6-MWT, and 30-STS). These observations do not support the clinical significance of specific moment, a measure that relies on expensive image equipment and staff, but indicate that PM_bw may be a useful supplement to other functional indices in the evaluation of these patients. Ultimately, the results presented here align with the recent literature in this area, which shows that strength training, well known to increase maximum muscle moment, also improves physical function indices in patients who had undergone bariatric surgery [15, 26].

Worldwide, the prevalence of obesity is currently high and is increasing, despite notorious associations with morbidly and mortality [8, 27, 28]. In general, non-pharmacological and pharmacological obesity treatments were associated with limited success [1, 2, 3, 4, 6, 7, 8]. Even when significant weight loss is achieved, a large fraction of the patients relapses within mid to long term. On the other hand, bariatric surgery procedures have been well documented to effectively induce large and persistent weight loss [1, 4, 6, 9], with beneficial effects on glycemic control [1], cardiovascular disease risk factors [11, 29], and all-cause mortality risks [6]. However, despite profound weight loss as a result of bariatric surgery, a substantial loss of FFM, particularly skeletal muscle mass [9, 30, 31] might occur, raising the concern of a potentially detrimental effect on muscle strength and physical performance. A recent systematic review demonstrated that a relevant amount of FFM is lost within one-year post-surgery [2]. It has also been reported that FFM decline is accompanied by a significant reduction in absolute muscle strength when compared to preoperative values [9]. The present study provides support that muscle strength is modestly associated with physical performance in women mid- to long-term after RYGB. The highest sores for the correlations with functional tests were observed for PM_bw (ranging from 0.37 to 0.52), which can explain 25% at best of the variance. While these observations demonstrate that factors other than muscle strength are important for functionality in this population, it also suggest that strength preservation would benefit the ability to perform everyday activities.

Muscle strength association with physical function in older individuals has been reported in a variety of studies [21, 32, 33, 34], but a similar relationship has also been shown in men and women one year after RYGB in one study [9]. Muscle strength, however, does not rely exclusively on muscle mass, and the relationship between strength and muscle mass is not linear [35]. The muscle quality concept has emerged to denote the amount of moment generated per unit of muscle mass, referred to as specific moment [18, 35]. Muscle quality has been recognized as a complementary prognostic tool, particularly in the evaluation of physical function. Individuals with obesity exhibit a high rate of poor muscle quality [23], which may partially explain their higher risk of functional inabilities. Intra and intermuscular lipid content seem to be considerably greater in obese individuals than in their non-obese counterparts, but the effects of RYGB on muscle quality and its association with function are unknown, especially in the mid- to long-term post-surgery. The results presented here, however, do not provide the support that specific moment outperforms strength measures in association with physical function in this population. In fact, muscle strength relative to body weight was the variable that was more contently related to functional performance.

Even though the relationship between muscle quality and physical function has not been previously examined in post-bariatric individuals, there are available data for other sections of the population. In men and women 65 years of age and older, Shaffer et al. (2017) analyzed whether muscle quality correlates more strongly with lower extremity function than muscle strength alone [22]. These authors reported that muscle quality did not outperform muscle strength in the relationship with function, which is in line with the results of our study. These findings may be of practical application, considering that muscle quality assessment relies on expensive and not broadly available equipment and staff. Thus, the assessment of muscle strength alone, PM_bw, serve to evaluate the relationship between skeletal muscle phenotype and physical function. Ultimately, the observations reported here aggregate the concept that interventions designed to mitigate post-bariatric strength loss are needed, with potentially positive effects on physical function. In fact, a recent study demonstrated that a 12-week strength training program improved muscle strength and physical function in individuals 2–7 years after RYGB and that improvements in strength partially explained physical function gains [26].

Strengths of the present study include the use of gold standards techniques for FFM and muscle strength assessment, the novelty of the findings considering the population under investigation, and the potential for practical application of the results in the evaluation of post-RYGB patients. This study also has some limitations. The procedures were conducted in well-functioning women, and thus the results may not apply to men or more frail sections of the post-bariatric population. Although specific moment (or strength) has been typically used to define muscle quality [19, 20, 21, 26], future studies are required to explore the association between muscle quality and physical function using image techniques such as computed tomography or magnetic resonance images to assess muscle composition, particularly intramuscular lipids. Finally, the cross-sectional nature of this study mid- to long-term after surgical interventions precludes comparisons with pre-operative values. Hence, future longitudinal data are necessary to better understand the role of skeletal muscle phenotype in functional capacity after RYGB, including in comparisons with pre-surgical state.

5. Conclusion

Based on the observed results, it is concluded that both muscle strength and quality are modestly associated physical function in women mid- to long-term after RYGB. Muscle strength expressed relative to body weight (i.e., PM_BW), however, outperformed absolute strength and muscle quality. These results do not provide support for the concept that muscle quality, a measure that relies on expensive image equipment, is clinically meaningful in terms of functional implications, while muscle strength relative to bodyweight seems a supplement in the evaluation of this population. Our results corroborate the concept that interventions designed to improve muscle strength will benefit patients who underwent bariatric surgery, particularly in their ability to perform activities of daily life.

Author contributions

GNG and RML conceived and designed the study. MB, FL, MM, KMC and ELS contributed to critical revision of the manuscript for important intellectual content. GNG, MPD and RML performed statical analysis. All the authors approved the manuscript.

Ethical considerations

The study was approved by the Institutional Review Board of the University of Brasilia and adhered to the Declaration of Helsinki.

Funding

The authors report no funding.

Footnotes

Acknowledgments

The authors would like to thank the Brazilian Coordination for the Improvement of Higher Education Personnel (CAPES) for the master scholarship grant to Gustavo N. Gomes.

Conflict of interest

All authors have no competing interests to disclose.

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The relationship between muscle strength and quality with functional performance in women mid- to long-term after Roux-en-Y gastric bypass

Abstract

BACKGROUND:

OBJECTIVE:

METHODS:

RESULTS:

CONCLUSIONS:

Keywords

1. Introduction

2. Materials and methods

2.1 Subjects

2.2 Muscle strength assessment

2.3 Body composition evaluation

2.4 Muscle quality

2.5 Physical function assessment

2.6 Statistical analyses

Table 1 Descriptive characteristics of the sample

Table 2 Correlations between muscle strength, muscle quality and functional performance ( n = 133)

5. Conclusion

Author contributions

Ethical considerations

Funding

Footnotes

Acknowledgments

Conflict of interest

References

Table 1
Descriptive characteristics of the sample

Table 2
Correlations between muscle strength, muscle quality and functional performance ( $n=$ 133)