Pediatric Exercise Science, 2014, 26, 444-454 http://dx.doi.org/10.1123/pes.2014-0073 © 2014 Human Kinetics, Inc.

Hormonal and Metabolic Responses to a Resistance Exercise Protocol in Lean Children, Obese Children, and Lean Adults Daniela A. Rubin, Diobel M. Castner, and Hoang Pham California State University

Jason Ng University of Alabama

Eric Adams and Daniel A. Judelson California State University During childhood, varying exercise modalities are recommended to stimulate normal growth, development, and health. This project investigated hormonal and metabolic responses triggered by a resistance exercise protocol in lean children (age: 9.3 ± 1.4 y, body fat: 18.3 ± 4.9%), obese children (age: 9.6 ± 1.3 y, body fat: 40.3 ± 5.2%) and lean adults (age: 23.3 ± 2.4 y, body fat: 12.7 ± 2.9%). The protocol consisted of stepping onto a raised platform (height = 20% of stature) while wearing a weighted vest (resistance = 50% of lean body mass). Participants completed 6 sets of 10 repetitions per leg with a 1-min rest period between sets. Blood samples were obtained at rest preexercise, immediately postexercise and 2 times throughout the 1-hr recovery to analyze possible changes in hormones and metabolites. Children-adult differences included a larger exercise-induced norepinephrine increase in adults vs. children and a decrease in glucagon in children but not adults. Similarities between adults and children were observed for GH-IGF-1 axis responses. Metabolically, children presented with lower glycolytic and increased fat metabolism after exercise than adults did. Obesity in childhood negatively influenced GH, insulin, and glucose concentrations. While adults occasionally differed from children, amount of activated lean mass, not maturation, likely drove these dissimilarities. Keywords: obesity, youth, endocrine, metabolism, exercise During childhood, exercise is a key stimulus to trigger positive adaptive responses for growth and health (35). Hormones released during or after exercise mediate some of these adaptations (38). Previous studies have presented differences in the magnitude of some acute hormonal responses to aerobic exercise between children and adults such as in catecholamines (18,33). Moreover, it has been demonstrated that children exhibit a higher reliance on oxidative metabolism compared with adults, as well as on fat versus carbohydrate during aerobic exercise (20,37). In recent years, physical activity guidelines in children and adults have included resistance exercise (RE) Rubin, Castner, Pham, Adams, and Judelson are with the Dept. of Kinesiology, California State University, Fullerton, CA. Ng is with the Dept. of Kinesiology, University of Alabama, Tuscaloosa, AL. Address author correspondence to Daniela A. Rubin at [email protected].

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in addition to aerobic exercise (19). Resistance exercise provides many benefits to children and adolescents such as improved body composition, muscle strength and power, cardiovascular fitness, motor performance, cardiometabolic profile and mental health (5,19). Acute hormonal responses to RE contribute to increases in muscle size, strength and power observed with resistance training (17). In contrast to aerobic exercise, the hormonal response to strength exercise in children is less studied (34). The only studies done in the topic have used traditional weight training exercises such as knee extensions or squats and were performed in adolescent males ages 14 and older (29,30). Thus, the literature is limited on responses to RE in younger children, particularly before or during early puberty. Obesity and overweight affects 1 in every 3 to 5 children and adolescents in the United States (25). Obese children likely become obese adults with increased risk for cardiovascular and metabolic complications. Unfortunately, obesity disrupts endocrine system function

Responses to Resistance Exercise in Children   445

during rest and aerobic exercise (9,38). Data in adults suggest obesity alters hormonal and metabolic responses to RE (4,26,36). However, data on obesity’s role on RE hormonal responses in children are not available. Therefore, this study was undertaken to describe acute hormonal and metabolic changes in response to a low-tomoderate intensity resistance protocol among prepubertal children with normal and high levels of body fat, as well as in adults. It was hypothesized that children would exhibit some differences in the hormonal responses and a heightened fat metabolism compared with adults, and body fat would negatively affect catecholamines and growth hormone (GH) responses.

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Participants Participants included 12 lean children (body fat percentage < 85th percentile for age and sex, lean), 13 obese children (body fat percentage > 95th percentile for age and sex, obese) and 10 lean men (body fat < 25%, adult; 2). Percentiles for age and sex for children percentages of body fat were obtained from McCarthy et al. (21). The study had institutional review board approval as well as approval from the Human Research Protection Office of the U.S. Army. Before participating, children signed an approved informed assent form while their parents signed an informed consent form. In addition, parents of participating children completed a medical history form that screened for contraindications to participation. Children also completed a validated questionnaire to assess pubertal development (27). Exclusion criteria for participation in children included insulin resistance, type 2 diabetes mellitus, other metabolic diseases, confirmed pregnancy, and inability to participate in vigorous physical activity. Adult participants also signed an informed consent form and completed a medical history form to check for contraindications to exercise. Exclusion criteria for adults included suffering from, or taking medication for, cardiac disease, pulmonary disease, metabolic disease, high cholesterol, and hypertension and thyroid disorders. Furthermore, adults were also excluded if they were undergoing hormone replacement therapy, if they chronically consumed alcohol and/or were smokers.

Anthropometrics and Baseline Measurements Body mass was measured in shorts and T-shirt via calibrated electronic scale (ES200L, Ohaus, Pinewood, NJ). Standing height was measured with no shoes at the end of inhalation via a wall-mounted stadiometer (Seca, Ontario, CA). Body composition was measured via dual energy X-ray absorptiometry following standard procedures (GE Healthcare, GE Lunar Corp., Madison, WI). Heart rate (HR) was measured via telemetry (Polar USA, Lake Success, NY) and blood pressure (BP) via standard sphygmomanometry (Silver Series DS65, Welch

Allyn, Skaneateles Falls, NY). Resting HR and systolic (SBP) and diastolic (DBP) were obtained after 10 min of seated rest.

Exercise Trial Exercise trials were completed in the morning (between 9 am and 11 am). Participants consumed a standardized breakfast containing 260 kcal/1088kJ, composed of 7 g of fat (21.5%), 37 g of carbohydrate (57.0%) and 14 g of protein (21.5%) 2 hr before reporting to the laboratory. Upon arrival, participants sat and an indwelling catheter was placed in an antecubital vein. A resting blood sample was obtained 30 min after catheter insertion (PRE). Afterward, participants completed a 5-min warm-up on a stationary bike with the aim of raising HR above 120 beats∙min-1 (bpm) followed by a set of 3 lower body stretches repeated 2 times. Then, participants completed a resistance protocol consisting of 6 sets of 10 repetitions per leg of a step-up exercise onto a platform while wearing a weighted vest. Rest periods of 1-min were allocated between the sets. Target platform height (20% of stature) and vest loading (50% of total body lean mass) were computed to represent the same amount of relative work for all groups. HR was monitored throughout the step-up exercise. BP was only obtained after completion of the third and sixth sets. The OMNI scale was used to obtain exercise rating of perceived exertion (RPE) in children (31) and adults (32) after each set. A brief anchoring exercise was done with children to familiarize them with the scale.

Hormones and Metabolites Measurement In addition to PRE, blood samples were obtained immediately postexercise (IP), as well as 15 min (+15) and 60 min (+60) into seated recovery. No measurements were obtained between sets because of the relatively short duration of the protocol. Moreover, we anticipated that responses would be observed either at IP or +15, with a return to baseline by +60. Approximately 10 ml of blood were collected at each time point and placed into blank serum tubes, chilled tubes pretreated with EDTA, and chilled tubes pretreated with EDTA and sodium fluoride (BD Diagnostics, Franklin Lakes, NJ). Samples were centrifuged at 4 °C for 15 min at 3000 rev∙min-1. Resulting serum and plasma were aliquoted and frozen at –80 °C until analysis. Investigators thawed individual samples only once and evaluated all samples in duplicate for a given subject during the same analytical run. Concentrations of epinephrine, norepinephrine, insulin-like growth factor-1 (IGF-1), insulin-like growth factor binding protein 3 ([IGFBP-3] ALPCO Diagnostics, Salem, NH), growth hormone ([GH] R & D Systems, Minneapolis, MN), insulin (Millipore, St. Charles, MO), and glucagon (Cusabio Biotech, Newark, DE) were measured via enzyme-linked immunosorbent assays. Concentrations of glucose and lactate were determined using enzymatic

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techniques (YSI 2300 STAT Plus Glucose/Lactate Analyzer, YSI, Yellow Springs, OH). Concentrations of free fatty acids (FFA), ketones (Wako Chemicals USA, Richmond, VA) and glycerol (Sigma-Aldrich, St. Louis, MO) were determined using enzymatic, colorimetric assays. All assays were performed following manufacturers’ recommendations. Sensitivity, intra- and interassay coefficients of variation, when applicable, were: epinephrine = 54.5 pmol/L, 13.4 and 11.8%; norepinephrine = 295.7 pmol/L, 12.6 and 15.6%; IGF-1 = 0.09 μg/L, 2.6 and 5.9%; IGFBP-3 = 0.1ng/ml, 4.8 and 4.2%; GH = 0.07 μg/L, 5.9% and 11.2%; insulin = 13.89 pmol/L, 4.6 and 8.7%; glucagon = 5 ng/L, 4.7 and 2.4%; glucose = 0.2 mmol/L, 1.9% and n/a; lactate = 0.1 mmol/L, 2.0% and n/a; FFA = 0.0014 mmol/L, 5.5 and 7.0%; ketones: 4.13 μmol/L 7.7 and 15.2% and glycerol = 0.0033 mmol/L, 11.3 and 3.4%. Concentrations are reported as measured values, uncorrected for plasma volume shifts, to reflect the target tissues’ actual exposure to the hormones and metabolites. Hormones were selected because of their role in metabolism, as well as in growth.

Statistical Analyses One-way ANOVAs were conducted to compare participant characteristics and nonhormonal or metabolic

exercise responses among groups. Three (lean vs. obese vs. adults) by 4 (time) mixed model ANOVAs were calculated to determine differences among sample means for all hormones and metabolites. In the case of significant F-ratios, post hoc Tukey’s HSD tests were used to make priori-determined comparisons between time points within each group, as well as to compare specific time point values among groups (i.e., PRE and IP). Data are presented as means ± SEs of the mean, unless otherwise noted. Statistical significance was set at p < .05.

Results Participant characteristics and exercise responses are presented in Table 1. Obese were heavier (p < .01), had higher percentage of body fat (p < .01) and a greater resting SBP (p = .03) than lean. As expected, adults were older, taller, and had more body mass and less body fat than children; in addition, they carried a heavier vest load and stepped onto a higher platform than children (p < .01 for all). Despite differences in resting HR, children and adults presented similar HR during exercise (mean HR throughout the 6 sets; p = .94) and at the end of exercise (p = .86), as well as similar RPE during exercise (mean RPE from all 6 sets; p = .39) and at the end of exercise (p = .43). In all groups, SBP increased with exercise

Table 1  Participant Characteristics and Resistance Exercise Measurements Presented as Mean ± SD Lean (n = 12)

Obese (n = 13)

Adult (n = 10)

Male/female

6/6

8/5

10/0

Age (y)

9.3 ± 1.4

9.6 ± 1.3

23.3 ± 2.4*†

Stature (cm)

140.8 ± 10.3

142.8 ± 7.4

177.2 ± 4.8*†

Body mass (kg)

31.41 ± 6.69

48.82 ±

Pubertal stage (I/II/III/IV)

7/2/3/0

6/3/3/1

Body fat (%)

18.3 ± 4.9

40.3 ± 5.2*

12.7 ± 2.9*†

Lean mass (kg)

24.29 ± 4.90

27.56 ± 5.13

65.09 ± 7.26*†

Resting HR (bpm)

79 ± 11

74 ± 11

58 ± 12*†

Resting SBP (mm Hg)

86 ± 10

98 ±

10.16*

13*

77.05 ± 6.36*†

107 ± 10*

Resting DBP (mm Hg)

59 ± 8

60 ± 5

66 ± 12

Vest load (kg)

12.14 ± 2.45

13.80 ± 2.55

32.54 ± 3.63*†

Step height (cm)

28.2 ± 2.1

28.6 ± 1.5

35.4 ± 1.0*†

Protocol duration (min)

12.5 ± 1.6

12.2 ± 2.0

10.6 ± 0.3*†

Mean exercise HR (bpm)

151 ± 18

164 ± 15

154 ± 13

End exercise HR (bpm)

159 ± 19

174 ±18

163 ± 14

End exercise SBP (mm Hg)

117 ± 14

127 ± 18

156 ± 20*†

End exercise DBP (mm Hg)

67 ± 11

60 ± 11

79 ± 11*

Mean exercise RPE (1–10)

5±2

6±2

4±1

End exercise RPE (1–10)

7±3

8±3

5±1

*Different than lean. †Different than obese; p < .05.

Responses to Resistance Exercise in Children   447

(data not shown). At the end of exercise, adults had a higher SBP than all children (p < .01) and higher DBP than obese (p < .01).

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Hormonal Responses No differences existed in the epinephrine response among groups, as presented in Figure 1 (p = .83 for interaction and p = .52 for group differences). In contrast, norepinephrine responses did vary by group, as presented in Figure 1 (p < .01 for interaction). Lean exhibited no change over time (p > .93 for all), while obese and adults presented an increase with exercise (IP > PRE, +15 and +60; p < .01 for all). In addition, norepinephrine concentration at IP in adults exceeded obese and lean concentrations for the same time point (p < .01). There were no significant group by time interactions for GH and IGF-1 responses to RE (presented in Figure 2; p = .14 and p = .50, respectively, for interactions). A group effect (p < .01) showed that obese presented lower

GH concentrations than lean and adults (p < .02 and p < .03, respectively). In contrast, no group differences were present for IGF-1 (p = .98). Although IGFBP-3 demonstrated a group by time interaction (p = .03), no physiologically meaningful comparisons resulted. There was a significant group by time interaction for insulin (p < .01) as presented in Figure 3. In lean, insulin PRE exceeded +60 (p < .01) and in obese, insulin PRE exceeded IP and +60 (p < .01 for both). However, in adults, no differences existed among time points (p > .27). Moreover, obese insulin PRE was higher than insulin PRE in lean and adults (p IP, +15 and +60; p < .05 for all). Likewise, obese demonstrated a decrease in glucagon in response to exercise (PRE > IP and +60; p = .02 and p < .01, respectively). In contrast, adults exhibited an increase in glucagon at 15 min into recovery (+15 > IP

Figure 1 — Epinephrine and norepinephrine responses to step-up resistance exercise. Epinephrine: No significant group by time interaction. Significant time effect: PRE < IP. Norepinephrine: Significant group by time interaction. Within-group difference: open marker = different than PRE. Between-group difference: *Different than lean, †Different than obese. Significance set at p < .05 for all analyses.

448

Figure 2 — a) Growth hormone (GH) response to step-up resistance exercise and comparison of responders vs. nonresponders and b) insulin-like growth factor-1 (IGF-1) and IGF binding protein-3 (IGFBP-3) responses to step-up resistance exercise. GH: No significant group by time interaction. Significant group effect: obese < lean and adult. Significant time effect: PRE < +15. IGF-1: No significant group by time interaction. Significant time effect: PRE < IP. IGFBP-3: Significant group by time interaction. No significant pairwise comparisons. Significance set at p < .05.

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Responses to Resistance Exercise in Children   449

Figure 3 — Insulin and glucagon responses to step-up resistance exercise. Insulin and glucagon: Significant group by time interaction. Within-group difference: open marker = different than PRE. Between-group difference: *Different than lean, #Different than adult. Significance set at p < .05 for all analyses.

and +60; p < .01 for both) but no difference compared with PRE (p = .80).

Metabolic Responses Figure 4 presents metabolic responses to RE. There was no significant group by time interaction for glucose (p = .25), but there was a group (p = .01) effect. Glucose in obese and adults exceeded glucose in lean (p = .03 for both). Differences existed in the lactate response among groups (p < .01 for interaction). Lean exhibited higher IP lactate compared with PRE and +60 (p = .03 and p < .01, respectively), whereas obese and adults exhibited higher IP lactate compared with all other points (p < .01 for all). The magnitude of change for IP was also higher in adults compared with lean (IP adults > IP lean; p < .01).

In terms of FFA and glycerol, there were group differences in the response to exercise (p £ .02 for interaction for both). Lean, obese and adults exhibited higher FFA at +15 compared with baseline for their respective pairwise comparisons (p < .01 for all). In lean and adults, FFA were also higher at 60 min into recovery compared with baseline (p < .01 and p = .03, respectively). In comparison, FFA in obese returned to baseline at 60 min into recovery (p = .98). In addition, lean had higher FFA concentrations at +60 than adults (p < .05) while obese exhibited higher FFA concentrations than adults at +15 (p < .01). In terms of glycerol, lean exhibited higher concentration immediately postexercise compared with baseline (p < .01) and obese demonstrated higher concentration at IP compared with both baseline and 60 min into recovery (p < .01 for both). In contrast, adults demonstrated no change in glycerol in response to exercise (p > .20 for all).

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Figure 4 — a) Glucose and lactate and b) free fatty acid (FFA), glycerol and ketone responses to step-up resistance exercise. Glucose: No significant group by time interaction. Significant group effect: obese < lean and adult. Significant time effect: PRE < +15. Lactate, FFA and glycerol: Significant group by time interaction. Within-group difference: open marker = different than PRE. Between-group difference: *Different than lean. #Different than adult. Ketones: Borderline time by group interaction. Significance set at p < .05 for all analyses.

Moreover, obese exhibited higher glycerol concentrations at IP and +15 compared with adults (p < .05 and p < .01, respectively). For ketones, the group by time interaction was borderline significant (p = .05) and therefore interpreted. Lean exhibited an increase in ketones at +60 compared with PRE and IP (p < .01 for both), and obese exhibited an earlier increase in ketones at +15 and +60 compared with IP (p < .01 for both), whereas adults showed no change (p ³ .60 for all).

Discussion This study evaluated hormonal and metabolic differences between children and adults, as well as the role of obesity in children’s responses to a brief RE protocol. Child-adult differences were observed for norepinephrine and glucagon. Similarities between adults and children were observed for the GH-IGF-1 axis. Metabolically, children presented with lower lactate concentrations and

Responses to Resistance Exercise in Children   451

increased fat metabolism after exercise compared with adults. Obesity in childhood negatively influenced GH, insulin, and glucose concentrations.

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Child-Adult Differences and Similarities Earlier studies contrasting the hormonal responses to exercise between children and adults presented differences for norepinephrine in response to graded maximal aerobic exercise (18) and RE (29). We demonstrated a larger norepinephrine increase in adults vs. children, similar to a previous comparison between adolescent boys and men (29). Other authors have indicated no role of maturation in these differences (33) as norepinephrine release during exercise is not only related to sympathetic nervous system stimulation but also to the activated skeletal muscles (16). We agree with previous studies as we conclude that likely, the larger rise in norepinephrine concentration in response to RE in adults vs. children is simply related to the larger muscle mass involved. Conversely, the lack of differences in the epinephrine response to RE between adults and children suggests a similar relative intensity among the groups (18), which is supported by a similar HR and RPE at the end of exercise in all groups. Factors such as exercise intensity and duration, fitness levels, core temperature and the metabolic cost of the exercise are related to GH release in response to exercise (11,17). The present study demonstrated a GH increase in response to exercise in all groups despite the large proportion of nonresponders (66% in lean, 76% in obese and 60% in adults; see Figure 2). The only factor affecting the response was the level of adiposity, which induced lower overall concentrations in obese children (discussed below). Fahey and colleagues demonstrated no effect of puberty on the GH response to maximal exercise (10); however, 2 other studies demonstrated a positive effect of puberty on GH (28,40), perhaps related to changes in lactate during aerobic exercise (40). In terms of the GH response to RE, adolescent boys and men showed a similar increase, which supports our results (30). In the current study, the GH increase was fairly small likely because of the large proportion of nonresponders. This lack of GH response in some participants might have been related to an insufficient RE intensity (11) and/or the pituitary refractory period occurring after spontaneous GH excursions (8). However, attained concentrations were comparable to low doses of recombinant GH in children (38). Due to the relatively small sample size we could not establish differences between GH responders to nonresponders. In the current study, a similar relatively small increase in IGF-1 concentration was observed in all groups. Studies in adults have reported transient increases in IGF-1 in response to exercise (11,14,17), as well as no change (11,17). The increase in IGF-1 in response to exercise is temporally unrelated to the release of GH (24). It is possible that IGF-1 sequestered extracellularly to the muscle may be released as the skeletal muscles contract, and thus contributes to the increase in concen-

tration observed in response to exercise (11). Therefore, it is reasonable that both children and adults experience such change. Insulin and glucagon exert opposite roles in the maintenance of euglycemia at rest, while their responses to exercise may also be different (15). In response to aerobic exercise, insulin concentrations decrease in children and adults (7,9,22). In RE, insulin response is coupled to blood glucose concentrations (17) explaining the lack of change in insulin in lean children and adults in the current study (4). In obese children, the high glucose and insulin at baseline may explain the RE-induced insulin decrease. In adults glucagon increases in response to aerobic exercise if exercise duration and intensity thresholds are met (22); but in healthy children, glucagon has been shown to increase (7) or not change (1,12). In the current study, adults showed no change in glucagon suggesting that the threshold was not met. Low glucose concentration also stimulates glucagon release. However, in the current study, as in another RE study (36), participants demonstrated a transient increase in glucose immediately after exercise, further explaining the lack of increase in glucagon. The decrease in circulating glucagon may be related to its short life (~5 min) and perhaps an increased clearance rate during recovery with little change in production and release by the pancreas (15). Metabolically, a few differences between children and adults were observed. Adults had higher glucose concentrations than lean children, which can be explained by the effect of age on glucose metabolism (6). Similarly, lean adults exhibited a greater increase in lactate compared with lean children, which coincides with previous results for aerobic exercise (20,37). Previous investigations have demonstrated enhanced fat metabolism during aerobic exercise in children vs. adults (20,37) and our findings support the results of these studies (20,37). Possible morphologic and functional differences between children and adults include a higher aerobic enzyme activity (3), which may contribute to enhanced overall oxidative metabolism in children vs. adults.

Obesity’s Influence Obese children presented an increase in norepinephrine in response to RE while lean did not. A larger increase in norepinephrine in obese than lean adults has also been previously reported (26). Despite lean and obese children having similar lean mass, it is possible that obese children activated more accessory muscles in the core, back and arms (16), which could easily have resulted in greater norepinephrine concentrations in obese than lean. Because excess adiposity appears to cause hypoadrenergic activity (39), we speculated that extra fat would dampen the epinephrine exercise-induced increase (4,9,26). Close examination of our data showed that 58% of lean and 46% of obese children demonstrated no REinduced increase in epinephrine >15% (more than assay variability). Thus, this proportion of children demonstrating no change in epinephrine might have contributed

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to the large intersubject variability, likely diminishing our statistical power to demonstrate an effect of obesity (please see Figure 1). Obesity has been demonstrated to decrease the GH response to aerobic exercise in children (9,12), as well as to RE in adults (11,26). Thus, our findings extend findings of RE in adults to children. The mechanism by which body fat affects GH release is yet to be understood; though speculations include a disrupted neuroendocrine stimulus related to blunted catecholamines and sympathetic nervous system and increased insulin and IGF-1 (9,22,36,39). Because GH is vital for children to achieve normal body composition and stature (38), our findings highlight the importance of obesity prevention and treatment in childhood. As demonstrated in numerous studies in children, obesity is associated with higher insulin concentrations at rest (13). In the current study, obese children displayed a decrease in insulin in response to exercise, similar to other studies of children (7,9) and adults performing aerobic exercise (39). This decrease in insulin was present despite the increase in glucose immediately after the exercise. In adults, the increase in insulin in response to RE has been hypothesized to be related to the rise in glucose, FFA and perhaps amino acids (36); however, the coexisting decrease in insulin and increase in glucose after RE in the obese children do not support this hypothesis. It appears that in children, regulating mechanisms of insulin suppression during exercise persist despite the increase in blood glucose, demonstrating the important role of exercise for improving insulin sensitivity. Last, it is no surprise that obese children exhibited higher glucose at baseline (2 hr postprandial) than lean (23). The high glucose concentrations in obesity likely relate to insulin resistance as demonstrated by insulin concentrations (13). In adults, obesity affects fat mobilization during and after exercise (22), but in the current study all children demonstrated a higher fat metabolism (FFA, glycerol and ketones) compared with adults in response to RE, independent of obesity. Nonetheless, obese children did show an earlier increase in ketone bodies compared with lean, suggesting incomplete fat oxidation.

Study Limitations Despite the novelty of these data, this study had several limitations that must be acknowledged. Limitations included a small sample size and the comparison of a mixed sample of girls and boys to adult males instead of a male-to-male comparison. However, most children were in early pubertal stages and no sex hormones were evaluated. In addition, there was no control for training status of the children; but HR and RPE responses suggested similar relative workload between lean and obese children despite possible differences in fitness. Moreover, adults took shorter time to complete the protocol than children did, perhaps because of familiarity with the type of exercise. Technical limitations include the lack of blood collection throughout the exercise bout

and the lack of more sophisticated techniques to assess fat mobilization.

Summary We evaluated the hormonal and metabolic responses to a brief moderate intensity RE protocol in children and adults. We demonstrated some hormonal differences likely related to muscle mass activation (norepinephrine) and perhaps metabolism (glucagon). We further confirmed the higher reliance on fat metabolism among children compared with adults, even in response to a short RE protocol. Lastly, our findings contribute to emphasize that obesity in childhood negatively influences hormonal responses to exercise. Acknowledgments Supported by US Army Medical Research and Materiel Command Contract W81XWH-08-1-0025. The authors thank James Tufano, Jeremy Tan, and William Wallace for their assistance with data collection.

References 1. Adolfsson P, Nilsson S, Albertsson-Wikland K, Lindblad B. Hormonal response during physical exercise of different intensities in adolescents with type 1 diabetes and healthy controls. Pediatr Diabetes. 2012; 13(8):587–596. PubMed doi:10.1111/j.1399-5448.2012.00889.x 2. American College of Sports Medicine. ACSM’s Guidelines for exercise testing and prescription, 8th ed. Baltimore, MD: Wolters Kluwer, Lippincott Williams & Wilkins, 2010. 3. Berg A, Kim SS, Keul J. Skeletal muscle enzyme activities in healthy young subjects. Int J Sports Med. 1986; 7(4):236–239. PubMed doi:10.1055/s-2008-1025766 4. Chatzinikolaou A, Fatouros I, Petridou A, et al. Adipose tissue lipolysis is upregulated in lean and obese men during acute resistance exercise. Diabetes Care. 2008; 31(7):1397–1399. PubMed doi:10.2337/dc08-0072 5. Council on Sports Medicine and Fitness, McCambridge TM, Sticker PR. Strength training by children and adolescents. Pediatrics. 2008; 121(4):835–840. PubMed doi:10.1542/peds.2007-3790 6. Cowie CC, Rust KF, Byrd-Holt DD, et al. Prevalence of diabetes and impaired fasting glucose in adults in the U.S. population: National Health and Nutrition Examination Survey 1999-2002. Diabetes Care. 2006; 29(6):1263– 1268. PubMed doi:10.2337/dc06-0062 7. Delamarche P, Gratas-Delamarche A, Monnier M, Mayet MH, Koubi HE, Favier R. Glucoregulation and hormonal changes during prolonged exercise in boys and girls. Eur J Appl Physiol Occup Physiol. 1994; 68(1):3–8. PubMed doi:10.1007/BF00599234 8. Eliakim A, Brasel JA, Cooper DM. GH response to exercise: assessment of the pituitary refractory period, and relationship with circulating components of the GH-IGF-I axis in adolescent females. J Pediatr Endocrinol Metab.

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1999; 12(1):47–55. PubMed doi:10.1515/JPEM.1999. 12.1.47 9. Eliakim A, Nemet D, Zaldivar F, et al. Reduced exerciseassociated response of the GH-IGF-I axis and catecholamines in obese children and adolescents. J Appl Physiol. 2006; 100(5):1630–1637. PubMed doi:10.1152/ japplphysiol.01072.2005 10. Fahey TD, Del Valle-Zuris A, Oehlsen G, Trieb M, Seymour J. Pubertal stage differences in hormonal and hematological responses to maximal exercise in males. J Appl Physiol. 1979; 46(4):823–827. PubMed 11. Frystyk J. Exercise and the growth hormone-insulin-like growth factor axis. Med Sci Sports Exerc. 2010; 42(1):58– 66. PubMed doi:10.1249/MSS.0b013e3181b07d2d 12. Garlaschi C, di Natale B, del Guercio MJ, Caccamo A, Gargantini L, Chiumello G. Effect of physical exercise on secretion of growth hormone, glucagon, and cortisol in obese and diabetic children. Diabetes. 1975; 24(8):758– 761. PubMed doi:10.2337/diab.24.8.758 13. George L, Bacha F, Lee S, Tfayli H, Adreatta E, Arslanian S. Surrogate estimates of insulin sensitivity in obese youth along the spectrum of glucose tolerance from normal to prediabetes to diabetes. J Clin Endocrinol Metab. 2011; 96(7):2136–2145. PubMed doi:10.1210/jc.2010-2813 14. Gregory SM, Spiering BA, Alemany JA, et al. Exercise-induced insulin-like growth factor I system concentrations after training in women. Med Sci Sports Exerc. 2013; 45(3):420–428. PubMed doi:10.1249/ MSS.0b013e3182750bd4 15. Guyton AC, Hall JE. Guyton and Hall textbook of medical physiology, 12th ed. Philadelphia, PA: Elsevier, 2011. 16. Kjaer M, Lange K. Adrenergic regulation of energy metabolism. In: Endocrinology of Physical Activity and Sport, 2nd ed., N Constantini and AC Hackney (Eds.). New York: Springer, 2013, pp. 167–174. 17. Kraemer WJ, Ratamess NA. Hormonal responses and adaptations to resistance exercise and training. Sports Med. 2005; 35(4):339–361. PubMed doi:10.2165/00007256200535040-00004 18. Lehmann M, Keul J, Korsten-Reck U. The influence of graduated treadmill exercise on plasma catecholamines, aerobic and anaerobic capacity in boys and adults. Eur J Appl Physiol Occup Physiol. 1981; 47(3):301–311. PubMed doi:10.1007/BF00422476 19. Lloyd RS, Faigenbaum AD, Stone MH, et al. Position statement on youth resistance training: the 2014 International Consensus. Br J Sports Med. 2014; 48:498–505. PubMed doi:10.1136/bjsports-2013-092952 20. Martinez LR, Haymes EM. Substrate utilization during treadmill running in prepubertal girls and women. Med Sci Sports Exerc. 1992; 24(9):975–983. PubMed doi:10.1249/00005768-199209000-00005 21. McCarthy HD, Cole TJ, Fry T, Jebb SA, Prentice AM. Body fat reference curves for children. Int J Obes. 2006; 30(4):598–602. PubMed doi:10.1038/sj.ijo.0803232 22. McMurray RG, Hackney AC. Interactions of metabolic hormones, adipose tissue and exercise. Sports Med. 2005; 35(5):393–412. PubMed doi:10.2165/00007256200535050-00003

23. Mittelman SD, Klier K, Braun S, Azen C, Geffner ME, Buchanan TA. Obese adolescents show impaired meal responses of the appetite-regulating hormones ghrelin and PYY. Obesity (Silver Spring). 2010; 18(5):918–925. PubMed doi:10.1038/oby.2009.499 24. Nemet D, Eliakim A. Growth hormone-insulin-like growth factor-1 and inflammatory response to a single exercise bout in children and adolescents. Med Sport Sci. 2010; 55:141–155. PubMed doi:10.1159/000321978 25. Ogden CL, Carroll MD, Kit BK, Flegal KM. Prevalence of obesity and trends in body mass index among US children and adolescents, 1999–2010. JAMA. 2012; 307(5):483–490. PubMed doi:10.1001/jama.2012.40 26. Ormsbee MJ, Choi MD, Medlin JK, et al. Regulation of fat metabolism during resistance exercise in sedentary lean and obese men. J Appl Physiol. 2009; 106(5):1529–1537. PubMed doi:10.1152/japplphysiol.91485.2008 27. Petersen AC, Crockett L, Richards M, Boxer A. A selfreport measure of pubertal status: reliability, validity, and initial norms. J Youth Adolesc. 1988; 17(2):117–133. PubMed doi:10.1007/BF01537962 28. Pomerants T, Tillmann V, Karelson K, Jurimae J, Jurimae T. Impact of acute exercise on bone turnover and growth hormone/insulin-like growth factor axis in boys. J Sports Med Phys Fitness. 2008; 48(2):266–271. PubMed 29. Pullinen T, Mero A, Huttunen P, Pakarinen A, Komi PV. Resistance exercise-induced hormonal response under the influence of delayed onset muscle soreness in men and boys. Scand J Med Sci Sports. 2011; 21(6):e184–e194. PubMed doi:10.1111/j.1600-0838.2010.01238.x 30. Pullinen T, Mero A, MacDonald E, Pakarinen A, Komi PV. Plasma catecholamine and serum testosterone responses to four units of resistance exercise in young and adult male athletes. Eur J Appl Physiol Occup Physiol. 1998; 77(5):413–420. PubMed doi:10.1007/s004210050353 31. Robertson RJ, Goss FL, Andreacci JL, et al. Validation of the children’s OMNI RPE scale for stepping exercise. Med Sci Sports Exerc. 2005; 37(2):290–298. PubMed doi:10.1249/01.MSS.0000149888.39928.9F 32. Robertson RJ, Goss FL, Rutkowski J, et al. Concurrent validation of the OMNI perceived exertion scale for resistance exercise. Med Sci Sports Exerc. 2003; 35(2):333–341. PubMed doi:10.1249/01.MSS.0000048831.15016.2A 33. Rowland TW, Maresh CM, Charkoudian N, Vanderburgh PM, Castellani JW, Armstrong LE. Plasma norepinephrine responses to cycle exercise in boys and men. Int J Sports Med. 1996; 17(1):22–26. PubMed doi:10.1055/s-2007-972803 34. Rubin DA, Tufano JJ, McMurray RG. Endocrine responses to acute and chronic exercise in the developing child. In: Endocrinology of Physical Activity and Sport, 2nd ed., N Constantini and AC Hackney (Eds.). New York: Springer, 2013, pp. 417–436. 35. Strong WB, Malina RM, Blimkie CJ, et al. Evidence based physical activity for school-age youth. J Pediatr. 2005; 146(6):732–737. PubMed doi:10.1016/j. jpeds.2005.01.055 36. Thomas GA, Kraemer WJ, Comstock BA, et al. Effects of resistance exercise and obesity level on ghrelin and cor-

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tisol in men. Metabolism. 2012; 61(6):860–868. PubMed doi:10.1016/j.metabol.2011.10.015 37. Timmons BW, Bar-Or O, Riddell MC. Oxidation rate of exogenous carbohydrate during exercse is higher in boys than in men. J Appl Physiol. 2003; 94(1):278–284. PubMed 38. Veldhuis JD, Roemmich JN, Richmond EJ, et al. Endocrine control of body composition in infancy, childhood and puberty. Endocr Rev. 2005; 26(1):114–146. PubMed doi:10.1210/er.2003-0038

39. Vettor R, Macor C, Rossi E, Piemonte G, Federspil G. Impaired counterregulatory hormonal and metabolic response to exhaustive exercise in obese subjects. Acta Diabetol. 1997; 34(2):61–66. PubMed doi:10.1007/ s005920050068 40. Wirth A, Trager E, Scheele K, et al. Cardiopulmonary adjustment and metabolic response to maximal and submaximal physical exercise of boys and girls at different stages of maturity. Eur J Appl Physiol Occup Physiol. 1978; 39(4):229–240. PubMed doi:10.1007/BF00421446

Hormonal and metabolic responses to a resistance exercise protocol in lean children, obese children and lean adults.

During childhood, varying exercise modalities are recommended to stimulate normal growth, development, and health. This project investigated hormonal ...
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