Skeletal Muscle Mass,Bone Mineral Density,and Walking Performance in Masters Cyclists

Abstract

Exercise mode and intensity/duration are important factors for influencing muscle morphology and function as well as bone. However, it is unknown whether masters cyclists who undergo regular moderate- to high-intensity exercise maintain lower-body skeletal muscle mass (SM) and function and bone health when compared with young adults. The purpose of this study was to compare SM, areal bone mineral density (aBMD), and gait performance between masters cyclists and young adults. Fourteen male masters cyclists (aged 53–71 years) and 13 moderately active young men (aged 20–30 years, exercising less than twice a week) volunteered. The masters cyclists were all training actively (four to five times per week, ∼200 miles per week) for on average the last 17 years (range 7–38 years). Thigh SM was estimated from an ultrasound-derived prediction equation using muscle thickness (MTH). Appendicular lean mass (aLM) and aBMD were also estimated using dual-energy X-ray absorptiometry. There were no significant differences (p<0.05) in thigh SM, anterior and posterior thigh MTH ratio, or aLM between masters cyclists and young men. Maximum straight and zigzag walking times were also similar between groups. Lumbar spine (L1–L4) aBMD was not different between groups, but femoral neck aBMD was lower (p<0.05) in the cyclists than in the young men. Our results suggest that appendicular as well as site-specific thigh muscle loss with aging were not observed in masters cyclists. This maintenance of muscle mass in masters cyclists may preserve walking performance to similar levels as moderately active young adults. However, long-term cycling does not preserve femoral neck aBMD.

Introduction

Sarcopenia, defined as the age-related loss of skeletal muscle mass (SM), has been used to assess the clinical condition of older people who have exceptionally low levels of total body muscle mass and/or declines in muscular strength and physical function.¹ SM in later life is determined by both peak SM attained in early life and the rate of muscle loss. Thus, higher SM in early life may present as an advantage for delaying or preventing sarcopenia. Daily physical activity and nutrition are crucial factors for preventing sarcopenia.^2
–4 Moderate-to-vigorous daily physical activity is positively correlated with lower-extremity SM and function in older adults.^5,6 Our laboratory^7,8 and others⁹ have recently reported that sarcopenia is observed as a site-specific loss of SM, especially for the quadriceps muscle. The site-specific thigh muscle loss appears before it is able to be detected at the whole-body level.¹⁰ A recent study reported that site-specific muscle loss is associated with zigzag walking performance, but not with normal and maximum straight walking speed in middle-aged and older women.¹¹

The reason for the site-specific decrease in quadriceps SM with age is largely unknown. Site-specific thigh muscle loss is likely multifactorial, as it is with the current dogmatic age-related model of homogeneous SM mass loss. One possible factor may be the intensity and duration of physical activity completed over a lifetime. Due to changes in physical activity– and/or age-related neuromuscular changes, it is conceivable that there may be a decline in anterior muscle activation with advancing age. A study examined muscle activity in the quadriceps during 24 hr of daily activity using electromyography and found that the vastus lateralis muscle was active for a short amount of time (1–3 hr) and at relatively low intensities (3%–11% of maximum voluntary isometric strength), although only one muscle was measured.¹² This is supported by research that has observed site-specific loss in motor units with advancing age.¹³

Recently, we investigated the effects of habitual recreational sports and exercise activity on site-specific muscle loss in young and old women. We found that quadriceps muscle size was still smaller in older active women than in young inactive women, although quadriceps muscle size was larger in the older active women than in the older inactive women.¹⁴ Thus, site-specific muscle loss is still observed in older women who perform low- and moderate-intensity habitual exercise. It is unknown whether or not recreational sports consisting of moderate and vigorous intensities (masters athletes) can prevent age-related site-specific quadriceps muscle loss.

A previous study investigated the impact of different sports on muscle morphology and function of masters athletes.¹⁵ They found that only strength-trained older athletes had greater quadriceps muscle cross-sectional area and knee extension strength compared to age-matched untrained controls, whereas no difference was observed between masters swimmers and runners and the untrained controls. Conversely, one study that measured thigh lean volume (estimated via anthropometrical methods [circumference and skinfolds]) observed no significant difference between young and masters cyclists.¹⁶ Thus, exercise mode and intensity/duration seem to be important factors for influencing muscle morphology and function in masters athletes. Interestingly, recent studies have reported that cycle exercise training resulted in significant quadriceps muscle hypertrophy and increased muscular function regardless of age.^17,18 Therefore, we hypothesized that masters cyclists training regularly at moderate and high intensities should maintain lower-body SM when compared with young individuals. The purpose of this study was to compare total and regional SM, walking performance, and bone mineral density between male masters cyclists and body mass index (BMI)-matched young men.

Methods

Participants

Fourteen masters cyclists (men, aged 53–71 years) and 13 young men (aged 20–30 years) volunteered for the study. Young men were recruited from the university population, and those who volunteered were considered to be moderately active but untrained (exercising less than twice a week). The masters cyclists were also recruited from the university campus and the surrounding area. All masters cyclists were members of a local area cycling team and were all training actively (four to five times/week, 80–200 miles/week) for, on average, 17 years (range 7–38 years). Two of the 14 cyclists performed exercise against their own body weight, such as abdominal flexion exercises and pushups, and one of them performed moderate-intensity resistance training a couple times per week. With the exception of one masters cyclist, all subjects had no known neurological, metabolic, or cardiovascular disease and none were taking medications known to affect bone metabolism. One cyclist had previously suffered from a minor myocardial infarction, but had been training (150 miles weekly) successfully for 7 years with no complications. All participants were caucasian. Prior to testing, study approval was granted by the University Institutional Review Board and informed consent was obtained from all participants.

Body composition by ultrasound

Body mass and standing height were measured using a standard height and a weight scale. BMI was defined as body mass divided by height in meters squared (kg/m²). Selected anthropometric measures were obtained bilaterally from all subjects, as described previously.¹⁹ Body density was estimated from subcutaneous fat thickness using an ultrasound-derived prediction equation.¹⁹ We have reported previously that the standard error of the estimate (SEE) of body density, calculated using the ultrasound equations, is approximately 0.006 gram/mL (or an error of about 2.5% body fat) in the normal-weight Japanese population.¹⁹ Percentage of body fat was calculated from body density using the equation of Brozek et al.²⁰ Fat free mass (FFM) was estimated as the difference between total body mass and fat mass. FFM index was calculated as FFM divided by height in meters squared (kg/m²).

Appendicular lean tissue mass and bone mineral density

Subjects underwent dual-energy X-ray absorptiometry scans (DXA) (Discovery A, Hologic Inc., Bedford, MA) to assess areal bone mineral density (aBMD, grams/cm²) of the anteroposterior (AP) lumbar spine (L1–L4) and proximal femur (femoral neck) of the non-dominant leg. A whole-body scan was used to determine percentage body fat (%BF), arm and leg lean tissue mass, and appendicular lean tissue mass (aLT). aLT index was calculated as aLT divided by height in meters squared (kg/m²). Quality assurance testing (QA) and calibration were performed the morning of data collection days to ensure that the DXA was operating properly. Subjects were asked to refrain from eating for at least 4 hr prior to being scanned. Test–retest reliability using intra-class correlation coefficient (ICC_3,1), standard error of the mean (SEM), and minimal difference to be considered real were previously determined from 17 subjects scanned twice 24 hr apart for aLT (0.99, 0.21 kg, and 0.58 kg), %BF (0.99, 0.49 %, and 0.95%), lumbar spine aBMD (0.99, 0.015 g/cm², and 0.031 g/cm²), and femoral neck aBMD (0.99, 0.009 g/cm², and 0.019 g/cm²).

Total body and thigh SM by ultrasound

SM was estimated from the ultrasound-derived prediction equation developed by Sanada et al.²¹ The sum of muscle thickness (MTH) at the nine sites was used to estimate total SM: Total SM (kg)=0.594×sum MTH (cm)×height −11.32 (R ²=0.96, standard error of estimate=1.1 kg). To estimate thigh SM, the sum of two MTH values at the thigh was used: Thigh SM=0.532×sum MTH×height −2.64. Recently, we examined the relationship between DXA-estimated aLT and total SM predicted by ultrasound and found that there is a strong correlation (R ²=0.95) between the two methods.²²

MTH was measured using B-mode ultrasound (Aloka SSD-500, Tokyo, Japan) at nine sites on the anterior and posterior aspects of the body (forearm, upper arm, trunk, thigh, and lower leg), as previously described.¹⁹ The measurements were taken while the subjects stood with their elbows and knees extended and relaxed. A 5-MHz scanning head was placed on the measurement site without depressing the dermal surface. Tissue distortion due to excess compression was eliminated by observing that no movement of tissue occurred in the real-time ultrasound image. The subcutaneous adipose tissue–muscle interface and the muscle–bone interface were identified from the ultrasonic image, and the distance between two interfaces was recorded as MTH. Test–retest reliability of MTH measurements using ICC_3,1, SEM, and mean difference was previously determined from 15 middle-aged subjects for anterior (0.88, 0.08 cm, and 0.00 cm) and posterior (0.96, 0.08 cm, and 0.04 cm) upper arm and anterior (0.98, 0.07 cm, and 0.01 cm) and posterior (0.95, 0.10 cm, and 0.04 cm) thigh.²³ SM index was calculated as SM divided by height in meters squared (kg/m²).

Thigh MTH ratio and isolated MTH by ultrasound

As described above, thigh MTH was measured using B-mode ultrasound on anterior and posterior of the thigh. To evaluate site-specific muscle loss of the thigh, the ratio of anterior and posterior thigh MTH (A50:P50 MTH) was calculated.^10,24 We also measured isolated MTH of the vastus lateralis (mid-thigh) and gastrocnemius medialis (at 30% proximal between the lateral malleolus of the fibula and the lateral condyle of the tibia) as described previously.²³ Briefly, the ultrasound transducer was placed perpendicular to isolated MTH for each muscle. With ultrasound images, the distance between subcutaneous adipose tissue–muscle interface and inter-muscular interface was adopted as isolated MTH.

Walking performance

Maximum walking time was measured by timing each subject as they walked across a 10-meter corridor on a hard-surfaced floor. The width of the corridor was set at 1-meter to encourage subjects to maintain a straight course. Subjects performed two timed trials. Subjects were asked to walk down the corridor as fast as possible without running. Times were calculated using a digital stopwatch (ADMD-001, SEIKO, Tokyo, Japan). The best time was used for maximum walking time. Zigzag walking time was measured using a 10-meter walkway. Four cones were placed 2 meters apart on the floor between the start and finish points.¹¹ The cones were set to alternate from side to side with a distance of 0.5-meters from a line drawn through the start and finish points. The subjects were asked to walk as quickly as possible without breaking into a jog/run. The test started with the subject standing on the start point. The subject then walked around the outside of each cone and walked through the finish point. The elapsed time from the subject passing the start and finish point was recorded. The best time of two trials was used for zigzag walking time.

Statistical analysis

Results are expressed as means and standard deviations (SD). Differences in the dependent variables between masters cyclists and moderately active young men were tested for significance by using unpaired Student t-tests. Before comparisons were made, the Shapiro–Wilk test was used to examine the dependent variables for normality of distribution. Consequently all variables obtained were normally distributed. Pearson product correlation coefficients were performed to determine the relationship between DXA-estimated aLT and ultrasound-predicted total SM as well as between walking performance or bone mineral density and aLT index/SM index. Statistical significance was set at p≤0.05.

Results

Master cyclists were older than moderately active young men, but body mass and BMI were similar (p<0.05) between groups. DXA- and ultrasound-estimated percent body fat and FFM were also similar (p>0.05) between masters cyclists and young men. However, FFM index was higher (p=0.02) in cyclists compared to young men (Table 1).

Table 1.

Body Composition in Masters Cyclists and Moderately Active Young Men

	Young men (n=13)	Master cyclists (n=14)	p value
Age (years)	23 (4)	61 (6)	<0.001
Standing height (meters)	1.81 (0.06)	1.75 (0.06)	0.009
Body mass (kg)	79.3 (10.8)	78.9 (9.1)	0.923
Body mass index (kg/m²)	24.2 (3.3)	25.8 (2.1)	0.158
Body fat_DXA (%)	20.5 (7.0)	19.2 (6.3)	0.607
Body fat_ultra (%)	22.1 (5.7)	20.6 (5.0)	0.459
Fat-free mass_ultra (kg)	61.4 (6.9)	62.6 (7.4)	0.686
Fat-free mass index_ultra (kg/m²)	18.7 (1.8)	20.4 (1.6)	0.016

DXA, dual energy X-ray absorptiometry; ultra, ultrasound.

There were no significant (p>0.05) differences in absolute and relative SM, arm and leg lean mass, or aLT between masters cyclists and young men. Anterior and posterior MTH as well as A50:P50 MTH ratio was similar (p>0.05) between groups. Isolated MTH of the gastrocnemius medialis was higher (p=0.024) in young men than in masters cyclists, although vastus lateralis MTH was similar between groups (Table 2).

Table 2.

Skeletal Muscle Mass, Areal Bone Mineral Density, and Walking Performance in Masters Cyclists and Untrained Young Adults

	Young men (n=13)	Master cyclists (n=14)	p value
Thigh SM_ultra (kg)	10.8 (1.5)	10.3 (1.1)	0.364
Thigh SM index_ultra (kg/m²)	3.28 (0.41)	3.36 (0.25)	0.543
Total SM_ultra (kg)	28.5 (3.7)	27.8 (4.2)	0.615
Total SM index_ultra (kg/m²)	8.69 (0.94)	9.04 (0.88)	0.333
Arm lean mass_DXA (kg)	6.9 (1.4)	6.9 (1.5)	0.978
Leg lean mass_DXA (kg)	20.3 (2.7)	20.2 (2.6)	0.964
Appendicular lean mass_DXA (kg)	27.1 (3.9)	27.1 (4.0)	0.983
Appendicular lean mass index_DXA (kg/m²)	8.25 (0.95)	8.83 (0.88)	0.117
Muscle thickness_ultra (cm)
Anterior thigh 50% (A50)	5.56 (0.68)	5.56 (0.55)	0.991
Posterior thigh 50% (P50)	6.30 (0.67)	6.29 (0.48)	0.975
A50:P50 ratio	0.89 (0.11)	0.89 (0.11)	0.973
Vastus lateralis	2.54 (0.40)	2.56 (0.31)	0.853
Gastrocnemius medialis	2.22 (0.31)	1.95 (0.27)	0.024
Bone mineral density_DXA (grams/cm²)
Femoral neck	0.916 (0.125)	0.760 (0.124)	0.003
Lumbar spine (L1–L4)	1.044 (0.152)	1.007 (0.146)	0.522
10-meter walking time (sec)
Straight	3.7 (0.4)	3.8 (0.7)	0.693
Zig-zag	4.9 (0.5)	5.1 (0.6)	0.469

SM, skeletal muscle mass; DXA, dual energy X-ray absorptiometry; ultra, ultrasound.

Lumbar spine aBMD was similar between groups, but femoral neck aBMD was significantly lower (p=0.003) in masters cyclists compared to young men. Maximum straight and zigzag walking times were also similar between masters cyclists and young men (Table 2).

There was a strong correlation between aLT and total SM in master cyclists (r=0.75, p=0.002), young men (r=0.90, p<0.001), and in the overall sample (r=0.91, p<0.001). Using the combined sample, maximum straight walking time did not correlate with either SM index (r=−0.38, p=0.052) or aLT index (r=−0.24, p=0.235). Zigzag walking time was negatively correlated with SM index (r=−0.45, p=0.019), but not with aLT index (r=−0.27, p=0.169). There was a significant correlation between SM index and lumbar spine (r=0.40, p=0.035) aBMD, but not femoral neck aBMD (r=0.29, p=0.136) when the overall sample was used. aLT index was not significantly correlated (p>0.05) with either femoral neck (r=0.19) or lumbar spine (r=0.22) aBMD.

Discussion

Although the current cross-sectional study had a small sample size composed only of men, our findings are consistent with those of our previous study employing a larger sample size.²⁵ The previous study found a similar value as the present one where the SM index in young caucasian men averaged 8.8 kg/m². In general, SM index gradually decreases with age and was 11% lower in men aged 50–59 years and 16% lower in men aged 60–69 years when compared to young men aged 20–29 years.¹⁰ In the present study, we focused on comparing moderately active untrained young men with masters cyclists to determine whether skeletal muscle mass would be similar between the two groups when regular moderate to vigorous cycling training was chronically performed in older men. Our findings showed that masters cyclists (mean age 61 years) had similar levels of absolute and relative SM as moderately active young men. Furthermore, DXA-estimated aLT was also similar between the two groups. Because the vastus lateralis is activated mainly during pedaling,^26,27 the MTH in the anterior thigh (quadriceps) as well as the vastus lateralis was preserved in masters cyclists in comparison to moderately active young men. In contrast, we found that the MTH of the gastrocnemius medialis was lower in the masters cyclists when compared to the moderately active young men. Percentage of type II fibers is approximately 60% and 50%, respectively, in the vastus lateralis and gastrocnemius muscles in sedentary men.²⁸ Reduced type II muscle fiber size is attributed mainly to age-related muscle mass loss.²⁹ Thus, the difference in gastrocnemius MTH between masters cyclists and moderately active young men obtained in this study may be associated with contributing factors other than muscle fiber types. Previous studies reported that MTH of the triceps surae gradually decreased with age in men,²³ and accelerometer-determined ambulatory activity, especially moderate and vigorous intensities, was positively correlated (r=0.41, p<0.01) with MTH of the triceps surae, but not MTH of the vastus lateralis.⁸ These results suggest that smaller gastrocnemius MTH in masters cyclists may be affected by decreasing daily physical activity with moderate/vigorous intensity. In addition, our masters cyclists did not perform high-intensity resistance training (three of 14 cyclists exercised against their own weight, i.e., abdominal flexion exercises and pushups or moderate-intensity resistance exercise). Therefore, our results suggest that regular moderate-to-vigorous cycling training may prevent age-related muscle mass loss of the thigh, but not in the triceps surae muscles. A previous study indicated that the prevalence of site-specific thigh muscle loss (low A50:P50 MTH ratio) displayed an age-related increasing pattern in both sexes, and that this loss appears before it can be detected at the whole-body level.¹⁰ With respect to the effect of habitual physical activity on site-specific thigh muscle loss, active older women who performed mainly walking, gateball, and gymnastic exercises (more than once a week) had greater anterior thigh muscle size than that of inactive older women.¹⁴ Compared to younger inactive women, however, anterior thigh muscle size was still lower in the active older women. These results suggest that low- and moderate-intensity physical activities are effective, but may not completely prevent age-related loss of anterior thigh muscle mass.¹⁴

In the present study, site-specific thigh muscle loss was not observed in masters cyclists (mean age 61 years). The vastus lateralis as well as biceps femoris muscles are activated regardless of cadence, and the activation increases with increment of workload in cyclists.²⁶ Therefore, moderate-to-vigorous cycling training performed in our masters cyclists (four to five times per week, 80–200 miles per week) seems to prevent site-specific thigh muscle wasting during aging and hence may help to preserve walking performance and physical independence.

Although our data suggest that chronic cycling training may help to preserve muscle mass over the life span, it may not confer the same benefits to clinically significant sites of the skeleton. Cycling is a non–weight-bearing physical activity that provides minimal load or strain to bone. Previous research suggests that male masters cyclists have reduced hip and lumbar spine aBMD when compared to their non-trained age-matched counterparts as well as young male competitive cyclists.³⁰ In support of these data, femoral neck aBMD in our cyclists was significantly lower compared to that of moderately active young men, although lumbar spine aBMD was not significantly different between groups. Some cross-sectional studies reported that femoral neck and lumbar spine aBMD in young cyclists was similar to that of young sedentary controls (exercising less 2 hr per week).^31,32 Considering the age-related decrease in aBMD, our results indicate that aBMD of the femoral neck is not preserved in high-level masters cyclists. Interestingly, the SM index correlated significantly with only lumbar spine aBMD when the overall sample was used. This is intriguing, especially since the vast majority of muscle activated during cycling does not act on the spine. One possibility for the discrepancy in our findings between femoral neck and lumbar spine aBMD may be due to different types of cycling terrain. Approximately half of our masters cyclists participated in cross-country cycling events, being exposed to different types of riding terrain. Previously, Warner et al. reported that mountain bike practitioners had higher aBMD compared to pure endurance road cyclists, which was perhaps due to the impact of riding on rougher terrain.³³ Although the magnitude of shear loading of the bone from muscle contractions would be related to the amount of activated muscle mass during cycling, lifelong road cycling exercise, including stationary bike, may not hold the same promise for maintaining bone health as our data suggest for muscle.

A number of limitations of this study should be mentioned. First, the frequency and weekly distance of cycle training were reported for the masters cyclists. However, exercise intensity may have more impact on age-related changes in muscle size and bone density than the frequency and distance of exercise. Second, although age-related declines in muscle mass/function and bone density are evident in normal lifestyle, we did not compare the masters cyclists to an age-matched nonathletic control group or young cyclists. Last, our samples comprised only men, so we cannot infer similar results for women. Additional research is needed to address these issues.

In conclusion, our results suggest that appendicular as well as site-specific thigh muscle loss with aging was not observed in masters cyclists. The maintenance of muscle mass in masters cyclists may preserve walking performance to similar levels as moderately active young adults. Therefore, cycling exercise may be a more practical form of long-term exercise for older adults due to the minimal impact imparted to the joints, as compared to a more weight-bearing option such as long-term running. However, long-term cycling does not preserve femoral neck aBMD.

Footnotes

Acknowledgments

We would like to thank the masters cyclists and students who participated in this study. The authors of this study wish to thank Professor Thomas W. Lombardo of the Department of Psychology, The University of Mississippi, for his help in recruiting the masters cyclists.

Author Disclosure statement

None of the authors had financial or personal conflicts of interest with regard to this study.

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