Effects of resistance exercise and fortified milk on

J Appl Physiol 107: 1864–1873, 2009. First published October 22, 2009; doi:10.1152/japplphysiol.00392.2009.

Effects of resistance exercise and fortified milk on skeletal muscle mass, muscle size, and functional performance in middle-aged and older men: an 18-mo randomized controlled trial Sonja Kukuljan,1 Caryl A. Nowson,1 Kerrie Sanders,2 and Robin M. Daly1,3 1

Centre for Physical Activity and Nutrition Research, School of Exercise and Nutrition Sciences, Deakin University, Melbourne; 2Department of Clinical and Biomedical Sciences: Barwon Health, The University of Melbourne, Geelong; and 3Department of Medicine, The University of Melbourne, Western Hospital, Melbourne, Australia Submitted 15 April 2009; accepted in final form 19 October 2009

resistance training; fortified milk; muscle function

(PRT) is one of the few approaches that has been shown to enhance muscle strength, mass, and size in older adults and the elderly (19, 20, 30, 34, 35). However, most studies have reported considerable heterogeneity in the skeletal muscle response to training. For muscle hypertrophy to occur, there must be a net increase in muscle protein balance, that is, muscle protein synthesis must exceed protein breakdown (11). While PRT alone stimulates muscle protein synthesis (8, 40), it has been suggested that the greatest gains in muscle mass will occur with an energy intake that exceeds requirements to meet the additional demands of train-

PROGRESSIVE RESISTANCE TRAINING

Address for reprint requests and other correspondence: R. M. Daly, Dept. of Medicine, The Univ. of Melbourne, Western Hospital, Footscray, Melbourne 3011, Australia (e-mail: [email protected]). 1864

ing (9, 19) and/or an increased intake of specific nutrients, particularly dietary protein (18, 35, 36). To date, however, the findings from several intervention studies in older adults that have examined whether increased dietary protein or the ingestion of essential amino acids combined with PRT can promote muscle hypertrophy have produced contrasting results (10 –12, 18, 24, 35, 43). This could be attributed to variations in the intensity, duration, and frequency of training and/or to differences in the amount or source of protein consumed, habitual protein intakes, or the timing of ingestion relative to the resistance training bout. There is emerging evidence that the ingestion of dairy foods, particularly whole or fat-free milk, may represent an ideal food source to enhance muscle protein synthesis and thereby skeletal muscle hypertrophy. Recent findings in young adults have demonstrated that the consumption of whole milk after resistance training can promote muscle protein synthesis and/or inhibit protein breakdown, leading to an improved net muscle protein balance (17, 46). The mechanisms by which whole milk can enhance the effects of exercise on muscle have been reported to be related to the fact that milk contains a mix of casein protein, which is considered a “slow” protein that inhibits protein breakdown, and whey protein, which is referred to as a “fast” protein that stimulates synthesis (17, 46). However, there are also likely to be other factors present in whole milk (e.g., vitamins, minerals, and carbohydrates) that could contribute to these beneficial effects on muscle. Indeed, a study (23) in young healthy moderately active men (novice weightlifters) found that the chronic consumption of fluid skim milk after PRT was associated with greater gains in lean mass compared with isoenergetic soy or carbohydrate consumption, despite similar increases in dietary protein intakes between the groups throughout the intervention. Maintaining adequate serum levels of vitamin D (25-hydroxyvitamin D) in the elderly has also been recognized as being important for optimal musculoskeletal health. This is because low 25-hydroxyvitamin D levels have been associated with sarcopenia, an accelerated loss in muscle mass and strength (44), reduced gait speed and poor balance, and an increased risk of falling (5, 45). While supplementation with vitamin D or vitamin D plus calcium can improve lowerextremity muscle performance in the elderly (7, 16, 38, 39), no studies have examined the potential long-term synergistic skeletal muscle adaptations to PRT and the oral ingestion of fluid milk containing additional vitamin D3, calcium, and protein in middle-aged and older men.

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Kukuljan S, Nowson CA, Sanders K, Daly RM. Effects of resistance exercise and fortified milk on skeletal muscle mass, size, and functional performance in middle-aged and older men: an 18-mo randomized controlled trial. J Appl Physiol 107: 1864 –1873, 2009. First published October 22, 2009; doi:10.1152/japplphysiol.00392.2009.— Limited data have suggested that the consumption of fluid milk after resistance training (RT) may promote skeletal muscle hypertrophy. The aim of this study was to assess whether a milk-based nutritional supplement could enhance the effects of RT on muscle mass, size, strength, and function in middle-aged and older men. This was an 18-mo factorial design (randomized control trial) in which 180 healthy men aged 50 –79 yr were allocated to the following groups: 1) exercise ⫹ fortified milk, 2) exercise, 3) fortified milk, or 4) control. Exercise consisted of progressive RT with weight-bearing impact exercise. Men assigned to the fortified milk consumed 400 ml/day of low-fat milk, providing an additional 836 kJ, 1000 mg calcium, 800 IU vitamin D3, and 13.2 g protein per day. Total body lean mass (LM) and fat mass (FM) (dual-energy X-ray absorptiometry), midfemur muscle cross-sectional area (CSA) (quantitative computed tomography), muscle strength, and physical function were assessed. After 18 mo, there was no significant exercise by fortified milk interaction for total body LM, muscle CSA, or any functional measure. However, main effect analyses revealed that exercise significantly improved muscle strength (⬃20 –52%, P ⬍ 0.001), LM (0.6 kg, P ⬍ 0.05), FM (⫺1.1 kg, P ⬍ 0.001), muscle CSA (1.8%, P ⬍ 0.001), and gait speed (11%, P ⬍ 0.05) relative to no exercise. There were no effects of the fortified milk on muscle size, strength, or function. In conclusion, the daily consumption of low-fat fortified milk does not enhance the effects of RT on skeletal muscle size, strength, or function in healthy middle-aged and older men with adequate energy and nutrient intakes.

EFFECTS OF RESISTANCE EXERCISE AND MILK ON MUSCLE

The aim of this study, which was part of an 18-mo factorial design randomized controlled trial examining the effects of a multicomponent strength and weight-bearing exercise program with and without a milk-based nutritional supplement on bone mineral density in middle-aged and older men (29), was to investigate the independent and combined effects of these factors on muscle strength, skeletal muscle mass and size, and lower-extremity muscle performance. We hypothesized that exercise combined with fortified milk would result in a greater skeletal muscle response than either exercise or fortified milk alone. MATERIALS AND METHODS

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During the first 12-wk introductory training cycle, participants completed 3 sets of 15–20 repetitions at 50 – 60% of their 1 repetition maximum (1-RM) strength. Thereafter, the training volume was set at 2 sets of 8 –12 repetitions. This consisted of a warm-up set at 60 – 65% of 1-RM followed by a single training set at the following loads: for the first 4 wk of each 12-wk training cycle, the training load was set at an intensity of 60 –70% of 1-RM, which increased to 80 – 85% for the remaining 8 wk. For the first 12 mo, all participants were instructed to perform each repetition in a slow, controlled manner, with a rest of 1–2 min between sets. For the final 6 mo of training, the program switched from maximal strength to high-velocity powerbased training in which the participants were instructed to perform all repetitions for each exercise as rapidly as possible during the concentric (rising) phase and then return the resistance (load) through the eccentric (lowering) phase at a slow and controlled speed. The same training intensity (60 – 85% of 1-RM) was prescribed during this period. Analysis of the average resistance training load lifted per session, which was calculated from the sum of the number of repetitions completed multiplied by the weight (in kg) lifted for each set of all exercises completed throughout the program, revealed that the average load increased from 7,635 kg at 12 mo to 8,515 kg during the final 6 mo. The weight-bearing impact exercises were designed to load the lower extremities. For each session, three impact exercises were interspersed between the resistance training exercises. Participants were initially required to complete 3 sets of 10 repetitions for each exercise, which progressively increased to a maximum of 20 repetitions that varied in magnitude, rate, and distribution (direction) by either increasing the height of jumps and/or by introducing more complex movement patterns (29). Exercise compliance was computed from daily exercise cards completed by the men at the gymnasium and checked by records completed daily by the trainers, which were returned to the research staff every month. The personal trainers also recorded any adverse events or injuries associated with the program. Calcium- and vitamin D3-fortified milk. Participants assigned to the fortified milk were asked to consume 400 ml/day (2 ⫻ 200-ml tetra packs) of reduced-fat (⬃1%) ultrahigh temperature (UHT) milk, which was specifically formulated by Murray Goulburn Cooperative (Brunswick, Australia). This is equivalent to ⬃1.5 glasses of milk per day, which is in line with the current Australian dietary recommendations of 2–3 servings of dairy per day. Participants were encouraged to consume one tetra pack in the morning and another in the afternoon or evening, but not specifically before or after training. Each 200-ml milk tetra pack was fortified with additional calcium and vitamin D3 (total ⬃500 mg calcium and 400 IU vitamin D3 per 200 ml) and also contained 418 kJ energy, 6.6 g protein, 2.2 g fat, 11 g lactose, 100 mg sodium, and 250 mg phosphorous. The milk was fortified with a calcium salt derived from fresh milk whey. The vitamin D (vitamin D3) that was used to fortify the milk was obtained from DSM Nutritional Products (New South Wales, Australia). Six batches of the milk were produced over the 18-mo intervention with participants receiving a new batch every 3 mo. The calcium and vitamin D3 levels of each batch were analyzed by Murray Goulburn Cooperative before being distributed. The average (⫾SD) calcium and vitamin D3 levels per 100 ml for the six batches were 247 ⫾ 17 mg and 190 ⫾ 26 IU, respectively. Participants recorded the number of tetra packs consumed per day on compliance calendars, which were collected and checked every 3 mo. Compliance was calculated as a percentage by dividing the number of tetra packs consumed by the expected consumption each month and multiplied by 100. Anthropometry and body composition. Height was assessed using a Holtain wall stadiometer (Crymych, Dyfed). Weight was measured using an A&D UC-321 electronic scale to the nearest 0.1 kg. BMI (in kg/m2) was calculated as body weight (in kg) divided by height (in m2). Total body lean mass, fat mass, and percent body fat were assessed by dual-energy X-ray absorptiometry (Prodigy, GE Lunar, Madison, WI) with analysis software version 8.10.027. The short-term

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Participants. As described previously (29), 180 healthy communitydwelling Caucasian men aged 50 –79 yr were recruited from within the local community in Geelong and the surrounding areas in Victoria, Australia. Participants were excluded if they had taken calcium and/or vitamin D supplements, had participated in resistance training in the past 12 mo, participated in high-impact weight bearing activities for ⬎30 min for 3 times/wk in the preceding 6 mo, had a body mass index (BMI) of ⬎35 kg/m2, had a history of osteoporotic fracture or any medical condition or used medication known to affect bone metabolism, were lactose intolerant, consumed ⬎4 standard alcoholic drinks/ day, were current smokers, or had any chronic condition that might limit their ability to be involved in the intervention. In addition, men with normal to below average areal bone mineral density (total hip or femoral neck T-score between ⫹0.4 and ⫺2.4 SD) were included in the study. All men were required to obtain a medical clearance from their local physician to ensure that they were free of any contraindicated medical conditions to exercise based on American College of Sports Medicine guidelines (1). The study was approved by the Deakin University Human Ethics Committee and Barwon Health Research and Ethics Advisory Committee, and written consent was obtained from all participants. Study design. This 2 ⫻ 2 factorial design study was an 18-mo randomized controlled trial. The two factors were exercise and calciumand vitamin D3-fortified milk; each were tested on two levels so that the 180 participants were randomly allocated to one of the four groups: 1) exercise plus fortified milk (n ⫽ 45), 2) exercise alone (n ⫽ 46), 3) fortified milk alone (n ⫽ 45), or 4) control (n ⫽ 44). Before randomization, participants were stratified according to age (⬍65 or ⱖ65 yr) and baseline dietary calcium intake (⬍800 or ⱖ800 mg/day). Exercise training. Supervised exercise was performed 3 nonconsecutive days/wk for 18 mo in one of four community leisure facilities under the supervision of qualified exercise trainers. Each session lasted 60 –75 min and consisted of warm-up and cool-down activities, PRT, and moderate-impact weight-bearing exercises. During the first 4 wk of the program, all exercise sessions were supervised to ensure correct lifting and landing techniques and to monitor the appropriate amount of exercise and rest intervals. Thereafter, 1 session/wk was supervised to provide ongoing personal attention, tuition, and supervision to ensure that participants adhered to the principle of progressive overload. For the remaining two sessions, participants were instructed to seek assistance from local trained gymnasium staff when needed. As reported previously (29), the PRT included a combination of upper and lower body machine and free weights and exercises to strengthen the core musculature. The primary exercises used throughout the program included the following: squats (or leg presses), lunges, hip abduction and adduction, latissimus dorsi pull down (or seated row), back extension, and a combination of abdominal and core stability exercises. Additional exercises, including leg extensions, calf raises, bench presses, military presses, bicep curls, tricep extensions, and lumbopelvic and spine stabilization exercises, were also rotated throughout the program to ensure the development of muscle balance.

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dicted basal metabolic rate (22). On this basis, we excluded 18% and 27% of the all food diaries at 12 and 18 mo, respectively. Leisure time and habitual physical activity outside of the exercise intervention (in kJ/wk) were assessed using the Community Healthy Activities Model Program for Seniors physical activity questionnaire (42). Information on disease history was determined by questionnaire, and medication use (including calcium and vitamin D supplementation) was determined by a questionnaire at each visit (baseline, 12 mo, and 18 mo) and confirmed by an interview. Serum 25-hydroxyvitamin D levels. Fasting morning (8 –10 AM) blood samples (10 ml) were obtained from each participant’s antecubital vein at 12 and 18 mo. All serum samples were subaliquoted and stored at ⫺80°C until assayed (in duplicate). Serum 25-hydroxyvitamin D levels were measured using a DiaSorin immunoassay (Stillwater, MN). The mean interassay CV ranged from 3.9% to 5.8%. Statistical analysis. Statistical analyses were conducted using Stata Statistical Software release 10.0 (Stata, College Station, TX). Baseline characteristics between the groups were compared using ANOVA with a Tukey post hoc test. Pooled time series regression analysis for longitudinal data was used to test for an interaction between exercise and fortified milk. If no significant interactions were detected, the main effects of exercise (exercise plus fortified milk and exercise alone vs. fortified milk and control) and fortified milk (exercise plus fortified milk and fortified milk vs. exercise and controls) were examined. Serum 25-hydroxyvitamin D, gait speed, step test, and all sway measures were log transformed before analyses. Between-group differences were calculated by subtracting within-group changes from the baseline values in each group for each parameter. Separate models were used to assess the within-group changes, which were expressed either as absolute changes or as percent changes from baseline. RESULTS

Baseline characteristics. As previously reported (29), there were no significant differences between the four groups for any of the baseline characteristics (Tables 1–3), with the exception that back and leg muscle strength were greater in the control group relative to the exercise or exercise plus fortified milk groups. On average, daily dietary protein and calcium intakes for all participants were above or equivalent to the current Australian recommended dietary intake (RDI) for men aged 51–70 yr (Table 2; RDI for protein: 0.84 g/kg and RDI for calcium: 1,000 mg/day) (36a). Mean baseline serum 25-hydroxyvitamin D levels were no different between the groups and averaged 86.2 ⫾ 35.9 nmol/l; no participants had severe vitamin D deficiency (25-hydroxyvitamin D ⬍12.5 nmol/l), one participant had moderate deficiency (25-hydroxyvitamin D ⫽ 12.5–25 nmol/l), and 17 participants (9.4%) had mild deficiency (25-hydroxyvitamin D ⫽ 25–50 nmol/l) (29).

Table 1. Baseline characteristics of the participants according to group

n Age, yr Height, cm Body mass index, kg/m2 Body fat, % Physical activity (moderate), h/wk Muscle strength Chest (bench press), kg Back (lateral pull down), kg Legs (leg press), kg

Exercise ⫹ Milk Group

Exercise Group

45 61.7⫾7.6 174.3⫾6.3 27.4⫾3.7 28.0⫾7.8 3.7⫾3.9

46 60.7⫾7.1 174.2⫾6.6 28.1⫾3.3 28.3⫾5.5 3.6⫾3.4

49.1⫾12.7 61.4⫾14.5 63.4⫾18.0

55.0⫾13.1 65.8⫾11.7 64.7⫾16.5

Milk Group

45 61.7⫾7.7 174.4⫾5.8 27.7⫾3.3 29.4⫾7.0 3.3⫾3.8 49.1⫾13.5 66.3⫾11.2 71.4⫾13.7

Control Group

44 59.9⫾7.4 175.0⫾6.6 26.7⫾2.9 26.5⫾6.8 3.4⫾4.1 52.7⫾11.8 68.7⫾12.1* 74.4⫾18.1†

Values are means ⫾ SD; n, no. of subjects/group. *P ⬍ 0.05 vs. the exercise group; †P ⬍ 0.05 vs. the exercise ⫹ milk group and the exercise group. J Appl Physiol • VOL

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coefficients of variation (CVs) for total body lean mass and fat mass in our laboratory were 0.7% and 1.0%, respectively. Midfemur muscle cross-sectional area (CSA) was measured using quantitative computed tomography (QCT; Philips Mx8000 Quad CT scanner, Philips Medical Systems). The scan parameters were 120 kVp, 85 mAs, and 2.5-mm slice thickness. The midpoint of the left femur was determined by drawing a line from the femoral head to the lateral femoral condyle using the QCT ruler function. A series of four 2.5-mm slices were taken at the midpoint, with the middle two slices from the left leg analyzed and averaged. All cross-sectional QCT images were analyzed using the Geanie software program (BonAlyse Oy, Jyvakyla, Finland). Muscle CSA was obtained by measuring the area defined within an attenuation range from 0 to 200 HU excluding the bone and marrow. The short-term CV for two consecutive measurements in our laboratory was 0.40%. Muscle strength. Before the determination of upper and lower body 1-RM muscle strength, participants attended two separate familiarization sessions where they were shown correct exercise techniques by a trained instructor and given the opportunity to become accustomed to the selected exercises. To determine 1-RM, each participant initially performed a warm-up set of eight repetitions with a light load. After the successful completion of a further five to six repetitions at a heavier weight selected by the instructor and after a brief rest (⬃2 min), the workload was increased incrementally until only one repetition with correct technique could be completed. The leg press, latissimus dorsi pull down, and bench press exercises were used to document changes in upper and lower body muscle strength. Physical function. Dynamic single limb stance was assessed using the step test. Participants were instructed to step on and off a 7.5-cm-high block as many times as possible in 15 s. One complete step consisted of stepping onto and off the block. Participants were instructed to place their entire foot onto the block and then return it fully to the floor. Gait speed was calculated as the time taken to walk along a 6-m line, heel to toe, while avoiding any excessive side-toside movements. Time (in s) was recorded manually using a stopwatch. Postural sway was measured using a sway meter, which measures the displacement of the body at the level of the waist (32). Participants were tested for 30 s while standing on the floor or a medium-density foam mat with both eyes open and eyes closed. Postural sway was calculated as the product of either maximal anterior-posterior or lateral sway (in mm2) for each of the four tests. Diet, physical activity, and medication use. Nutrient intakes were assessed using a 3-day food diary (2 weekdays and 1 weekend day), with the option of weighing items, and analyzed using the Foodworks nutrient analysis software program (Xyris Software, Brisbane, Queensland, Australia). While all participants were provided with detailed verbal and written instructions for completing their food diaries, underreporting of habitual food intake is well known. Therefore, we used the Goldberg cutoff method to identify underreporters (22). Using this method, food diaries were excluded from nutrient intake analysis if reported energy intakes were ⬍1.5 times the pre-

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Table 2. Mean estimated dietary intakes by group at baseline and mean changes after 12 and 18 mo Exercise Group

Milk Group

Control Group

9,694⫾2,149 461 (⫺390, 1,313) ⫺249 (⫺1,168, 669)

9,884⫾1,948 250 (⫺525, 1,026) ⫺647 (⫺1,251, ⫺43)*

9,761⫾1,717 846 (84, 1,609)* ⫺337 (⫺1,122, 448)

10,199⫾2,201 ⫺318 (⫺1,079, 442) ⫺1,144 (⫺2,085, ⫺203)*

1.26⫾0.32 0.21 (0.08, 0.35)† 0.06 (⫺0.07, 0.19)

1.32⫾0.32 0.08 (⫺0.03, 0.19) ⫺0.10 (⫺0.20, 0.00)*

1.23⫾0.28 0.16 (0.07, 0.26)‡ 0.00 (⫺0.11, 0.10)

1.33⫾0.31 ⫺0.04 (⫺0.15, 0.08) ⫺0.06 (⫺0.21, 0.08)

257⫾66 6 (⫺21, 34) ⫺11 (⫺44, 21)

257⫾62 18 (⫺8, 44) ⫺15 (⫺35, 5)

260⫾63 16 (⫺8, 41) ⫺11 (⫺39, 17)

266⫾60 ⫺3 (⫺26, 19) ⫺28 (⫺59, 4)

84⫾29 4 (⫺8, 15) ⫺3 (⫺13, 6)

83⫾23 ⫺3 (⫺15, 8) ⫺5 (⫺14, 5)

86⫾21 9 (⫺2, 19) ⫺6 (⫺14, 3)

87⫾26 ⫺3 (⫺13, 7) ⫺13 (⫺24, ⫺2)*

911⫾360 827 (677, 977)‡ 607 (444, 770)‡

1,064⫾449 21 (⫺83, 127) ⫺133 (⫺223, ⫺42)†

1,039⫾455 682 (537, 828)‡ 551 (391, 711)‡

996⫾293 46 (⫺90, 181) ⫺81 (⫺202, 39)

1.2⫾2.1 19.1 (16.7, 21.4)‡ 17.5 (15.2, 19.9)‡

0.8⫾1.1 1.1 (0.6, 2.2)* 0.4 (⫺0.7, 1.6)

1.4⫾3.0 18.3 (16.2, 20.3)‡ 19.7 (17.6, 21.9)‡

0.7⫾1.0 1.1 (0.0, 2.2)* 0.6 (⫺0.2, 1.3)

Baseline values are means ⫾ SD, and change at 12 and 18 mo values are means with 95% confidence intervals in parentheses. The number of food diaries included in the analysis based on the Goldberg method (22) was as follows: for the change at 12 mo, exercise ⫹ milk group, n ⫽ 38; exercise group, n ⫽ 37; milk group, n ⫽ 39; and control group, n ⫽ 35; and for the change at 18 mo, exercise ⫹ milk group, n ⫽ 34; exercise group, n ⫽ 32; milk group, n ⫽ 39; and control group, n ⫽ 35. *P ⬍ 0.05, †P ⬍ 0.01, and ‡P ⬍ 0.001 for within-group changes from baseline.

Study attrition and compliance. Eight of the 180 men (4.4%) withdrew from the study over the 18-mo period (exercise plus fortified milk group: n ⫽ 2, exercise group: n ⫽ 2, fortified milk group: n ⫽ 2, and control group: n ⫽ 2). The reasons for withdrawal included the following: illness unrelated to the study (n ⫽ 2), work or personal time commitments (n ⫽ 5), and dissatisfaction with the group allocation after randomization (n ⫽

1). The average compliance with the exercise program was 63% (95% confidence interval: 57, 69) and did not differ between the exercise plus fortified milk group and the exercise alone group (65% vs. 61%). The average compliance in the fortified milk group was 90% (95% confidence interval: 87, 93) and was no different between the exercise plus fortified milk group and the fortified milk group (92% vs. 89%).

Table 3. Body composition characteristics by group at each time point and within-group changes relative to baseline Within Group

Weight, kg Exercise ⫹ milk group Exercise group Milk group Control group Fat mass, kg Exercise ⫹ milk group Exercise group Milk group Control group Lean mass, kg Exercise ⫹ milk group Exercise group Milk group Control group Midfemur CSA, cm2 Ex ⫹ Milk Ex Milk Controls

Baseline

12 mo

18 mo

Change at 12 mo

Change at 18 mo

83.2⫾11.9 85.2⫾10.9 84.1⫾9.8 81.9⫾10.7

83.9⫾12.1 85.3⫾11.1 84.7⫾9.4 81.9⫾11.0

83.8⫾12.2 85.2⫾11.5 85.1⫾9.9 81.6⫾10.5

0.6 (⫺0.1, 1.4) 0.0 (⫺0.8, 0.8) 1.3 (0.7, 2.0)‡ 0.0 (⫺0.6, 0.6)

0.7 (⫺0.2, 1.6) 0.0 (⫺0.9, 0.9) 1.7 (0.9, 2.5)‡ 0.1 (⫺0.7, 0.8)

22.9⫾8.7 23.5⫾6.6 24.2⫾7.4 21.2⫾7.5

22.5⫾8.7 22.8⫾6.8 24.4⫾7.5 21.1⫾7.7

22.3⫾8.5 23.0⫾6.8 25.2⫾7.6 21.1⫾7.4

⫺0.4 (⫺1.0, 0.3) ⫺0.8 (⫺1.6, 0.0)* 0.7 (0.2, 1.2)* ⫺0.1 (⫺0.6, 0.4)

⫺0.3 (⫺1.0, 0.3) ⫺0.4 (⫺1.2, 0.4) 1.3 (0.7, 2.0)‡ 0.1 (⫺0.5, 0.7)

57.0⫾6.4 58.5⫾6.5 56.6⫾5.3 57.5⫾5.8

58.2⫾6.1 59.1⫾6.4 56.8⫾5.4 57.5⫾5.6

58.2⫾6.1 58.8⫾6.6 56.5⫾5.0 57.1⫾5.9

1.0 (0.4, 1.5)‡ 0.7 (0.2, 1.1)† 0.4 (⫺0.1, 0.8) 0.1 (⫺0.4, 0.5)

0.9 (0.3, 1.6)† 0.3 (⫺0.2, 0.9) 0.2 (⫺0.4, 0.8) ⫺0.2 (⫺0.5, 0.1)

145.9⫾17.6 151.9⫾18.3 143.9⫾17.4 148.5⫾20.0

147.8⫾18.2 153.1⫾20.2 143.5⫾18.9 144.8⫾19.5

1.4 (0.1, 2.7)* 0.7 (⫺0.5, 1.8) ⫺0.1 (⫺1.0, 0.8) ⫺1.5 (⫺2.5, ⫺0.5)‡

Values for baseline, 12 mo, and 18 mo are means ⫾ SD, and values for within-group changes represent means with 95% confidence intervals in parentheses. Values for weight, fat mass, and lean mass are absolute changes (in kg), and values for midfemur cross-sectional area (CSA) are percent changes. *P ⬍ 0.05, †P ⬍ 0.01, and ‡P ⬍ 0.001 for within-group changes from baseline. J Appl Physiol • VOL

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Energy, kJ/day Baseline Change at 12 mo Change at 18 mo Protein, g 䡠 kg⫺1 䡠 day⫺1 Baseline Change at 12 mo Change at 18 mo Carbohydrate, g/day Baseline Change at 12 mo Change at 18 mo Fat, g/day Baseline Change at 12 mo Change at 18 mo Calcium, mg/day Baseline Change at 12 mo Change at 18 mo Vitamin D, ␮g/day Baseline Change at 12 mo Change at 18 mo

Exercise ⫹ Milk Group

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Adverse events. There were no serious injuries or adverse events associated with the exercise program. The limited number of minor injuries included the exacerbation of longstanding gout of the foot (n ⫽ 1), aggravated knee or hip pain (n ⫽ 2; both subjects were able to continue with exercise after program modification), lower back injury (n ⫽ 2; one subject recovered with 2-wk rest and one subject withdrew from the exercise program due to aggravated pain associated with a long-standing prolapsed disc but remained in the study), and the aggravation of a long-standing shoulder injury (n ⫽ 2; both participants returned to exercise after treatment). Three men were diagnosed with an inguinal hernia, but all were able to continue with the exercise program after treatment. Nutrient intake and physical activity. As expected, consumption of the fortified milk led to significant (⬃16%) increases in dietary protein intake (in g䡠 kg⫺1 䡠day⫺1) after 12 mo but not 18 mo relative to baseline (Table 2). Dietary intakes of calcium and vitamin D, but not total fat or carbohydrate intake, increased significantly in the fortified milk groups and were greater than in the nonsupplemented groups after both 12 and 18 mo (all P ⬍ 0.001). For the exercise group, there were no significant differences for any of the dietary parameters compared with the nonexercise group. Leisure time and recreational activity habits did not differ between the groups throughout the intervention. Serum 25-hydroxyvitamin D levels. There was a significant main effect of fortified milk on serum 25-hydroxyvitamin D levels after 12 mo (P ⬍ 0.001). This was due to a mean 11.3% increase (P ⬍ 0.01) in the fortified milk group compared with an 11.6% reduction (P ⬍ 0.01) in the nonsupplemented group, resulting in a net difference of 22.9% (29). After 18 mo, the mean increase in the fortified milk group remained significant relative to baseline (10.8%, P ⬍ 0.01), but the change in the nonsupplemented group was no longer significant (3.2%). There was no main effect of exercise on serum 25-hydroxyvitamin D levels. Body composition, muscle size, strength, and function. After 18 mo, the gains in total body lean mass and midfemur muscle CSA were two- to threefold greater in the exercise plus fortified milk group compared with either group alone or the control group, but the interaction terms were not statistically significant for any muscle or functional parameter (Fig. 1 and Table 3). Subsequent analysis of the main effects of exercise revealed that there was a net gain of 0.6 kg (P ⬍ 0.05) in total body lean mass relative to the nonexercise groups after 12 mo, and this difference remained after 18 mo (P ⬍ 0.05; Table 4*/). There was also a net 1.8% exercise-induced gain in midfemur muscle CSA (P ⬍ 0.001; Table 4). There were no significant effects of exercise on body weight, but there was a net exercise-related reduction of 0.8 and 1.1 kg in fat mass relative to nonexercise after 12 and 18 mo, respectively (P ⬍ 0.01 and ⬍0.001; Fig. 1 and Table 4). Upper and lower body muscle strength improved by 22–56% (all P ⬍ 0.001) after 12 mo of training and tended to plateau thereafter with the exception of leg muscle strength, which decreased in the exercise groups from 12 to 18 mo (both P ⬍ 0.05; Fig. 2). Gait speed improved by 11% (P ⬍ 0.05) after 18 mo in the exercise group relative to the nonexercise group (Tables 4 and 5). There were no other beneficial effects of exercise on any functional parameter, although various measures of sway improved in all four groups after 12 and/or 18 mo.

Fig. 1. Mean absolute changes (⫾SE) from baseline for total body fat mass and lean mass and percent changes for midfemur muscle cross-sectional area (CSA) according to group. There were no exercise by fortified milk interactions, but exercise resulted in significant improvements in total body lean mass, fat mass, and muscle CSA relative to the nonexercise group (main effects: P ⬍ 0.05 to P ⬍ 0.001).

In the fortified milk group compared with the nonsupplemented groups, body weight and fat mass increased by 1.0 kg (P ⬍ 0.01) and 0.6 kg (P ⫽ 0.07) after 12 mo, respectively, and these differences persisted after 18 mo (Fig. 1 and Tables 3 and 4). This was largely due to a significant increase in the fortified

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Table 4. Main effects for exercise and fortified milk for the changes in body weight, total body fat mass, total lean mass, midfemur muscle CSA, and gait speed Main Effects Exercise

Weight Change at 12 Change at 18 Fat mass Change at 12 Change at 18 Lean mass Change at 12 Change at 18 Midfemur CSA Change at 18 Gait speed Change at 12 Change at 18

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due to the fact that our participants were healthy communitydwelling men with adequate energy and protein intakes and sufficient circulating 25-hydroxyvitamin D levels and/or that the timing of milk consumption was not controlled. In partial support of the latter explanation, the findings from a recent

Milk

mo mo

⫺0.3 (⫺1.1, 0.3) ⫺0.6 (⫺1.4, 0.3)

1.0 (0.3, 1.6)† 1.2 (0.4, 2.0)‡

mo mo

⫺0.8 (⫺1.5, ⫺0.2)† ⫺1.1 (⫺1.8, ⫺0.4)‡

0.6 (0.0, 1.3) 0.7 (0.0, 1.4)*

mo mo

0.6 (0.1, 1.1)* 0.6 (0.1, 1.2)*

0.3 (⫺0.2, 0.8) 0.5 (0.0, 1.0)*

mo

1.8 (0.7, 2.9)‡

1.0 (⫺0.1, 2.1)

mo mo

⫺7 (⫺16, 2) ⫺11 (⫺21, ⫺2)*

2 (⫺7, 11) 6 (⫺4, 15)


Values are mean net differences with 95% confidence intervals in parentheses. Values for weight, fat mass, and lean mass are net absolute differences between the groups (in kg), values for midfemur CSA are net percentage differences between the groups, and values for gait speed are net percentage differences between the groups based on log-transformed data. *P ⬍ 0.05, †P ⬍ 0.01, and ‡P ⬍ 0.001 for between-group differences.

milk alone group; neither weight nor fat mass increased significantly in the exercise plus fortified milk group at any time. There was also a net benefit in the fortified milk group for total body lean mass (0.5 kg, P ⬍ 0.05) and a trend for a greater increase in midfemur muscle CSA (1.0%, P ⫽ 0.07) after 18 mo. However, these benefits were largely attributed to significant gains in the exercise plus fortified milk group and/or marked losses in the control group. There were no significant within-group changes for lean mass or muscle CSA in the fortified milk alone group. Finally, there were no main effects of fortified milk on muscle strength or any functional measure. DISCUSSION

The findings from this 18-mo factorial design randomized controlled trial indicate that the provision of a daily milk-based nutritional supplement providing additional energy, protein, vitamin D3, and calcium did not significantly enhance the effect of exercise on any muscle or functional performance measure in healthy community-dwelling middle-aged and older men. Consistent with these findings, Rankin et al. (41) reported that milk consumption after each bout of resistance training over 10 wk was associated with a twofold, but nonsignificant, greater gain in total body lean mass in young healthy men compared with those participants given an isocaloric carbohydrate solution. In this study, the lack of a significant additive effect of exercise and milk on lean mass was likely due to the small sample size (n ⫽ 19) and/or relatively high habitual dietary protein intakes (⬃1.2 g䡠kg⫺1 䡠 day⫺1). In our 2 ⫻ 2 factorial design study, the gains in total body lean mass and lower-extremity muscle CSA were two- to threefold greater in the exercise plus fortified milk group compared with either of these groups alone or the control group, but the “synergistic” interaction terms were not significant despite our larger sample size (n ⫽ 180). This lack of a statistically significant exercise by fortified milk interaction is most likely J Appl Physiol • VOL

Fig. 2. Mean percentage changes (⫾SE) from baseline for upper body (bench press), back (lat pull down), and lower body (leg press) muscle strength according to group. Exercise resulted in significant increases in all muscle strength measures relative to both baseline and to the nonexercise group (main effects: all P ⬍ 0.001).

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Table 5. Measures of physical function at each time point and within-group changes relative to baseline Within Group

Step test, no. of steps Exercise ⫹ milk group Exercise group Milk group Control group Gait speed, m/s Exercise ⫹ milk group Exercise group Milk group Control group

Baseline

12 mo

10.2⫾2.1 10.3⫾2.7 9.9⫾2.9 10.3⫾2.8

11.2⫾3.1 11.7⫾3.0 10.2⫾3.0 11.2⫾3.2

2.58⫾0.94 2.92⫾1.04 2.84⫾0.96 3.08⫾1.36

18 mo

Change at 12 mo

Change at 18 mo

12.2⫾2.6 12.6⫾3.0 11.4⫾3.0 12.0⫾3.3

6 (⫺1, 13)* 12 (5, 19)‡ 3 (⫺4, 10) 10 (4, 17)‡

17 (11, 24)‡ 19 (11, 27)‡ 13 (6, 20)‡ 15 (9, 22)‡

2.32⫾0.79 2.52⫾0.76 2.74⫾1.06 2.86⫾1.07

2.15⫾0.73 2.44⫾0.80 2.79⫾1.17 2.66⫾1.12

⫺9 (⫺18, 0)* ⫺14 (⫺24, ⫺4)† ⫺6 (⫺13, 2) ⫺4 (⫺14, 6)

⫺18 (⫺28, ⫺8)‡ ⫺20 (⫺31, ⫺9)‡ ⫺3 (⫺12, 5) ⫺12 (⫺21, ⫺3)†

241⫾185 343⫾303 294⫾282 320⫾366

300⫾354 288⫾319 252⫾211 227⫾154

180⫾153 205⫾159 326⫾420 179⫾147

12 (⫺23, 47) ⫺39 (⫺76, ⫺1)* ⫺19 (⫺52, 14) ⫺18 (⫺54, 17)

⫺48 (⫺87, ⫺9)* ⫺42 (⫺77, ⫺7)* ⫺17 (⫺58, 23) ⫺30 (⫺59, ⫺2)*

235⫾158 279⫾210 364⫾318 285⫾232

294⫾286 291⫾272 372⫾384 362⫾344

279⫾277 287⫾333 241⫾192 320⫾373

6 (⫺31, 43) ⫺9 (⫺43, 25) ⫺3 (⫺40, 33) 6 (⫺19, 31)

⫺3 (⫺29, 23) ⫺19 (⫺53, 14) ⫺45 (⫺78, ⫺11)† ⫺21 (⫺57, 15)

492⫾241 565⫾455 737⫾762 597⫾532

412⫾302 331⫾270 572⫾783 347⫾249

391⫾267 367⫾275 596⫾733 348⫾266

⫺29 (⫺53, ⫺5)* ⫺59 (⫺87, ⫺32)‡ ⫺39 (⫺70, ⫺9)* ⫺56 (⫺85, ⫺27)‡

⫺38 (⫺67, ⫺9)† ⫺48 (⫺78, ⫺17)‡ ⫺38 (⫺71, ⫺4)* ⫺51 (⫺75, ⫺28)‡

1,201⫾981 1,332⫾930 1,317⫾875 1,437⫾1217

1,041⫾1,044 875⫾675 925⫾781 1,086⫾831

933⫾1,085 864⫾662 1,045⫾787 1,254⫾1489

⫺31 (⫺61, ⫺1)* ⫺44 (⫺70, ⫺19)‡ ⫺46 (⫺72, ⫺20)‡ ⫺38 (⫺70, ⫺6)*

⫺46 (⫺74, ⫺19)† ⫺48 (⫺74, ⫺21)‡ ⫺32 (⫺60, ⫺4)* ⫺29 (⫺55, ⫺3)*

Sway, mm2

Values for baseline, 12 mo, and 18 mo are means ⫾ SD, and values for within-group changes are means with 95% confidence intervals in parentheses. All within-group percent changes are based on the log-transformed data, which represent the absolute differences from baseline multiplied by 100. *P ⬍ 0.05, †P ⬍ 0.01, and ‡P ⬍ 0.001 for within-group changes from baseline.

12-wk intervention in 56 healthy young novice male weightlifters with baseline protein intakes of ⬃1.2–1.4 g䡠kg⫺1 䡠day⫺1 revealed that milk consumption immediately and 1 h after exercise led to a significant ⬃1.5-fold greater gain in lean mass compared with isoenergetic soy or carbohydrate consumption (23). Habitual dietary protein intakes of the men in our study were above current RDIs. The mean baseline dietary protein intake across all groups was 1.30 g 䡠kg⫺1 䡠day⫺1, which exceeds the current Australian RDI value of 0.84 –1.07 g 䡠kg⫺1 䡠 day⫺1 for men aged ⬎50 yr (36a). Although there are some reports that dietary protein requirements should increase in older adults engaged in resistance training (33), a recent review concluded that the additional intake of dietary protein in older people who consume adequate dietary protein (in excess of 0.8 g䡠kg⫺1 䡠day⫺1) does not enhance the effects of resistance training on muscle mass and strength in older people (11). However, as already indicated, an important factor that could explain the lack of an interactive effect in our study relates to the timing in which the fortified milk was consumed. In a 12-wk study of elderly men, Esmarck et al. (18) reported that protein delivery immediately after each bout of resistance training, as opposed to 2 h later, augmented the exerciseinduced gains in muscle hypertrophy. In our study, the timing of milk consumption in relation to the exercise program was J Appl Physiol • VOL

not controlled, and thus it is possible that the men may have missed the important “window of anabolic opportunity” to enhance muscle protein synthesis (8). Indeed, the findings from a 10-wk resistance training trial in recreational male body builders revealed that the ingestion of a supplement containing protein, creatine, and glucose before and after each workout resulted in significantly greater skeletal muscle gains compared with a matched group who consumed the supplement outside of the pre- and postworkout time frames (14). However, several other acute resistance training studies have indicated that the window of opportunity for feeding may be extended for up to 24 h after resistance training, although it has been suggested that earlier feeding provides some additional advantages since this is when muscle protein synthesis is stimulated to the greatest extent (8). Interestingly, however, the findings from several intervention studies in older men have reported that ingesting additional protein either before and/or after a bout of resistance training does not provide additional skeletal muscle benefits (12, 13, 42). It has been suggested that the potential benefits of timed (protein) supplementation might be limited to specific elderly subpopulations, such as the frail elderly or malnourished (28). Vitamin D deficiency has also been associated with reduced muscle strength, slower walking speed, and impaired balance in the elderly (4, 44, 45), which have been reported to improve

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Eyes open, on floor Exercise ⫹ milk group Exercise group Milk group Control group Eyes closed, on floor Exercise ⫹ milk group Exercise group Milk group Control group Eyes open, on foam Exercise ⫹ milk group Exercise group Milk group Control group Eyes closed, on foam Exercise ⫹ milk group Exercise group Milk group Control group



improvements in gait speed were related to the inclusion and progressive difficulty of the weight-bearing activities throughout the intervention. A recent systematic review on the effects of PRT alone on balance in older adults reported that only 22% of all balance tests reported showed significant improvement in balance performance after training (37). In contrast, there is a growing body of evidence to support the findings that highvelocity resistance training can effectively improve muscle function in older adults, including gait and stair climbing speed (3, 25, 26). An unexpected finding in our study was the significant net gain in total body lean mass and, to a lesser extent, midfemur muscle CSA in the fortified milk group compared with the nonsupplemented groups. Despite reports that the ingestion of milk can stimulate muscle protein synthesis (17), the gains observed in our study appear to be largely attributed to the significant within-group increases in the exercise plus fortified milk group combined with the lack of change or losses in the control group. Inspection of the changes in the fortified milk alone group revealed that there were no changes in either lean mass or muscle CSA throughout the intervention. However, the ingestion of the fortified milk, particularly without exercise, resulted in a significant gain in total body fat mass. Although these changes were similar in magnitude to those reported in previous milk supplementation trials in older men (15) and women (13, 31), it is important to note that the consumption of fortified milk was not associated with an increase in total fat intake. While the strength of our study lies in its randomized controlled design, relatively long-term followup, high study retention, and compliance to the intervention, there are a number of limitations. First, our sample size was relatively small to detect a significant exercise by fortified milk interaction on the muscle outcomes. Post hoc sample size calculations based on the changes in total body lean mass in our study indicated that we would require ⬃265 participants/group to detect a significant synergistic interaction between exercise and fortified milk. Second, the timing of milk consumption was not controlled in our study, and we recruited relatively healthy, ambulatory community-dwelling men with adequate energy and protein intakes and serum 25-hydroxyvitamin D levels, all of which may have limited our ability to detect any significant interactions if they were present. Finally, we did not include a placebo or energy-matched control drink. Therefore, if any significant interaction or main effects of fortified milk were detected, we would not be able to determine whether it was due to the additional protein, calcium, and/or vitamin D present in the milk. In addition, it is possible that the nonsupplemented groups may have increased their daily dairy intake, although the findings from our dietary analysis indicate that there were no marked changes in habitual energy, calcium, or protein intake in these groups. In conclusion, daily consumption of 400 ml of low-fat fortified milk providing additional energy, protein, vitamin D3, and calcium does not significantly enhance the effects of progressive resistance exercise on muscle mass, size, strength, or function in healthy community-dwelling middle-aged and older men with adequate energy and nutrient intakes. However, we were able to show that a community-based resistance training program involving a single high-intensity training set performed 3 days/wk over 18 mo was effective for improving

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with vitamin D and/or calcium supplementation in some (7, 16, 38, 39) but not all (27) studies. In our study, serum 25hydroxyvitamin D levels significantly increased by ⬃10 nmol/l after supplementation with fortified milk, but it is unlikely that this would have enhanced the effects of resistance exercise on muscle mass or function because baseline vitamin D levels were already sufficiently high (mean ⫾ SD: 86.2 ⫾ 35.9 nmol/l). There is emerging evidence and expert opinion that serum 25-hydroxyvitamin D levels above 75– 80 nmol/l are needed for optimal muscle function, after which further increases are unlikely to translate into any marked functional improvements (6). Despite the lack of a significant interactive effect, the present study showed that a community-based progressive moderate to high-intensity resistance training program in combination with a diverse range of weight-bearing exercises performed 3 days/wk was safe, feasible, and effective for improving muscle strength, total body lean mass, lower-extremity muscle size, and gait performance and reducing fat mass in healthy community-dwelling middle-aged and older men. The observed 20 –52% improvements in upper and lower body muscle strength after 18 mo were comparable to the gains reported in a number of previous resistance training trials in older men (12, 18, 34, 35, 43). However, the net 1.8% gain in midfemur muscle CSA was considerably less than the 4 –9% gains reported in several previous trials after 12 wk (20, 23, 34) to 2 yr (34) of resistance training. The most likely explanation for the attenuated gains in our study is that the total volume and intensity of training were lower than those reported in the previous studies. Our program consisted of a single warm-up set at 60 – 65% 1-RM followed by a single training set at 60 – 85% 1-RM, whereas participants in most previous studies typically performed 3 sets at 75– 80% 1-RM (20, 23, 33). In support of this notion, previous research has indicated that greater skeletal muscle gains can be achieved with multiset resistance training (21). Nevertheless, we believe that the findings from our study are important because they highlight that significant, albeit smaller, gains in muscle mass and size can still be achieved with a single set of moderate to highintensity resistance training performed 3 days/wk in healthy middle-aged and older men. An important strength of our study lies in its long-term followup with repeated measurements. This provided a unique opportunity to quantify the time course for skeletal muscle adaptations to resistance training in middle-aged and older men. For muscle strength, we found that the greatest increases occurred after 6 to 12 mo of training, after which no further improvements were detected. This coincides with the plateau observed in total body lean mass after 12 mo of training. It is difficult to explain the lack of a continual increase in muscle strength and lean mass because the average resistance training load per session increased by ⬃12% from 12 to 18 mo. Nevertheless, these findings are consistent with the principle of diminished returns, which suggests that after an initial training adaptation, any further gains are likely to be slow and of small magnitude. Importantly, however, we believe that the introduction of the high-velocity training phase during the final 6 mo contributed to the significant improvements in gait speed in the exercise group after 18 mo of training; no exercise-induced improvements were observed in any functional measures after the initial 12 mo of traditional PRT. It is also possible that the

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total body lean mass and fat mass, lower-extremity muscle CSA, and gait speed. Importantly, the low attrition and relatively good exercise compliance coupled with the low number of adverse events indicates that this type of program is safe, feasible, and well tolerated in previously untrained but otherwise healthy middle-aged and older men. ACKNOWLEDGMENTS The authors thank Tiana Mahncke for analyzing the QCT scans. The authors also thank Murray Goulburn Cooperative Company Limited for providing the calcium- and vitamin D3- fortified low-fat UHT milk used in the study and the City of Greater Geelong and Ocean View Health Club for the generous provision of the gymnasium facilities used throughout the study. The authors also thank the following people for contributions to this study: Shona Bass, Nicole Petrass, Joanne Daly, and Sam Korn. GRANTS

DISCLOSURES No conflicts of interest are declared by the author(s). REFERENCES 1. American College of Sports Medicine. ACSM. Guidelines for Exercise Testing and Prescription. Philadelphia, PA: Lippincott, Williams and Wilkins, 2000. 3. Bean JF, Herman S, Kiely DK, Frey IC, Leveille SG, Fielding RA, Frontera WR. Increased velocity exercise specific to task (InVEST) training: a pilot study exploring effects on leg power, balance, and mobility in community-dwelling older women. J Am Geriatr Soc 52: 799 – 804, 2004. 4. Bischoff-Ferrari HA, Borchers M, Gudat F, Durmuller U, Stahelin HB, Dick W. Vitamin D receptor expression in human muscle tissue decreases with age. J Bone Miner Res 19: 265–269, 2004. 5. Bischoff-Ferrari HA, Dietrich T, Orav EJ, Hu FB, Zhang Y, Karlson EW, Dawson-Hughes B. Higher 25-hydroxyvitamin D concentrations are associated with better lower-extremity function in both active and inactive persons aged ⬎ or ⫽60 y. Am J Clin Nutr 80: 752–758, 2004. 6. Bischoff-Ferrari HA, Giovannucci E, Willett WC, Dietrich T, DawsonHughes B. Estimation of optimal serum concentrations of 25-hydroxyvitamin D for multiple health outcomes. Am J Clin Nutr 84: 18 –28, 2006. 7. Bischoff HA, Stahelin HB, Dick W, Akos R, Knecht M, Salis C, Nebiker M, Theiler R, Pfeifer M, Begerow B, Lew RA, Conzelmann M. Effects of vitamin D and calcium supplementation on falls: a randomized controlled trial. J Bone Miner Res 18: 343–351, 2003. 8. Burd NA, Tang JE, Moore DR, Phillips SM. Exercise training and protein metabolism: Influences of contraction, protein intake, and sexbased differences. J Appl Physiol 106: 1692–1701, 2009. 9. Campbell WW, Crim MC, Young VR, Evans WJ. Increased energy requirements and changes in body composition with resistance training in older adults. Am J Clin Nutr 60: 167–175, 1994. 10. Campbell WW, Crim MC, Young VR, Joseph LJ, Evans WJ. Effects of resistance training and dietary protein intake on protein metabolism in older adults. Am J Physiol Endocrinol Metab 268: E1143–E1153, 1995. 11. Campbell WW, Leidy HJ. Dietary protein and resistance training effects on muscle and body composition in older persons. J Am Coll Nutr 26: 696S–703S, 2007. 12. Candow DG, Chilibeck PD, Facci M, Abeysekara S, Zello GA. Protein supplementation before and after resistance training in older men. Eur J Appl Physiol 97: 548 –556, 2006. 13. Chee WS, Suriah AR, Chan SP, Zaitun Y, Chan YM. The effect of milk supplementation on bone mineral density in postmenopausal Chinese women in Malaysia. Osteoporos Int 14: 828 – 834, 2003. 14. Cribb PJ, Hayes A. Effects of supplement timing and resistance exercise on skeletal muscle hypertrophy. Med Sci Sports Exer 38: 1918 –1925, 2006. J Appl Physiol • VOL

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This work was financially supported by a grant from the Australian Research Council Linkage Scheme in collaboration with Murray Goulburn Cooperative Company Limited. R. Daly was supported by National Health and Medical Research Council Career Development Award ID 425849.

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