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Obesity Research & Clinical Practice (2015) xxx, xxx—xxx

ORIGINAL ARTICLE

Changes in lower extremity muscle mass and muscle strength after weight loss in obese men: A prospective study Bokun Kim a,∗, Takehiko Tsujimoto b, Rina So b,c, Kiyoji Tanaka b a

Doctoral Program in Sports Medicine, Graduate School of Comprehensive Human Sciences, University of Tsukuba, Ibaraki, Japan b Faculty of Health and Sports Sciences, University of Tsukuba, Ibaraki 305-8574, Japan c Japan Society for the Promotion of Science, Tokyo, Japan Received 13 September 2014 ; received in revised form 29 November 2014; accepted 4 December 2014

KEYWORDS Obesity; Weight loss; Lower extremity muscle mass; Lower extremity muscle strength

Summary Background: Obesity is not only associated with internal diseases but also with surgical problems. Surgical diseases related to obesity frequently occur in the load bearing joints of the lower limbs. To decrease the occurrence of surgical diseases related to obesity, weight loss has been recommended. It is important for obese men to maintain muscle mass and muscle strength after weight loss because low muscle mass and muscle strength are also related to the occurrence of surgical diseases. To date, the importance of muscle mass and muscle strength after weight loss in obese men has been underappreciated. Objective: The purpose of this study was to investigate changes in lower extremity muscle mass and muscle strength resulting from a weight loss programme consisting of caloric restriction and exercise. Methods: All participants concurrently attended a 12-week diet class 1 day/week and a 12-week exercise class 3 days/week. Body weight and body composition by dual-energy X-ray absorptiometry and knee extensor strength by dynamometry were assessed. Results: The weight loss programme led to a 14.1% weight loss accompanied by significant loss of leg muscle mass, static maximal muscle strength, dynamic maximal muscle strength and dynamic muscle endurance but not with significant loss of dynamic muscle power. Decline of muscle strength was related to a decrease in

∗ Corresponding author at: Graduate School of Comprehensive Human Science, University of Tsukuba, 1-1-1 Tennodai, Tsukuba 305-8577, Japan. Tel.: +81 29 838 5600x8365; fax: +81 29 838 2602. E-mail address: [email protected] (B. Kim).

http://dx.doi.org/10.1016/j.orcp.2014.12.002 1871-403X/© 2015 Published by Elsevier Ltd on behalf of Asia Oceania Association for the Study of Obesity.

Please cite this article in press as: Kim B, et al. Changes in lower extremity muscle mass and muscle strength after weight loss in obese men: A prospective study. Obes Res Clin Pract (2015), http://dx.doi.org/10.1016/j.orcp.2014.12.002

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B. Kim et al. muscle mass, but not completely dependent on a decrease in muscle mass. Body weight-normalised muscle strength increased significantly. Conclusion: We recommend utilising resistance exercise to restore muscle mass and muscle strength in the legs after substantial weight loss. © 2015 Published by Elsevier Ltd on behalf of Asia Oceania Association for the Study of Obesity.

Introduction Obesity is linked to many chronic diseases such as diabetes, hypertension, heart disease and some cancers [1]. In addition, obesity is not only associated with such internal diseases, but is also associated with surgical diseases. Disorders of the musculoskeletal system frequently occur in the load bearing joints of the lower limbs and the low back [2]. As musculoskeletal system disorders worsen over time, obese individuals tend to avoid regular weight bearing exercise [3]. As a result, muscles are weakened and weight gain is exacerbated [4]. Because of this, weight loss is an important tool to break this vicious cycle [5,6]. Losses of muscle mass and strength may have undesirable effects on physical function and metabolism [7]; low muscle mass and strength after weight loss are also related to occurrence of musculoskeletal system disorders [8]. Accordingly, it is necessary to decrease fat mass while maintaining muscle mass and muscle strength in order to prevent obesity-related surgical disease. According to existing reports, weight loss programmes focused on caloric restriction have a desirable influence on weight loss, but unfortunately the rate of muscle mass and muscle strength loss is high [7,9]. On the other hand, while weight loss programmes focused on exercise suppress losses of muscle mass and muscle strength, the rate of weight loss is low and it is possible that musculoskeletal system disorders may increase [7,10]. These findings suggest that while weight loss with caloric restriction may induce loss of muscle strength, exercise combined with caloric restriction may suppress the loss of muscle strength. The association between body weight and the occurrence of musculoskeletal system disorders is strongest in knee joint [2]. Considering that the knee joint is supported and controlled by the femoral muscle, maintenance of muscle mass and muscle strength in the femoral muscle is especially

important after weight loss. However, only a limited number of studies on lower extremity muscle mass and muscle strength after weight loss programmes in obese men have been reported. This is due, in large part, to the fact that the importance of muscle mass and muscle strength in obese men has been underappreciated. Thus, the purpose of this study was to investigate changes in lower extremity muscle mass and muscle strength resulting from a weight loss programme consisting of caloric restriction and exercise.

Methods Experimental design Obese men took part in a 12-week weight loss programme consisting of caloric restriction and comprehensive exercise. Every assessment was executed before beginning the weight loss programme and repeated within 2 weeks after completing the weight loss programme. The primary outcomes of the present study were changes in lower extremity muscle mass and muscle strength after the weight loss programme.

Participants We recruited participants from communities which are advertised in local newspapers and distributing study flyers. Eligibility criteria for participation in this study were as follows: body mass index (BMI) > 25 kg/m2 according to the domestic obesity guidelines and age between 30 and 65 years [11]. Participants were eligible for the present study if complete weight loss programme data on body composition and muscle strength from baseline and 12-week follow up were available. As described in Fig. 1, 97 participants were included in the study, but only 60 participants were included in the data analysis. The remaining 37 participants were not

Please cite this article in press as: Kim B, et al. Changes in lower extremity muscle mass and muscle strength after weight loss in obese men: A prospective study. Obes Res Clin Pract (2015), http://dx.doi.org/10.1016/j.orcp.2014.12.002

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Changes in lower extremity muscle mass and muscle strength: A prospective study

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Figure 1 Flow diagram of the participants

included in the analysis for the following reasons: 2 dropped out of weight loss programme for private reasons, 4 of them had incomplete data and 31 did not take part in the muscle strength assessment. We permitted participants not to take parts in the muscle strength assessment among participants who do not desire for muscle strength assessment, because one of the purposes on study was the health support in the region. The study purpose and design were adequately explained to every participant before they gave written informed consent. The research protocol was approved by the institutional review board at the University of Tsukuba.

Weight loss programme We conducted caloric restriction and exercise classes aimed at positively influencing the participants’ lifestyles. Details of these classes are as follows. Caloric restriction class: This class included a weekly group-based, 90-min instructional session once a week for 12 weeks. In each class, participants received low-calorie diets and attended eating-behaviour-themed lectures. Dieticians instructed participants to ingest a well-balanced, 1680 kcal per day diet. Participants kept a daily food diary in which they recorded all the food they ate. At each class, the dieticians reviewed

the participants’ diaries and offered individualised feedback to participants regarding energy intake and nutritional balance. Exercise class: Every participant took part in a 90-min combined exercise programme 3 days/week for 12 weeks. Each session began with 10—20 min of warm-up activities such as stretching. This was followed by the main exercise, 40—60 min of brisk walking and jogging in the outdoors. On rainy days, indoor exercise using stationary cycling and ladder climbing was the main exercise. Each session concluded with 10—20 min of resistance exercise with body weight and cool-down exercises. Every exercise was executed under the supervision of several trained physical trainers at the University of Tsukuba. Participants were encouraged to exercise at their maximum heart rates’ level or near their maximum heart rates’ level. Heart rates were monitored by short-range telemetry (Polar RS400, Kempele, Finland). Participants were allowed to participate in their preferred type of physical activity on days without exercise class.

Body composition Body composition was assessed by whole-body dual energy X-ray absorptiometry (DEXA; QDR 4500, Hologic Inc., Bedford, MA). To assess body composition, the participants were positioned in a supine

Please cite this article in press as: Kim B, et al. Changes in lower extremity muscle mass and muscle strength after weight loss in obese men: A prospective study. Obes Res Clin Pract (2015), http://dx.doi.org/10.1016/j.orcp.2014.12.002

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B. Kim et al.

position with the arms held against the sides of the body. Hologic software was used to analyse the assessments, yielding estimates of fat, lean, and bone tissue mass (in kilograms). Extended analyses were used to divide the body composition results into arms, legs, and trunk, yielding data on fat, lean, bone tissue mass for each body region. Leg muscle mass was calculated using leg lean mass excluding leg bone mass [12].

Muscle strength Isometric and isokinetic knee extensor strength was assessed with a commercial dynamometer (Biodex System 3: Biodex Medical Systems, Shirley, NY). Biodex System 3 has been found to be acceptably valid and reliable regarding joint torques and positions [13]. The participants were seated with the back supported and hips flexed at 120◦ and were secured to the seat of dynamometer with thigh and pelvis straps. Visual inspections were conducted to correctly align the axis of rotation of the knee with the axis of rotation of the Biodex System 3 before each trial. The isometric assessment was executed with the knee extended at 60◦ . The 60◦ knee extension position provides closeto-optimum muscle lengths for the quadriceps in order to produce maximal force. We surmised that there might be a possibility of different results in isokinetic assessments when angular velocities were different. Therefore, we assessed isokinetic muscle strength at different angular velocities. Angular velocities of 60◦ /s and 180◦ /s have been widely used in isokinetic assessments to evaluate isokinetic muscle strength. In the isometric assessment, the protocol consisted of 3 maximal efforts (each extension lasted 3 s), with a 15-s pause between extensions. In the isokinetic assessment of angular velocity at 60◦ /s and 180◦ /s, participants executed 3 and 12 maximal extensions, respectively. The highest muscular force output at any moment during a repetition was defined as the peak torque, reported in absolute terms (N m), and normalised to body weight, represented as body weight-normalised (N m/kg) peak torque. The amount of work accomplished for an entire set defined the total work and is reported as an absolute (W), while the average of total work divided by time defined the average power and is reported as an absolute (J). We adopted the peak torque in isometric assessment to evaluate static maximal muscle strength, the peak torque in isokinetic assessment to evaluate dynamic maximal muscle strength, the amount of work in isokinetic assessment to evaluate dynamic muscle endurance and the average power in isokinetic assessment to

evaluate dynamic muscle power. Every assessment was executed on both legs and we calculated the average of strength in both legs for lower extremity muscle strength.

Statistical analysis Data are expressed as the mean ± standard deviation (SD) values. A comparison of variables before and after the weight loss programme was made using the paired t-test. Partial correlation analysis was performed to remove the effect of age between variables before the weight loss programme and between changes in variables before the weight loss programme to follow up after the weight loss programme. To evaluate whether change in muscle mass is correlated with change in body weight and whether change in muscle strength is correlated with change in muscle mass, partial correlation analysis was applied to remove the effect of age. P < 0.05 was considered to indicate statistical significance. Every statistical analysis was performed with SPSS software, version 20.0 (IBM Inc., Armonk, NY, USA).

Results Demographic information, body composition and muscle strength characteristics before and after taking part in the weight loss programme are presented in Table 1. During the weight loss programme, the participants lost an average −12.1 ± 4.0 kg (−14.1 ± 4.4%, P < 0.01) of body weight. After weight loss, significant changes were found in both body composition and muscle strength. Whole body lean mass, whole body fat mass, leg muscle mass and leg fat mass were significantly decreased (by −5.1 ± 2.3 kg, −6.6 ± 2.1 kg, −1.6 ± 2.3 kg and −1.9 ± 0.9 kg, respectively; P < 0.01). Static maximal muscle strength (−9.1 ± 28.2 N m at 60◦ ; P < 0.05), dynamic maximal muscle strength (−11.9 ± 23.9 N m at 60◦ /s and −6.9 ± 14.8 N m at 180◦ /s, respectively; P < 0.01) and dynamic muscle endurance (−24.5 ± 68.4 N m at 60◦ /s and −71.2 ± 189.5 N m at 180◦ /s, respectively; P < 0.01) declined significantly, whereas dynamic muscle power (−1.9 ± 15.4 N m at 60◦ /s; P = 0.34 and −3.4 ± 28.5 N m at 180◦ /s; P = 0.36) did not decline significantly and body weight-normalised muscle strength (0.3 ± 0.3 N m/kg at 60◦ , 0.2 ± 0.3 N m/kg at 60◦ /s and 0.7 ± 0.3 N m at 180◦ /s, respectively; P < 0.01) was significantly increased. Every result in the dynamic strength assessment was correlated at angular velocities of 60◦ /s and 180◦ /s, contrary to our assumption before the weight loss programme.

Please cite this article in press as: Kim B, et al. Changes in lower extremity muscle mass and muscle strength after weight loss in obese men: A prospective study. Obes Res Clin Pract (2015), http://dx.doi.org/10.1016/j.orcp.2014.12.002

Before (range) 49.5 ± 9.2 (31.0, 64.0) 171.8 ± 5.6 (161.2, 193.0) 86.1 ± 8.9 (70.3, 120.0) 29.1 ± 2.2 (25.0, 36.3) 61.5 ± 6.5 (51.2, 76.3) 21.5 ± 4.6 (14.6, 36.7) 20.3 ± 2.9 (16.8, 35.8) 6.7 ± 1.8 (4.1, 12.0) 204.0 2.4 180.4 2.1 501 108.3 117 1.4 1323.8 165.6

± ± ± ± ± ± ± ± ± ±

41.2 (106.2, 300.0) 0.4 (1.2, 3.1) 38.1 (99.3, 263.8) 0.4 (112.8. 274.5) 97.1 (221.4, 719.5) 25.2 (44.0, 163.8) 28.0 (55.8, 202.8) 0.3 (62.6, 194.7) 307 (561.1, 1976.3) 46.7 (62.9, 268.2)

After (range)

Change (95% CI)

P

74.0 25.0 56.4 14.9 18.8 4.8

± ± ± ± ± ±

9.1 2.4 6.1 4.8 2.0 1.5

(60.4, 114.0) (21.3, 31.1) (46.7, 74.2) (8.2, 34.9) (15.7, 25.8) (2.8, 11.0)

−12.1 −4.1 −5.1 −6.6 −1.6 −1.9

± ± ± ± ± ±

4.0 1.3 2.3 2.1 2.3 0.9

(−13.1, −11.1) (−4.4, −3.8) (−5.7, −4.5) (−7.2, −6.1) (−2.2, −1.0) (−2.1, −1.7)

Changes in lower extremity muscle mass and muscle strength after weight loss in obese men: A prospective study.

Obesity is not only associated with internal diseases but also with surgical problems. Surgical diseases related to obesity frequently occur in the lo...
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