The relationship between muscle quality index and physical function in older adults

Abstract

BACKGROUND:

The muscle quality index (MQI) has been proposed as a diagnostic tool to detect individuals at risk of limited physical function.

OBJECTIVE:

Our goal was to examine the relationship of the MQI with physical function and compare its predictive ability with other muscle parameters of strength and mass in an older population.

METHODS:

Sixty-eight healthy older adults (34 male, 34 female) aged between 69 and 89 years were tested for body composition, MQI, maximum isokinetic concentric KES and physical function including sit-to-stand (STS) time, normal and maximum walking speed (WS), Timed Up and Go (TUG) and static balance. Pearson’s correlation was applied to examine the relationship between muscle parameters. Linear regression analysis including age and sex as additional covariates was performed to assess their predictive ability for physical functions.

RESULTS:

MQI correlated significantly with relative KES ( $r=$ 0.611, $p<$ 0.001), total KES ( $r=$ 0.829, $p<$ 0.001) and leg lean tissue mass ( $r=$ 0.690, $p<$ 0.001). The MQI was not a significant predictor for any physical function ( $p>$ 0.05). STS time was a significant predictor for normal WS and TUG time ( $p<$ 0.001). Relative KES was a significant predictor for all physical functions except static balance ( $p<$ 0.001). No muscle parameter and only age was a significant predictor for static balance. Models explained 20.4%–57.3% of variances of dependent variables.

CONCLUSIONS:

The MQI is a useful tool to assess leg lean tissue mass and strength of the knee extensor muscles and outperforms STS time. However, STS time and relative KES are more closely related to physical function than the MQI.

Keywords

Knee extensor strength sit-to-stand gait speed balance timed up and go

1. Introduction

Through the progress of medical and technological research, life expectancy has increased, and more people reach an advanced stage of life. As a consequence, age-related diseases and physical conditions have become a more relevant socioeconomic topic [1].

Age-related loss of muscle mass and function, known as sarcopenia, is a major problem in a senescent population [2], and is related to loss of strength, functional impairment, falls, disability, and hospitalization [3, 4, 5, 6]. Definitions of sarcopenia are based on different muscle mass, gait speed, and grip strength cut-offs [7]. However, muscle mass declines at a different rate than muscle strength and power, and is less related to the physical function status of an individual [8, 9, 10]. In this, context the concept of muscle quality as the strength per unit of muscle mass was developed [11]. Assessment of grip strength is an unspecific strength test and lower body muscle strength is closer related to functional capacities [12]. Gait speed is a good indicator for physical function and is related to lower limb strength [13]. However, this relationship is not linear, and gait speed measurements provide limited information about force production capacities [14].

Partially in response to these limitations, a review by Barbat-Artigas et al. [15] proposed the muscle quality index (MQI) as an additional “clinical screening tool to detect individuals at risk of physical incapacities based on muscle quality”. The MQI assesses lower extremity muscle function through testing of sit-to-stand power and anthropometric parameters. It was originally developed as a “sit-to-stand” test by Takai et al. [16] to assess knee extensor strength in older adults. The sit-to-stand power calculation incorporates the test time, leg length, chair height, number of repetitions and body weight, and is a sensitive measure for age-related decline in older adults [17]. By considering the subject’s anthropometry in relation to the chair height, the sit-to-stand power provides a more comparable test result for subjects with different body dimensions. While sit-to-stand time alone was not correlated to knee extensor strength, the MQI correlated strongly ( $r=$ 0.730, $p<$ 0.001) [16]. Only after body mass and lower limb length were statistically controlled for, there were significant negative correlations between sit-to-stand time and knee extensor strength ( $r=$ 0.342, $p=$ 0.011). Therefore, it is unclear whether the sit-to-stand time is an indicator of relative knee extensor strength, and whether the MQI is an indicator of total knee extensor strength.

The MQI is a lower extremity-specific test and is a more complete index of muscle quality compared to non-specific measures such as grip strength, particularly due to the consideration of the velocity at which muscle shortens (i.e. muscle power), which is reflective of the neuromuscular component [18]. While there is no generally accepted definition of sarcopenia, a valid diagnostic tool is certainly warranted due to the prevalence of the disorder [19, 20, 21]. In this context, Fragala et al. [18] clarified that no current sarcopenia definition integrated the potentially more valid MQI into its criteria. The few studies which have assessed the MQI demonstrate its value for the assessment of leg and hip muscle function, diagnosis of osteoarthritis and as a predictor for mortality in older adults, however none of these previous studies have examined its relationship with physical function [16, 18, 22, 23, 24, 25]. Although this test was suggested to detect individuals at risk of physical incapacities, it remains unclear how the MQI predicts functional performance other than sit-to-stand time in older adults, whether it outperforms other muscle parameters like knee extensor strength and leg lean tissue mass, and ultimately whether it is indeed a valid tool for assessing lower body muscle strength and function.

Therefore, the aim of this study is to examine the predictive value of the MQI compared to other markers of performance, including sit-to-stand time, knee extensor strength and lean leg mass, for physical function in older men and women.

2. Methods

2.1 Participants

68 healthy older adults (34 male, 34 female) aged between 69 and 89 were recruited via local newspaper advertisements. Before testing, eligibility for study participation was ensured via inclusion criteria: participants needed to 1) be at least 65 years old, and 2) be able to walk independently. Exclusion criteria included: 1) the presence of neurological diseases like Alzheimer’s, stroke, and Parkinson’s disease, 2) participants with severe orthopaedical conditions like severe foot deformities and leg length differences that might unnaturally influence gait or balance were excluded, 3) participants with artificial joints, prostheses, and other metals in their lower limbs were also excluded, 4) participants had to be injury-free in their lower limbs and torso for at least the last six months, and 5) participants had to show no high risk for cardiovascular complications before the examination. Every participant received a study information sheet and provided informed consent. Ethical approval was obtained by the Ethical Commission of the local ethics committee (protocol number: FSV 18/49).

2.2 Testing procedures

2.2.1 Anthropometry and body composition

Height was measured with a stadiometer. The leg length, classified as the distance from the greater trochanter of the femur to the malleolus lateralis of the dominant leg, was obtained with a measuring tape [16]. Leg dominance was determined by personal preference [26]. Body composition was obtained with the Inbody 720 (JP Global Markets GmbH, Eschborn, Germany) and included weight, skeletal muscle mass, fat mass, body fat percentage, and leg lean tissue mass. The bioimpedance analysis with the Inbody 720 is demonstrated to be a valid tool for the assessments of total body and segmental body composition in adults [27].

2.2.2 Functional assessment

For the assessment of functional capabilities, the sit-to-stand time, normal and fast walking speed, and static and dynamic balance were measured in a fixed order. The tests were selected based on their relevance for physical functioning during daily activities and the evidence for their reliability and validity. Each participant attended one single session where all tests were performed by the same investigator with experience in strength and motor performance assessment.

a) Sit-to-stand test and MQI

Participants were instructed to stand up from a chair as fast as possible 10 times in a row with hands placed across the chest. The testing procedure was performed according to Takai et al. [16]. Before testing, the correct sit-to-stand motion was practised by a shortened practice trial. The time to perform the task was measured with a stopwatch over two trials. The fastest time was chosen for data analysis. A standardized chair height of 40 cm was used. MQI as a measure of muscle power was calculated by the formula provided by Takai et al. [16] and included leg length (m), chair height (m), body mass (kg), acceleration of gravity (9.8 m/s ${}^{2}$ ), number of repetitions, and test time (s).

$\displaystyle\textit{sit-to-stand power}=$ $\displaystyle\frac{(\textit{leg length}-0.4)\times\textit{body mass}\times% \textit{gravity}\times 10}{\textit{sit-to-stand time}}$

b) Walking speed

Participants were instructed to walk six meters at their normal walking speed and as fast as possible. Time was measured over two trials by a stopwatch for the central four meters of the walkway [28]. The fastest time was chosen for data analysis.

c) Static balance

Static balance was measured by assessing postural sway (centre of pressure path length) with a Kistler force plate (Kistler Instrumente GmbH, Sindelfingen, Germany) [29, 30]. Participants were instructed to stand as still as possible for 30 s with their hands on the hips, open eyes, looking straight and standing in a semi-tandem stance. For analysis, postural sway values were divided by height in centimetres [31].

d) Timed Up and Go test

Dynamic balance was assessed using the Timed Up and Go test [32, 33]. Participants were instructed to stand up from a chair, then walk as fast as possible three meters towards a cone, walk around the cone, walk back and sit again on the chair. Time was measured with a stopwatch. Acceptable reliability and validity of the stopwatch-measured Timed Up and Go test were reported previously [33, 34]. Every participant performed a test trial followed by two timed trials. The fastest time was chosen for data analysis.

2.2.3 Strength assessment

Only the dominant side of the body was measured. Isokinetic concentric muscle strength of knee extensors was measured with the Isomed 2000 system (Isomed 2000 ${}^{\text{\textregistered}}$ , D&R Ferstl GmbH, Hemau, Germany). This test was performed seated. At first, the seat and adapter lengths were adjusted to the femur and shank lengths, respectively. To transfer the strength of the thigh muscles to the pad, the adapter was fixed to the distal part of the shank slightly above the malleoli. Next, the pivot point of the knee joint (centre of the knee joint) and the device were synchronized to each other. The backrest and seat were slightly inclined so that the hip angle was around 90 ${}^{\circ}$ . The initial angle of the knee was 90 ${}^{\circ}$ . Lastly, to prevent evasion movements, the subject’s femur was fixed with straps, the pelvis was strapped with a belt, and shoulders were restrained with shoulder pads. The tested range of motion ranged from 5 ${}^{\circ}$ to 90 ${}^{\circ}$ of knee flexion. The assessments were performed with an angular velocity of 60 ${}^{\circ}$ per second. Before starting the test trials, participants underwent a familiarisation phase where they could perform the movements with submaximal effort. Following this, the testing phase consisted of two trials with three maximal repetitions per trial with 2 minutes of complete rest between trials. Three repetitions were performed in each direction (flexion and extension) so that the participant had a sufficient number of attempts to display maximum strength. In case of a high moment difference (5%) between the last two trials, an additional trial was performed. The maximum of the three trials was used for data analysis. Participants were encouraged verbally by the tester during the trials. Results were presented as newton meters and were divided by body weight for further analysis.

2.3 Data analysis

Table 1
Characteristics of participants

	Total	Male	Female
Characteristics	Mean \| SD	Mean \| SD	Mean \| SD	$p$
Age (yrs)	76.9 $\pm$ 4.8	77.1 $\pm$ 4.7	76.6 $\pm$ 4.9	0.706
Height (m)	166.8 $\pm$ 9.0	172.9 $\pm$ 6.7	160.7 $\pm$ 6.7	$<$ 0.001
Weight (kg)	73.0 $\pm$ 11.9	78.0 $\pm$ 8.8	68.1 $\pm$ 12.6	$<$ 0.001
BMI (kg/m ${}^{2}$ )	26.3 $\pm$ 3.6	26.1 $\pm$ 2.4	26.5 $\pm$ 4.5	0.436
Skeletal muscle mass (kg)	26.5 $\pm$ 5.2	30.6 $\pm$ 3.5	22.3 $\pm$ 2.7	$<$ 0.001
Total fat (kg)	24.3 $\pm$ 8.3	22.3 $\pm$ 6.1	26.4 $\pm$ 9.7	0.160
Body fat percentage (%)	33.0 $\pm$ 8.00	28.2 $\pm$ 6.0	37.8 $\pm$ 6.9	$<$ 0.001
Sit-to-stand time (s)	19.0 $\pm$ 6.9	17.7 $\pm$ 5.3	20.33 $\pm$ 8.05	0.123
Muscle quality index (W)	161.0 $\pm$ 51.1	192.4 $\pm$ 44.4	129.6 $\pm$ 36.2	$<$ 0.001
Timed Up and Go (s)	6.9 $\pm$ 1.3	6.7 $\pm$ 1.2	7.02 $\pm$ 1.32	0.282
Normal walking speed (m/s)	1.3 $\pm$ 0.2	1.3 $\pm$ 0.2	1.3 $\pm$ 0.2	0.814
Fast walking speed (m/s)	1.8 $\pm$ 0.3	1.9 $\pm$ 0.3	1.75 $\pm$ 0.3	0.025
Open eyes semi-tandem stance (mm/mm)	0.6 $\pm$ 0.2	0.6 $\pm$ 0.3	0.6 $\pm$ 0.2	0.573
Total knee extensor strength (Nm)	108.0 $\pm$ 31.7	129.1 $\pm$ 26.2	87.0 $\pm$ 20.9	$<$ 0.001
Relative knee extensor strength (Nm/kg)	1.5 $\pm$ 0.4	1.7 $\pm$ 0.3	1.3 $\pm$ 0.3	$<$ 0.001

Table 2

Relationship between muscle parameters (STS $=$ sit-to-stand, LTM $=$ lean tissue mass, KES $=$ knee extensor strength)

Variable		MQI	STS time	Leg LTM	Relative strength
STS time	Pearson’s $r$	$-$ 0.588
	$p$ -value	$<$ 0.001
Leg LTM	Pearson’s $r$	0.690	$-$ 0.027
	$p$ -value	$<$ 0.001	0.827
Relative KES	Pearson’s $r$	0.611	$-$ 0.580	0.406
	$p$ -value	$<$ 0.001	$<$ 0.001	$<$ 0.001
Total KES	Pearson’s $r$	0.829	$-$ 0.413	0.739	$-$ 0.849
	$p$ -value	$<$ 0.001	$<$ 0.001	$<$ 0.001	$<$ 0.001

Statistical analyses were performed with JASP (JASP Team (2020)), version 0.12.2. Data were checked for normality, outlying scores, and missing data. Missing data due to physical limitations were transformed into one unit above/below the next most extreme score. An independent $t$ -test was used to compare mean values between men and women. In case equality of variance was violated, the Mann-Whitney-U Test was used. Pearson’s correlation was applied to examine the relationship between muscle parameters. Correlations coefficients of 0.10 $\leqslant$ $r$ $\leqslant$ 0.39 indicated a weak, 0.40 $\leqslant$ $r$ $\leqslant$ 0.69 a moderate, and $r\geqslant$ 0.70 a strong correlation as classified by Schober et al. [35]. Linear regression analysis including age and sex as additional covariates was performed to assess the predictive ability of muscle parameters for physical functions. Collinearity diagnostics were performed to assess variance inflations in the predictors. Relative and total knee extensor strength had high collinearity and because relative knee extensor strength is reported to be more closely related to physical function [10, 36], it was chosen for the regression analysis. For the six included predictors, variance inflation factor and tolerance ranged from 1.328–5.215 and 0.192–0.753, respectively.

3. Results

Table 3
Linear regression analysis between muscle performance variables with physical function with age and sex as covariates (STS $=$ sit-to-stand, LTM $=$ lean tissue mass, KES $=$ knee extensor strength)

	Normal walking speed				Maximum walking speed
	$\beta$	SE	$p$ -value	$R^{2}$ ( $p$ -value)	$\beta$	SE	$p$ -value	$R^{2}$ ( $p$ -value)
MQI	$-$ 0.369	9.716e $-$ 4	0.126	0.338 ( $\bm{p<}$ 0.001)	$-$ 0.063	0.001	0.777	0.427 ( $\bm{p<}$ 0.001)
STS time	$-$ 0.502	0.006	0.01		$-$ 0.339	0.008	0.058
Leg LTM	0.223	0.029	0.315		$-$ 0.145	0.04	0.483
Relative KES	0.372	0.091	0.021		0.337	0.126	0.025
Age	$-$ 0.053	0.005	0.662		$-$ 0.148	0.007	0.19
Sex	$-$ 0.188	0.074	0.295		0.189	0.103	0.257
	Timed up and go time				Postural sway
	$\beta$	SE	$p$ -value	$R^{2}$ ( $p$ -value)	$\beta$	SE	$p$ -value	$R^{2}$ ( $p$ -value)
MQI	$-$ 0.085	0.005	0.657	0.573 ( $\bm{p<}$ 0.001)	0.272	0.011	0.301	0.206 ( $\bm{p<}$ 0.026)
STS time	0.465	0.027	0.003		0.341	0.063	0.104
Leg LTM	0.26	0.138	0.147		$-$ 0.052	0.315	0.832
Relative KES	$-$ 0.306	0.437	0.019		$-$ 0.068	0.997	0.697
Age	0.1	0.025	0.305		0.318	0.058	0.019
Sex	$-$ 0.032	0.355	0.823		0.104	0.81	0.594

Table 1 shows the anthropometric characteristics, physical function, and knee extensor strength of all participants. Neither gender differed regarding their age, BMI and total fat mass but male participants were significantly ( $p<$ 0.001) taller, heavier, leaner, and had more skeletal muscle mass than female participants. Sex-specific comparisons of physical function tests show significant differences in gait speed and muscle power, with men walking faster than women ( $p=$ 0.025) and displaying higher sit-to-stand power ( $p<$ 0.001). While the sit-to-stand time, TUG time, and postural sway showed no sex differences.

Secondly, MQI correlated significantly with relative knee extensor strength ( $r=$ 0.611, $p<$ 0.001), and total knee extensor strength ( $r=$ 0.829, $p<$ 0.001) Table 2. Sit-to-stand time also correlated significantly to relative knee extensor strength ( $r=$ $-$ 0.580, $p<$ 0.001) and total knee extensor strength ( $r=$ $-$ 0.413, $p<$ 0.01) but to a smaller extent. While sit-to-stand time was not correlated to leg lean tissue mass, the MQI correlated significantly ( $r=$ 0.690, $p<$ 0.01).

Out of all independent variables in the linear regression, the MQI was not a significant predictor for any physical function ( $p>$ 0.05) Table 3. Sit-to-stand time and relative knee extensor strength were significant predictors for normal walking speed and TUG time ( $p<$ 0.001). Relative knee extensor strength was a significant predictor for maximum walking speed ( $p<$ 0.001). No muscle parameter was a significant predictor of static balance, with only age identified as a significant predictor. Models explained 20.4%–57.3% of variances of dependent variables.

4. Discussion

The MQI has been proposed as a diagnostic tool to detect individuals at risk of physical incapacities and to evaluate knee extensor muscle strength [15, 16], however until now it remained unclear how it related to general physical function. Our findings indicate that the MQI was not a significant predictor for any physical function in healthy older adults with an age between 69 and 89 years. Relative knee extensor strength and sit-to-stand time showed a closer relationship with all physical functions (except static balance) than the MQI. Therefore, we conclude that although the MQI can estimate some physical capacities, it is not superior to sit-to-stand time or knee extensor strength in identifying individuals with physical incapacities. Leg lean tissue mass correlated with no parameter of physical function, which is in agreement with previous research [9, 37, 38]. Also, in agreement with other literature is our finding indicating the lack of predictive ability of muscle parameters for static balance. It has been reported that body morphology, visual and peripheral sensory function play a superior role in static balance than muscle strength [39, 40, 41].

Although the MQI was not a significant predictor for physical function, our results indicate that it is a good tool to assess relative and total knee extensor strength in healthy older adults. Contrary to the study by Takai et al. [16] our sit-to-stand time was also related to both knee extensor strength parameters. This result is possibly due to differences in contraction types (concentric in this study vs isometric Takai et al. [16]) used between the studies. Additionally, our results showed that the MQI is more closely related to total than relative knee extensor strength. Further, the MQI displayed a significant and moderate ( $r=$ 0.690) relationship with leg leg lean tissue mass which was not the case for sit-to-stand time. This may be partly explained by the incorporation of leg length and body weight into the calculation which are related to leg lean tissue mass. This might be useful to assess muscle loss in the leg.

To calculate the MQI, participants had to perform sit-to-stand transfer (seated position to fully upright standing) ten times as suggested by Takai et al. [16]. Our participants were healthy old adults with no apparent physical limitations. However, due to the relatively high number of sit-to-stand repetitions, MQI might be especially difficult for physically less capable populations, and therefore performing the more common five repetitions sit-to-stand test where reference values are available is another factor that favors the sit-to-stand time over the MQI [42, 43]. Additionally, the MQI equation calculates sit-to-stand power only in the vertical direction. The horizontal component of the sit-to-stand transfer to shift the body mass over the base of support (feet) is not included. This is of importance since individuals with muscle weakness prefer to use stabilization-strategies during sit-to-stand tasks which require more horizontal work, characterized by higher trunk and hip flexion [44].

Only few studies have used the MQI in their methods previously. Machado-Payer et al. [24] observed that MQI performance was related to osteoarthritis, while Jerez-Mayorga et al. [22, 23] showed that the MQI was related to hip muscle strength. Additionally, Jerez-Mayorga et al. compared MQI between older and younger women and found no difference [23]. Brown et al. [25] demonstrated that the MQI was a predictor of mortality in older adults. Fragala et al. examined the changes in MQI due to resistance training [18], observing that both MQI and sit-to-stand time improved with resistance training. To our knowledge, our study is the first to examine the validity of the MQI regarding its connection to physical function in adults without physical limitations.

The power calculation by the MQI results from the moved distance from chair height to upright standing, the subject’s bodyweight, number of repetitions and test duration. However, the MQI might have limited comparability to other measures of muscle power (work per unit of time) that have been performed in previous studies [45]. In general, Alcazar et al. [46] found major discrepancies in muscle power testing protocols among studies, and Regterschot et al. [47] stated that commonly used strength and power-related field tests do not meet all criteria important for the application of strength and power-related field tests in older adults. Muscle power declines at a higher rate than muscle strength at an advanced age. Therefore, research has been conducted to examine whether muscle power is more directly related to physical function than muscle strength. In a systematic review by Byrne et al. [45], out of forty-four studies investigating relationships between muscle power and physical functions, sixteen studies were identified which enabled a comparison between the explanatory ability of muscle power and muscle strength regarding physical function. Data from these studies established both parameters to be important predictors of physical function in older adults, with evidence that muscle power is a marginally better predictor of functional performance than strength. Whereas in our case, the MQI was not related to physical function when compared to other muscle performance parameters.

In context of the results, some limitations of this study should be considered. We compared multiple parameters of muscle function and their relationship to physical function. However, we did not report and include real knee extension muscle power in our analysis. Since power is calculated by torque times distance per time, we opted not to report power values because beside torque, all other components of power were almost identical for all subjects during isokinetic testing. Further, time to reach peak torque is dependent on the force-length relationship and joint angle of the muscle [48] which again depend highly on the angular velocity of the test.

Although we tested important physical functions for activities of daily living, we did not include other physical capabilities (e.g. climbing stairs, changes in direction) which may display unique correlations with the tests used, including the MQI.

5. Conclusion

The MQI is a useful tool to assess leg lean tissue mass and strength of the knee extension muscles and outperforms sit-to-stand time in this regard. However, sit-to-stand time and knee extension strength are more closely related to physical function than the MQI. Therefore, although the MQI may be useful in assessing muscle loss in the lower limbs, muscle strength and sit-to-stand time seem to be more valuable and accurate tools for assessing physical capacities in older adults.

Author contributions

CONCEPTION: Andreas Stotz.

PERFORMANCE OF WORK: Andreas Stotz.

INTERPRETATION OR ANALYSIS OF DATA: Andreas Stotz, Joel Mason and Astrid Zech.

PREPARATION OF THE MANUSCRIPT: Andreas Stotz, Joel Mason and Astrid Zech.

REVISION FOR IMPORTANT INTELLECTUAL CONTENT: Joel Mason and Astrid Zech.

SUPERVISION: Astrid Zech.

Ethical considerations

Every participant received a study information sheet and provided informed consent. Ethical approval has been obtained by the Ethical Commission of the local ethics committee (protocol number: FSV 18/49, 10.12.2018).

Funding

The authors report no funding.

Footnotes

Acknowledgments

The authors have no acknowledgments.

Conflict of interest

The authors have no conflicts of interest to report.

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The relationship between muscle quality index and physical function in older adults

Abstract

BACKGROUND:

OBJECTIVE:

METHODS:

RESULTS:

CONCLUSIONS:

Keywords

1. Introduction

2. Methods

2.1 Participants

2.2 Testing procedures

2.2.1 Anthropometry and body composition

2.2.2 Functional assessment

2.2.3 Strength assessment

2.3 Data analysis

Table 1 Characteristics of participants

Table 3 Linear regression analysis between muscle performance variables with physical function with age and sex as covariates (STS = sit-to-stand, LTM = lean tissue mass, KES = knee extensor strength)

5. Conclusion

Author contributions

Ethical considerations

Funding

Footnotes

Acknowledgments

Conflict of interest

References

Table 1
Characteristics of participants

Table 3
Linear regression analysis between muscle performance variables with physical function with age and sex as covariates (STS $=$ sit-to-stand, LTM $=$ lean tissue mass, KES $=$ knee extensor strength)