Abstract
It is unknown whether or not the daily swim training distances of master swimmers (MS) affect the observed changes in skeletal muscle mass (SM) and physical function commonly associated with the aging process. Twenty-two male MS aged 52–82 years were divided into two groups based upon training distance: High MS (>3000 meters swim/session and 4.1 times/week; n=11) and moderate MS (1500–2800 meters swim/session and 3.4 times/week; n=11). Eleven age- and body mass index–matched older (aged 56–80 years) men served as controls (AMC). Subjects who performed resistance training were excluded in this study. Muscle thickness (MTH) was measured by ultrasound at nine sites on the anterior/posterior aspects of the body (forearm, upper arm, trunk, thigh, and lower leg), and from this, total and segmental SM mass values were estimated. Thigh MTH (anterior:posterior mid-thigh, A50:P50) ratio was calculated to assess the site-specific thigh muscle loss. Straight and zigzag walking performance and maximum knee extension/flexion strength were also measured. Arm SM was greater for high MS and moderate MS than for AMC. Total SM index was higher for high MS than for moderate MS and AMC. A50:P50 ratio was greater for high MS than for AMC. Absolute and relative knee extension strength, but not flexion strength, was greater in high MS than in AMC. The A50:P50 ratio inversely correlated (p<0.05) with zigzag walking time, whereas relative knee extension strength positively correlated (p<0.05) with both straight and zigzag walking performance. Training distance in older MS may be an important factor for maintaining muscle mass and function in the aging process.
Introduction
T
Swimming as a recreational or competitive sport is rapidly increasing in popularity for a number of reasons. Recent estimates from England suggest that approximately 2.9 million people there swim at least once a week and that swimming is England's most popular participation sport. 13 In the United States, nearly 60,000 adult swimmers are registered members of the United States Masters Swimming, Inc. (USMS). 14 It is likely that nearly 50–100 times this number of adults swim daily at local recreational and YMCA aquatic centers nationwide. Several cross-sectional and intervention studies on older swimmers have been initiated and have reported positive cardiac and vascular effects of swimming. 15,16 Only one study, however, has examined the effects of aquatic physical activity on muscle mass and function in older athletes. 17 As might be hypothesized, due to upper body predominance during swim propulsion, no difference in quadriceps muscle CSA or knee extension strength between master swimmers (MS) and age-matched untrained controls was observed. 17 However, the daily swimming distances for subjects in this study appeared to be low, reportedly between 800 and 1000 meters per swim session, with exercise intensity during these sessions undefined. 17
Anecdotal reports in popular swim lay periodicals suggest that typical training distance may range from several thousand meters a session to as much as 15,000 meters a day for swimmers in their fifth, sixth, and seventh decades of life. 18 This training is not only greater in distance but much of it is at a moderate to high intensity. Therefore, it is unknown whether or not these previously reported results are generalizable or if they were associated with the minimal training distances and intensities per session for these swimmers. Thus, the purpose of this study is to determine if daily swim training distances of MS affects the observed changes in skeletal muscle mass (SM) and physical function commonly associated with the aging process. We hypothesized that MS completing an adequate amount of swimming distance regularly at moderate-to-high intensities should have higher SM and muscular function compared with age-matched untrained controls.
Methods
Subjects
Twenty-two male MS (aged 52–82 years) and 11 age- and body mass index (BMI)-matched moderately active men (aged 56–80 years) volunteered for the study. Before participation was initiated, a written description of the purpose and safety of the study was distributed to potential participants and informed consent was obtained. The study was conducted according to the Declaration of Helsinki and was approved by the Human Subjects, Institutional Review board for Human Experiments of the Indiana University.
The MS were recruited by word of mouth and by information fliers posted on the university campus and at the USMS National Championship. In this study, a MS is defined as a registered member of the USMS. To qualify for study participation, volunteers had to be at least 50 years of age and have no musculoskeletal, neuromuscular, or cardiovascular-pulmonary conditions that would impair their training program. MS who participated in moderate- or high-intensity resistance training were excluded from participation because it was thought this would confound the results. In the present study, the MS were divided into two groups: High swimming distance (>3000 meters per session; high MS, n=11) and moderate swimming distance (1500–2800 meters per session; moderate MS, n=11). Age- and BMI-matched controls (AMC), who partook in some aerobic-type exercises (two or less times per week), were also recruited from the university campus and surrounding areas. Similar to the MS though, AMC who participated in moderate- or high-intensity resistance training were excluded from participation. Physical characteristics and training history of each group are indicated in Table 1.
Perceptional swimming intensity was assessed based on a Borg scale (range 6–20). High swimming intensity was defined as a Borg scale rating 14 or higher (hard) during training sessions.
Two of the high MS regularly perform aerobic exercise (∼60-min run or ∼90-min bike), two to three times per week.
Two of the moderate MS regularly perform aerobic exercise (20-min run or 30-min bike), two to five times per week.
MS, master swimmers.
Muscle thickness measurements
Muscle thickness (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 subjects stood with their elbows and knees extended and relaxed because MTH for the prediction equation of SM was measured in a standing position. A linear transducer with a 5-MHz scanning head was coated with water-soluble transmission gel to provide acoustic contact and reduce pressure by the scanning head to achieve a clear image. The scanning head was placed perpendicularly on the skin surface of the measurement site using the minimum pressure required, and cross sections of each muscle were imaged. Two images from each site were printed (Sony UP-897MD, Tokyo, Japan), and mean values of each site were used for data analysis. 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 for limb muscles. For measurements in trunk, MTH was defined as the distance between the adipose tissue–muscle interface and the deep muscle fascia interface.
Test–retest reliability of MTH measurements using intra-class correlation coefficient (ICC3,1), standard error of measurement (SEM), and minimum difference was previously determined from 15 middle-aged subjects for anterior (0.88, 0.08 cm, and 0.22 cm) and posterior (0.96, 0.08 cm, and 0.22 cm) upper arm and anterior (0.98, 0.07 cm, and 0.19 cm) and posterior (0.95, 0.10 cm, and 0.28 cm) thigh. 20 To evaluate site-specific muscle loss, the anterior-to-posterior (A50:P50) MTH ratios of the thigh were calculated.
Skeletal muscle mass estimations
Total and segmental SM was estimated from ultrasound-derived prediction equations that converted MTH to SM. 21 A positive, statistically significant correlation (R 2 =0.94) has previously been observed between magnetic resonance imaging–measured total SM and ultrasound-predicted total SM. 21 Recently, we examined the relationship between dual-energy X-ray absorptiometry–determined appendicular lean tissue mass and total SM predicted by ultrasound and found a similar, positive, statistically significant correlation (R 2 =0.95) between these two methods. 22
Body composition and anthropometry
Subcutaneous fat thickness was measured using ultrasound at nine sites, as described previously. 19 Body density was estimated from subcutaneous fat thickness using an ultrasound-derived prediction equation. 19 Percent body fat (%fat) was calculated from body density using the Brozek equation. 23 Previously, we reported that the standard error of the estimate of body density calculated using the ultrasound equations is approximately 0.006 g/mL (or an error of about 2.5 %fat) in a non-obese Japanese population. 19 Fat-free mass (FFM) was estimated as total body mass minus fat mass. Body mass and standing height were measured to the nearest 0.1 kg and 0.1 cm, respectively, by using an electronic weight scale and a stadiometer. BMI was defined as body mass/height 2 (kg/m2).
Knee joint strength measurements
Maximum voluntary isometric strength of the knee extensors and flexors was determined using a Cybex II Dynamometer (CYBEX, Ronkonkoma, NY). Subjects were carefully familiarized with the testing procedures of voluntary force production before testing. The subjects were seated on a chair with their hip joint angle positioned at 85°. The center of rotation of the knee joint was visually aligned with the axis of the lever arm of the dynamometer, and the ankle of the right leg was firmly attached to the lever arm of the dynamometer with a strap.
After a warm-up consisting of submaximal contractions, the subjects were instructed to perform maximal isometric (maximum voluntary contraction [MVC]) knee extension at a knee joint angle of 90° and knee flexion at a knee joint angle of 40°. A knee joint angle of 0° corresponded to full extension of the knee. If MVC strength for the first two trials varied by >5%, an additional MVC was performed. Torque output from the dynamometer was recorded by a personal computer, and the highest torque value was used for data analysis. The dynamometer was calibrated for the recorded torque values using known weight. The coefficient of variation for this test in our laboratory was 7% maximum isometric knee extension and flexion strength divided by body mass was calculated for evaluating knee joint strength index.
Walking performance
Maximum straight walking time was measured using a 10-meter walkway. The width of the corridor was set at 1 meter to encourage subjects to maintain a straight course. Subjects were asked to walk down the corridor as fast as possible without running (one foot must be on the floor). Zigzag walking time was also 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 meter from a line drawn through the start and finish points. The test started with the subject standing on the start point. The subject then walked around the outside of each cone through the finish point. The elapsed time from the subject passing the start and finish point was recorded using a digital stopwatch (ADMD-001, Seiko, Tokyo). The fastest time of two trials was used for maximum straight and zigzag walking time. Test–retest reliability of walking tests using ICC3,1, SEM, and minimal difference was determined from 21 older adults (11 men and 10 women) for the maximum straight walking test (0.93, 0.27, and 0.74 sec) and zigzag walking test (0.96, 0.21, and 0.59 sec).
Statistical analysis
Results are expressed as means and standard deviation (SD). The differences between groups for age, height, body mass, BMI, body composition, MTH, SM index, strength, and walking performance were tested for significance by one-way analysis of variance (ANOVA), followed by pairwise comparisons using the Tukey multiple comparison procedure if a significant F test was obtained. If variances were unequal, the Dunnett C procedure was performed. Pearson product correlation coefficients were performed to determine the relationship between thigh MTH and knee joint strength and between walking performance and thigh MTH ratio or knee joint strength index. p values<0.05 were considered statistically significant.
Results
The mean age of the three groups was 64 (SD 8), 66 (SD 8), and 69 (SD 9) years for high MS, moderate MS, and AMC, respectively. BMI, body fat, and FFM were similar among MS (high MS and moderate MS) and AMC. The MS were all training actively and had been training for, on average, the last 30 years (range 7–55 years) for high MS and 26 years (range 5–54 years) for moderate MS. As planned, average swim training distance per session was greater in high MS than in moderate MS. Self-reported percentage of high-intensity swim distance (>70% of maximum effort) during swimming sessions was 69% for high MS and 41% for moderate MS. The AMC were moderately active (two or less times per week) and had been so for at least the last 5 years (Table 1).
High MS had greater MTH at anterior and posterior upper arm, anterior trunk, anterior thigh, and anterior and posterior lower leg compared with the AMC. On the other hand, moderate MS only had greater MTH at the posterior upper arm compared with the AMC. Thigh MTH ratio was higher in high MS than in AMC (Table 2).
Significant group difference from older control men.
Significant group difference from moderate MS.
MS, master swimmers; A, anterior; P, posterior.
Compared with AMC, arm SM was higher in both high MS and moderate MS; however, total and thigh SM was higher in only high MS. Total SM index was greater in high MS than in moderate MS and AMC. Absolute and relative knee extension strength was greater in high MS compared with AMC, whereas knee flexion strength and walking performance were similar between the two groups. There were no differences in knee joint strength and walking performance between moderate MS and AMC (Table 3).
Significant group difference from older control men.
Significant group difference from moderate MS.
MS, master swimmers; SM, skeletal muscle mass; Nm, newton-meters; BM, body mass.
Thigh (A50:P50) MTH ratio was inversely correlated with zigzag walking time (r=−0.355, p=0.042) but not straight walking time (r=−0.200, p=0.264). Knee extension strength index was inversely correlated with straight (r=−0.492, p=0.004) and zigzag (r=−0.466, p=0.006) walking time. On the other hand, knee flexion strength index was correlated only with straight walking time (r=−0.399, p=0.021), but not zigzag walking (r=−0.224, p=0.209). Anterior thigh MTH was strongly correlated with knee extension strength (r=0.703, p<0.001), whereas posterior thigh MTH was correlated knee flexion strength (r=0.388, p=0.025).
Discussion
The primary findings of the present study were that: (1) MS who completed greater daily swim distances had greater total SM index and thigh MTH ratio compared with age- and BMI-matched control men, (2) absolute and relative (divided by body mass) knee extension strength was also higher in MS who completed greater daily swim distances than in older control men, and (3) relative knee extension and flexion strength were inversely correlated with walking performance, although group differences in walking performance were not apparent.
There is strong evidence from the present data suggesting that muscle hypertrophy is observed in the posterior upper arm (triceps brachii) muscle in MS. In the present study, posterior upper arm MTH was, respectively, 40% and 27% greater in high MS and moderate MS when compared with “non-swimmers” of the same age and BMI. We use the term non-swimmers here only to differentiate these men from the men who regularly and routinely participate in swimming as their main mode of exercise. In other words, we are not stating that the “controls” do not know how to swim, rather, they simply do not.
Electromyogram (EMG)-determined muscle activity patterns during front crawl stroke phases indicate that the integrated EMG of the triceps brachii is highly activated (43% of maximum integrated EMG) in the aquatic elbow extension phase of the swim stroke. 24 Thus, it is appropriate that following an 8-week swimming program in previously untrained men (approximately 2000 meters per session, three times/week), type II fiber CSA of the triceps brachii has been reported to increase, on the average, by 24%. 25 This research supports our findings showing that MTH at six of nine measured sites as well as arm and thigh SM was greater in high MS compared with AMC. Most importantly, the total SM index in high MS (9.49 kg/m2) was significantly greater than moderate MS (8.28 kg/m2) and AMC (7.75 kg/m2). The SM index for the high MS is greater than that previously reported for young Caucasian men (8.8 kg/m2; mean age 31.4 years) using similar analytic techniques. 26 Previous research has shown total SM index gradually decreases with age, and is 11% lower in Japanese men aged 50–59 years (7.66 kg/m2) and 16% lower in Japanese men aged 60–69 years (7.24 kg/m2) when compared to Japanese young men (8.57 kg/m2) aged 20–29 years. 2 Therefore, our findings suggest that MS with higher swimming distances maintain a high SM index, even greater than that of active (but presumably non-swimming) young men.
In contrast to this, in the lower limbs, Klitgaard et al., 17 using less sophisticated technology, investigated the impact of swimming exercise on leg muscle morphology and function of MS. They reported that no difference was observed mid-thigh muscle CSA and knee extension strength between MS and age-matched untrained controls. However, the training distances of the MS in that study appears low (800–1000 meters per session) when compared to the training distances reported by the swimmers in the present study. Thus, as our results indicate, additional comparisons are difficult to make because of the difference in training distance. Nevertheless, in the present study, total and thigh SM and knee joint strength was similar between moderate MS (swim 1500–2800 meters per session) and AMC, although high MS (swim 3000–4000 meters per session) had greater SM and knee extension strength. The reasons for the effects of swimming distance on leg muscle morphology and function are largely unknown.
As mentioned earlier, Lavoie et al. 25 reported muscle fiber hypertrophy of the triceps brachii following an 8-week swimming training program. The subjects performed repeat sets of 50-, 100-, and 200-meter swims and an occasional longer distance (400 and 800 meters) swim, with total swimming distance approximating 2000 meters. The swimming speeds at each distance were adjusted to obtain a heart rate of 160 beats/min. The heart rate of 160 beats/min is comparable to an exercise intensity of 70%–80% heart rate reserve.
In the present study, the MS were asked to assess perceptional swimming intensity during training sessions, which was based on a Borg scale (range 6–20). 27 High swimming intensity was defined as a Borg scale rating of 14 or higher (hard). The self-reported percentage of high intensity swim distance (>70% of maximum effort [Borg Rating of Perceived Exertion scale >14]) during swimming sessions was estimated around 70% (range 50%–80%) in high MS and around 40% (range 25%–60%) in moderate MS. The estimated average high-intensity swim distance per session was approximately 2300 meters in high MS and 800 meters in moderate MS. The swim distance of approximately 2200 meters with high intensity is at a similar level observed with a previous study 25 that reported swimming training-induced arm muscle hypertrophy, although that study 25 did not measure changes in muscle size in the lower extremities. We recognize that this is self-reported and relatively undocumented. However, a number of our subjects participated in parallel study quantifying current active patterns. 28 Training was largely “interval” in nature and relatively intense rather than long, slow, and continuous. Heart rate estimates from these subjects during swim training were above 70% roughly 45% of the daily training time. Therefore, typical swim training may require not only longer distances but also moderate and vigorous intensities to maintain muscle size and strength in MS.
The reason for maintaining lower body muscle size and strength in high MS is largely unknown. It is predicted that intensity and duration of exercise differ between maintaining and enhancing muscle function and mass during the aging process. A recent study has revealed that aerobic exercise (60%–80% heart rate reserve) alters muscle protein metabolism and induces skeletal muscle hypertrophy. 29 Similarly, it is reported that high levels of long-term physical activity can provide a maintenance of motor units in exercising muscle. 30 In the present study, estimated swim distance completed at a high intensity (Borg scale >14) accounted for about 70% of total daily swim distance in high MS. In addition, swim fins are widely used for improving swim performance and have been associated with altering leg muscle activation during swim training sessions. 31 Although the mechanisms are currently speculative, future work may be able to delineate the physiological and molecular mechanisms involved with swimming-induced leg muscle hypertrophy.
A previous study of age-related muscle wasting indicated that the prevalence of site-specific thigh muscle loss (low A50:P50 MTH ratio) displayed an age-related pattern in both sexes and that muscle mass loss appears before it can be detected at the whole body level. 2 The major reason for a decreasing thigh MTH ratio would be due to lower anterior thigh MTH, because posterior thigh MTH was not significantly decreased among age groups under the age of 60 in men and under the age of 70 in women. 2,20
In support of these data, our findings in the present study showed that anterior thigh MTH was higher in MS with high swimming distances than in AMC, whereas posterior thigh MTH was similar among the three groups. A previous study reported a positive relationship between anterior-to-posterior thigh MTH ratio and duration of vigorous physical activity in middle-aged and older women. 32 In addition, we recently examined whether chronic vigorous exercise (masters cyclists) prevents the site-specific thigh muscle loss experienced in sedentary adults and found that the thigh MTH ratio was similar between master cyclists and young active men. 33 Interestingly, this is supported by research that has observed site-specific losses in motor units with advancing age. 34 A recent study demonstrated that the lifelong running can provide a localized maintenance of motor units in exercising muscle, but not systemically. 30 Thus, lifelong swimming exercise session with long distance (>3000 meters) may prevent the site-specific muscle loss of the thigh.
In the present study, thigh MTH ratio was inversely associated with zigzag walking performance but not straight walking time, although no significant group differences were found in walking performance. In other words, the higher the MTH ratio, the less time subjects took to complete the zigzag task. Consistent results were observed in a previous study that found a significant correlation between thigh MTH ratio and zigzag walking time, but not maximum straight walking, in middle-aged and older women. 11 Interestingly, knee extension strength index (torque divided by body mass) was also inversely associated with zigzag walking performance, although knee flexion strength index did not correlate to zigzag walking in the present study.
A recent study reported biomechanical factors contributing to quickness in lateral movements and found that extension torques of the hip, knee, and ankle joints contribute substantially to the changes in side-step distances, whereas hip abduction torque accelerates the center of mass laterally in the earlier phase of the movement. Thus, it is possible that the site-specific loss of anterior thigh muscle as well as reduced knee extension strength play a significant role in zigzag walking performance in older adults as well as in MS.
Our results indicated that knee extension as well as knee flexion strength index were inversely correlated with straight walking performance. Therefore, changes in knee joint strength index cause changes in walking performance regardless of the habitual activity pattern. Walking performance dramatically decreases in later life and is suggested to lead to the associated cardiovascular disease, mobility limitation, and mortality. 35,36 Factors that account for age-related declines in knee extension/flexion strength index include loss of thigh SM and/or increased body fat, changes in neurological characteristics with age, 37 selective loss of type II fibers, 38 and reduced specific force in both type I and type IIa single fibers. 39 In the present study, we did not measure specific force (strength divided by muscle CSA) in each muscle group. Considering the insignificant differences in walking performance among the groups, increase in knee joint strength index appears to be a beneficial and perhaps unanticipated “side effect” resulting from habitual swimming.
In the present study, we used an ultrasound technique to estimate total and segmental muscle mass. The prediction equation used in this study is a valid method to predict SM. 21,22 However, we could not use a standard technique such as dual-energy X-ray absorptiometry, which is widely viewed as the preferred method to assess body composition, due to limited availability of the subjects. In addition, our MS did not perform moderate- or high-intensity resistance training, and four of 22 MS exercised aerobic-type exercise in both high MS (n=2) and moderate MS (n=2). However, it was not possible to assess changes in daily physical activity and nutritional status with advancing age for each subject. Further cross-sectional and longitudinal studies into these issues are needed.
In conclusion, these results suggest that swimming distance in MS is an important factor for improving and/or maintaining muscle mass and function during the aging process. Although upper body measures are those most likely to improve in response to swim training, differences also are manifest in the lower limbs. Although we are not able to provide a complete description of the “dose response” to swimming per se, it does appear that in the present study “more is better” or “3000 meters per session and weekly four sessions as a rough guide.” Because the maintenance of the ability to walk is critical in terms of independence and general health and well being in older adults, it would appear that swim training may be a particularly beneficial activity in this regard. This may be particularly so when it is considered that it is non-impact in nature and the potential for falls during swimming is minimal.
Footnotes
Acknowledgments
The authors thank the individuals who participated in this study. We also thank Koichi Kitano and Hsuan-Yu Wan for their assistance in the testing of this study.
Author Disclosure Statement
No competing financial interests exist.
