The Journal of Nutrition Vol. 128 No. 1 January 1998, pp. 73-78

Acute and Chronic Resistive Exercise Increase Urinary Chromium Excretion in Men as Measured with an Enriched Chromium Stable Isotope^1,2

Michelle A. Rubin^*, John P. Miller, Alice S. Ryan, Margarita S. Treuth, Kristine Y. Patterson^**, Richard E. Pratley, Ben F. Hurley, Claude Veillon^**, Phylis B. Moser-Veillon^*, and Richard A. Anderson^{**, 3}

^* Department of Nutrition and Food Science,  Department of Kinesiology, University of Maryland, College Park, MD 21218; ^** USDA, Beltsville Human Nutrition Research Center, Nutrient Requirements and Functions Laboratory, Beltsville, MD 20705-2350; and  Division of Gerontology, Department of Medicine, University of Maryland at Baltimore, Baltimore VA Medical Center, Baltimore, MD 21201

	ABSTRACT

Abstract Introduction Methods Results Discussion References

Both exercise and chromium exert beneficial effects on insulin function. The mechanism by which exercise improves insulin response may involve an alteration in Cr metabolism. To determine the effects of acute and chronic resistive exercise on urinary Cr losses, we measured the effects of acute resistive exercise and 16 wk of resistive exercise training on urinary Cr losses of 10 men 53-63 y of age. Subjects consumed diets in compliance with the American Heart Association Phase I diet with a Cr content of 30 ± 4 µg/d. Sixteen weeks of resistive exercise training led to ~40% increases in upper and lower body strength, increases in fat-free mass and decreases in the percentage of body fat. An enriched stable isotope of Cr, ⁵³Cr, was employed to differentiate the exogenously administered Cr from the native endogenous Cr. Both acute and chronic resistive exercise increased ⁵³Cr losses. These data demonstrate that the improvements in body composition due to resistive exercise are associated with increased urinary Cr losses that are consistent with increased absorption.

	INTRODUCTION

Abstract Introduction Methods Results Discussion References

Most research on the effects of exercise on glucose metabolism has focused on aerobic exercise (Kahn et al. 1990, King et al. 1990, Seals et al. 1984, Tonino 1989). However, anaerobic exercise such as resistive exercise or strength training may be an ideal mode of exercise for older individuals. Chronic resistive exercise has been shown to increase bone mineral density (Menkes et al. 1993, Ryan et al. 1994), increase strength (Craig et al. 1989, Fiatarone et al. 1990, Menkes et al. 1993, Miller et al. 1994, Ryan et al. 1994, Smutok et al. 1993, Treuth et al. 1994), and in some cases, increase fat-free mass and decrease the percentage of body fat (Craig et al. 1989, Miller, J. et al. 1994, Miller, W. et al. 1984, Ryan et al. 1994, Treuth et al. 1994). Chronic resistive exercise also improves insulin response to a glucose load (Craig et al. 1989, Hurley et al. 1988, Smutok et al. 1993).

The mechanism for this improvement in glucose metabolism is unclear, but it is known that strength training increases glucose uptake through an enhanced insulin sensitivity (Miller et al. 1994). In addition, it is known that as a person ages there is a decrease in fat-free mass (FFM)³. It is conceivable that this loss of muscle mass is responsible for the glucose intolerance and hyperinsulinemia observed in older individuals (Fulop et al. 1987, Rowe et al. 1983, Shimokata et al. 1991). Increasing FFM may prevent the age-associated deterioration in glucose metabolism. However, this relationship has yet to be fully investigated.

Another proposed mechanism for an improvement in glucose tolerance and insulin sensitivity involves the trace mineral chromium (Cr). Cr is an essential trace element involved in carbohydrate metabolism (Anderson 1993 and 1995, Mertz 1993). Chromium alters blood glucose levels by potentiating insulin action. The U.S. Food and Nutrition Board has proposed a safe and adequate intake of 50-200 µg Cr/d for adults (NRC 1989). However, dietary intakes of Cr may be far below this level (Anderson 1993 and 1995, Anderson and Kozlovsky 1985, Bunker et al. 1984, Gibson and Scythes 1982). Perhaps the deterioration in glucose tolerance and insulin sensitivity associated with advancing age is associated with an alteration in Cr metabolism due to inadequate chromium intake, absorption and/or utilization.

Aerobic exercise has been shown to alter the excretion and distribution of Cr (Anderson et al. 1982, 1984 and 1988, Anderson 1993 and 1995, Vallerand et al. 1984). It is possible that the mechanism by which exercise improves insulin response involves an alteration in Cr metabolism. Our hypothesis was that resistive exercise, which leads to improved body composition, and glucose and insulin metabolism, also leads to increased Cr absorption. We used an enriched stable isotope of Cr, ⁵³Cr, to differentiate increased Cr losses of endogenous Cr from the ⁵³Cr that was given before and after resistive exercise and training. Essentially all absorbed Cr is excreted via the urine (Doisy et al. 1976).

	SUBJECTS AND METHODS

Abstract Introduction Methods Results Discussion References

Subjects.  Ten healthy, sedentary men between the ages of 53 and 63 y (59 ± 0.9 y, mean ± SEM) participated in the study. After receiving a detailed explanation of the procedures, subjects provided written consent as outlined by the Institutional Review Boards of the University of Maryland and the USDA Human Studies Committee. No subject had participated in any regular exercise program for at least 6 mo before the onset of the study. Only nondiabetic subjects who were free of cardiovascular and renal diseases were included in this study. Determinations were made by a physician on the basis of a medical exam, a graded exercise treadmill test, blood profile, urine analysis and a 2-h oral glucose tolerance test (Miller et al. 1994).

Strength testing and training.  Strength testing and training were conducted on Keiser K-300 variable resistance machines (Keiser Sports Health Inc., Fresno, CA). Before any testing, subjects were given a minimum of four training sessions to become accustomed to the equipment. Maximal force production (strength) was measured using a 3-repetition maximum test for the leg press, leg extension, chest press, lat pull-down, military press and upper back row exercise machines. The 3-repetition maximum test assessed the maximal resistance that could be moved three times through the full range of motion for each exercise.

Subjects strength trained on nonconsecutive days, three times a week for 16 wk. The strength training program consisted of the following 14 exercises: seated leg press, seated chest press, leg curl, lat pull-down, leg extension, military press, abductor-adductor machine, upper back row, seated triceps extension, trunk extension (lower back), abdominal crunches, seated dumbbell biceps curls and supine modified sit-ups. Before each training session, subjects completed a low intensity 3-min warm-up on a stationary cycle and 10 min of static stretching. Two exercise specialists and a registered nurse, who was also an exercise specialist, supervised each training session. After the accommodation period, the first three to four repetitions were performed at 90% of the 3-repetition maximum weight for each machine. The resistance was then decreased just enough to complete another one to three repetitions. This procedure was repeated for each subsequent two to three repetitions without altering the cadence of the exercises until 15 repetitions were performed. This protocol required subjects to exert almost maximal effort on every repetition. One set was performed for upper body exercises, and two sets were performed for lower body exercises. Approximately 90 s rest was allowed between each exercise. Blood pressure was monitored before the warm-up, after completion of the sixth exercise and 1 and 10 min postexercise.

Dietary control.  In an attempt to standardize diet, subjects were instructed by a trained nutrition counselor to follow the American Heart Association (AHA) Phase I diet, a diet comprised of <30% fat, 15% protein and 50-55% of total energy as carbohydrates with emphasis on complex carbohydrates. Saturated, monounsaturated and polyunsaturated ratio was 1:1:1. Compliance was monitored by analyzing 7-d food records and 24-h dietary recalls (Nutritionist III, Silverton OR). Subjects met with the nutrition counselor a minimum of once every 3 wk. Each subject was weight stable on the AHA diet for at least 6 wk before any testing.

Maximal oxygen uptake (VO_2 max).  VO_2 max was determined by using a progressive treadmill test as described (Miller et al. 1994). Briefly, expired air was collected at 1-min intervals into neoprene meteorological balloons and analyzed for oxygen and carbon dioxide concentrations by using a Model 2000 mass spectrometer (Airspec, Kent, England). Gas volumes were measured by using a Collins 120 L chain spirometer (Collins, Boston, MA). VO_2 max was considered to have been achieved if two of the following three criteria were met: 1) a plateau in oxygen uptake with an increasing workload; 2) a heart rate within 10 beats of the subject's age-predicted maximum heart rate; or 3) a respiratory exchange ratio > 1.10.

Body composition measurements.  The percentage of body fat was estimated from determination of body density using the hydrostatic weighing technique. Body density was determined after correction for residual lung volume, as measured by the oxygen-dilution method using the mass spectrometer (Wilmore et al. 1980). The percentage of body fat was estimated as described (Brozek et al. 1963).

Measurement of chromium metabolism using ⁵³Cr.  A chromium stable isotope, ⁵³Cr enriched to 98.2%, was used as a tracer to follow the metabolism of orally ingested chromium. During the pre- and posttraining phases of the study, one dose was given during a rested state (no exercise) and one dose was given immediately before a single exercise session (Fig. 1).

View larger version (19K): [in this window] [in a new window]   Fig 1. Study design of stable isotope and resistive exercise chromium study.

Dosing period 1.  Two weeks before the first day of exercise, subjects arrived at the laboratory in a fasted state. Subjects ingested ~300 µg (5.77 µmol) of ⁵³Cr as CrCl₃ in water and were instructed not to participate in any exercise for the next 72 h. Urine was collected for 72 h after the dosing in three separate jugs (0-24, 24-48 and 48-72 h). Urinary creatinine was determined to verify complete urine collection. The preweighed urine jugs containing the urine collections were reweighed to determine urinary volume. A specific gravity of 1.0 was assumed. Jugs were shaken, and urine samples were transferred into polyethylene bottles and frozen for future analyses. The subjects were instructed to record all food and beverages consumed during this 72-h time period.

Dosing period 2.  Two weeks after the initial dose, the subjects received their second dose. The administration of the dose was identical to dosing period 1. After ingestion of the dose, subjects completed a single exercise session. Urine collection was identical to that of dosing period 1. The subjects were instructed to record all food and beverages consumed during this 72-h time period.

Dosing period 3.  Two weeks before the completion of the 16 wk of strength training, the subjects consumed the third dose of ⁵³Cr. Dosing period 3 was identical to dosing period 2. The 72-h diet record that was recorded during dose period 2 was replicated for dosing period 3.

Dosing period 4.  Four days after the last bout of resistive exercise, dosing period 4 was completed. Dosing period 4 was identical to dosing period 1. The 72-h diet record that was recorded during dosing period 1 was replicated for dosing period 4.

During wk 8 of the study, subjects completed a 24-h duplicate diet collection. This consisted of the subjects collecting duplicate samples of all of the foods and beverages consumed in a 24-h period. The duplicate diets were weighed and homogenized in a blender equipped with low Cr steel blades. The homogenized diets were transferred into polyethylene tubes and frozen for future analysis.

Analytical determination.  Diets were thawed and mixed, and 1 g of each diet was weighed out. Samples were dried (Model 42 RePP Freeze Drier; FTS Systems, Stone Ridge, NY) and the percentage of moisture was determined. Digestion was conducted by using the wet and dry ashing technique described by Hill et al. (1986). Samples were analyzed for Cr content using atomic absorption spectrometry (Anderson and Kozlovsky 1985) with a graphite furnace (Perkin Elmer Model 5000; Perkin Elemer, Norwalk, CT) equipped with Zeeman background correction (Perkin Elmer Model HGA 500). National Institute of Standards and Technology (Gaithersburg, MD) standard reference material 1577, bovine liver, was used as a control. Comparison with the standard curve was used to determine the amount of Cr present in each diet sample.

Urine samples were thawed and ~3 g was weighed into acid-cleaned silanized quartz tubes. A weighed aliquot of ~0.1 g of 9.5 ng ⁵⁰Cr/g was added to each sample, and 0.025 g to the blanks, as an internal standard. Digestion and chelation of samples were as described by Veillon et al. (1994). All samples from each individual were analyzed simultaneously.

Urine samples were analyzed by gas chromatography-mass spectroscopy (Veillon et al. 1994) [Finnigan Model 9610 gas chromatograph (GC) linked to a Finnigan Model 4000 mass spectrometers; San Jose, CA]. The GC column was a 2 mm × 3 m silanized borosilicate glass tube, packed with 1% SP-2401 on Chromosorb 750, 100-120 mesh. The injection temperature was 175°C and column temperature was 130°C. Masses 356, 358 and 359 corresponding to ⁵⁰Cr(tfa)⁺₂, ⁵²Cr(tfa)⁺₂ and ⁵³Cr(tfa)⁺₂ were monitored. A USDA urine pool that had also been analyzed by graphite furnace atomic absorption spectroscopy was used as an internal control for each assay.

Statistical Analyses  Paired t tests were used to determine differences between untrained and trained means for the following variables: body weight, (FFM) the percentage of body fat, VO_2 max and various strength measurements. A two-way ANOVA was used to determine differences in urinary excretion of ⁵³Cr and natural Cr at each time point (0-24, 24-48 and 48-72 h postdose) between dosing periods. Urinary excretion of ⁵³Cr was expressed as a percentage of dose. All values are expressed as means ± SEM. Differences were considered significant at P < 0.05.

	RESULTS

Abstract Introduction Methods Results Discussion References

Group characteristics.  There were no significant differences in VO_2 max and body weight before and after 16 wk of resistive exercise (Table 1). There was a 95% average attendance and all subjects completed the study.

Nutritional evaluation.  Analysis of food records verified that subjects complied with the AHA diet. There were no significant differences in 7-d food record values before and after training for total energy (9364 ± 289 vs. 9606 ± 289 kJ) or percentage of energy derived from fat (30 ± 0.4 vs. 30 ± 0.2%), protein (18 ± 0.5 vs. 18 ± 1%) and carbohydrate (51 ± 1 vs. 51 ± 1%). Daily Cr intake, based on analysis of duplicate diets, was 30 ± 4 µg/d.

Muscular strength.  The resistive exercise program resulted in a 40% increase in upper body strength (P < 0.001) and a 41% increase in lower body strength (P < 0.001). This accounted for a 41% increase in total body strength (P < 0.001) when the 3-repetition maximum strength test results were summed (Table 2).

Urinary excretion of ⁵³Cr.  The urinary losses of ⁵³Cr were increased significantly by a single bout of exercise on the basis of urinary losses 0-24 h postdose (Fig. 2). Urinary ⁵³Cr losses in the initial 24 h after an oral dose increased from 0.65 ± 0.05% during rest to 0.94 ± 0.11% during the exercise period. Sixteen weeks of strength training also increased losses of ⁵³Cr 24-48 h (0.25 ± 0.02 to 0.34 ± 0.03%) and 48-72 h post-dose (0.15 ± 0.01 to 0.20 ± 0.02%) (Fig. 3).

View larger version (23K): [in this window] [in a new window]   Fig 2. Urinary excretion of 53Cr following no exercise and after resistive strength training session in 53- to 63-y-old men. Similar changes were observed before and after training; the data are combined. Values are means ± SEM, n = 22. *P < 0.05.

View larger version (23K): [in this window] [in a new window]   Fig 3. Urinary excretion of 53Cr before and after 16 wk of resistive exercise in 53- to 63-y-old men. Similar changes were observed following no exercise and after a strength training session; data are combined, n = 22. Values are means ± SEM, *P < 0.05.

	DISCUSSION

Abstract Introduction Methods Results Discussion References

Acute aerobic exercise increases Cr losses (Anderson et al. 1982, 1984 and 1988). However when only the total native Cr is measured, increased Cr losses cannot be differentiated from increased absorption and/or excretion. Increased urinary Cr losses could be due to increased tissue losses that are not accompanied by increased replenishment of tissue stores as a result of increased Cr absorption. In this study, with the use of ⁵³Cr, a stable isotope of Cr, we were able to differentiate the newly absorbed ⁵³Cr from endogenous tissue Cr losses. Because endogenous tissue stores would not contain ⁵³Cr, all ⁵³Cr excreted in the urine would be due to newly absorbed ⁵³Cr and not increased excretion from tissue stores.

Within 24 h of a single exercise session, there was a significant increase in ⁵³Cr urinary excretion of the newly absorbed ⁵³Cr. The extra Cr lost due to acute and chronic resistive exercise appears to have been replenished by increased Cr absorption, leading to little or no net loss of Cr as a result of exercise.

Increased Cr absorption associated with acute and chronic resistive exercise is important from a human health view because the Cr status of most individuals is marginal (Anderson 1993 and 1995). If not replenished, increased losses due to acute exercise could further exacerbate Cr status. This would be inconsistent with the observation that exercise (Fulop et al. 1987, Kahn et al. 1990, King et al. 1990, Kovisto et al. 1986, Shimokata et al. 1991, Treuth et al. 1994), as well as Cr, leads to improved glucose utilization (Anderson 1993 and 1995, Anderson et al. 1982, Mertz 1993).

Miller et al. (1984) also observed that strength training improved insulin response to a glucose load without a change in glucose tolerance. Smutok et al. (1993) observed both an improvement in insulin response and glucose tolerance in subjects with either impaired glucose tolerance or type II diabetes. As part of this study, Miller et al. (1994) determined that 16 wk of chronic resistive exercise did not change fasting glucose or areas concentrations under the glucose response curves. Areas under the insulin response curves but not fasting insulin concentrations decreased. Improvements in insulin response without a change in glucose tolerance suggest an improvement in insulin sensitivity.

It has been suggested that strength training may improve glucose-stimulated insulin response by increasing FFM (Craig et al. 1989, Fiatarone et al. 1990, Fulop et al. 1987). In this study, we found a significant increase in FFM after 16 wk of resistive exercise. Increased dietary Cr intake has also been shown to increase lean body mass and decrease the percentage of body fat in humans and pigs (Kaats et al. 1996, Lindemann et al. 1995, Page et al. 1993). Not all investigators (Hallmark et al. 1996, Lukaski et al. 1996) have reported significant effects of Cr on body composition or glucose and insulin variables (see Anderson 1993 and 1995 for reviews). In addition to effects on body composition, improved Cr nutrition also leads to improved glucose and insulin metabolism in humans and experimental animals (Anderson 1993 and 1995, Mertz 1993). Further studies are required to determine whether there is a relation between the similar responses to exercise and Cr. Accompanying the improved glucose and insulin responses associated with exercise, there is also an increase in ⁵³Cr excretion in response to acute exercise and training (Fig. 3).

In conclusion, this study demonstrates that there may be an increase in Cr absorption in response to acute exercise and strength training as determined by the increased excretion of the ⁵³Cr isotope. There was also an improvement in insulin response to a glucose load, a decrease in the percentage of body fat and an increase in FFM. Because improved Cr metabolism and exercise both lead to improved glucose and insulin metabolism and body composition, it is likely that some of the improvements due to exercise are related to increased Cr absorption. However, further studies are required to address these issues and to determine if the apparent increase in Cr absorption could be partially responsible for exercise training-induced improvements in insulin response.

	ACKNOWLEDGMENTS

The authors thank Noella Bryden and Andrew Goldberg for their support and assistance.

	FOOTNOTES

Manuscript received 29 April 1997. Initial reviews completed 12 June 1997. Revision accepted 15 September 1997.

	LITERATURE CITED

Abstract Introduction Methods Results Discussion References

• Anderson, R. A. (1993) Recent advances in the clinical and biochemical effects of chromium deficiency. In: Essential and Toxic Elements in Human Health and Disease: An Update, (Prasad, A. S., ed.), pp. 221-234. Wiley Liss, New York, NY.
• Anderson R. A. Chromium, glucose tolerance, diabetes and lipid metabolism. J. Advancement Med. 1995; 8:37-49
• Anderson R. A., Bryden N. A., Polansky M. M., Deuster P. A. Exercise effects on chromium excretion of trained and untrained men consuming a constant diet. J. Appl. Physiol. 1988; 64:249-252 ^{[Abstract/Free Full Text]}
• Anderson R. A., Kozlovsky A. S. Chromium intake, absorption, and excretion of subjects consuming self-selected diets. Am. J. Clin. Nutr. 1985; 41:1171-1183
• Anderson R. A., Polansky M. M., Bryden N. A. Strenuous running: acute effects on chromium, zinc and selected clinical variables in urine and serum of male runners. Biol. Trace Elem. Res. 1984; 6:327-336
• Anderson R. A., Polansky M. M., Bryden N. A., Roginski E. E., Patterson K. Y., Reamer D. C. Effect of exercise (running) on serum glucose, insulin, glucagon, and chromium excretion. Diabetes 1982; 31:212-216 [Abstract]
• Brozek J., Grande F., Anderson J., Keys A. Densitometric analysis of body composition: revision of some quantitative assumptions. Ann. N.Y. Acad. Sci. 1963; 110:113-140
• Bunker V. W., Lawson M. S., Delves H. R., Clayton B. E. The uptake and excretion of chromium by the elderly. Am. J. Clin. Nutr. 1984; 39:792-802 ^{[Abstract/Free Full Text]}
• Craig B. W., Everhart J., Brown R. The influence of high-resistive training on glucose tolerance in young and elderly subjects. Mech. Aging Dev. 1989; 49:147-157
• Doisy, R. J., Streeten, D.H.P., Freiberg, J. M., and Schneider, A. J. (1976) Chromium metabolism in man and biochemical effects. In: Trace Elements in Human Health and Disease, Vol. II. Essential and Toxic Elements (Prasad, A. S. & Oberleas, D., eds.), pp. 79-104. Academic Press, New York, NY.
• Fiatarone M. A., Marks E. C., Ryan N. D., Meredith C. N., Lipsitz L. A., Evans W. J. High-intensity strength training in nonagenarians: effects on skeletal muscle. J. Am. Med. Assoc. 1990; 263:3029-3034 [Abstract/Free Full Text]
• Fulop T., Nagy J. T., Worum I., Foris G., Mudri K., Varga P., Udardy M. Glucose intolerance and insulin resistance with aging: studies on insulin receptors and post-receptor events. Arch. Gerontol. Geriat. 1987; 6:107-115 [Medline]
• Gibson R. S., Scythes C. A. Chromium, selenium, and other trace element intakes of a selected sample of Canadian premenopausal women. Biol. Trace Elem. Res. 1982; 6:105-116
• Hallmark M. A., Reynolds T. H., DeSouza C. A., Dotson C. O., Anderson R. A., Rogers M. A. Effects of chromium and resistance training on muscle strength and body composition. Med. Sci. Sports Exer. 1996; 28:139-144 [Medline]
• Hill A. D., Patterson K. Y., Veillon C., Morris E. R. Digestion of biological materials for mineral analysis using a combination of wet and dry ashing. Anal. Chem. 1986; 58:2340-2342
• Hurley B. F., Hagberg J. M., Goldberg A. P., Seals D. R., Ehsani A. A., Brennan R. E., Holloszy J. O. Resistive training can reduce coronary risk factors without altering VO2max or percent body fat. Med. Sci. Sports Exer. 1988; 20:150-154 [Medline]
• Kaats G. R., Blum K., Fisher J. A., Adelman J. A. Effects of chromium picolinate supplementation on body composition: a randomized, double-masked, placebo-controlled study. Curr. Ther. Res. 1996; 57:747-756
• Kahn S. E., Larson V. G., Beard J. C., Cain K. C., Fellingham G. W., Schwartz R. S., Veith R. C., Stratton J. R., Cerqueira M. D., Abrass I. B. Effect of exercise on insulin action, glucose tolerance, and insulin secretion in aging. Am. J. Physiol. 1990; 258:E937-E943 [Abstract/Free Full Text]
• King D. S., Staten M. A., Kohrt W. M., Dalsky G. P., Elahi D., Holloszy J. O. Insulin secretory capacity in endurance-trained and untrained young men. Am. J. Physiol. 1990; 259:E155-E161 [Abstract/Free Full Text]
• Kovisto V. A., Yki-Jarvinen H., DeFronzo R. A. Physical training and insulin sensitivity. Diabetes/Metab. Rev. 1986; 1:445-481
• Lindemann M. D., Wood C. M., Harper A. F., Kornegay E. T., Anderson R. A. Dietary chromium picolinate additions improve gain:feed and carcass characteristics in growing-finishing pigs and increase litter size in reproducing sows. J. Anim. Sci. 1995; 73:457-454 [Abstract]
• Lukaski H. C., Bolonchuk W., Siders W. A., Milne D. Chromium supplementation and resistance training: effects on body composition, strength and trace element status of men. Am. J. Clin. Nutr. 1996; 63:954-965 [Abstract/Free Full Text]
• Menkes A., Mazel S., Redmond R. A., Koffler K., Libanati C. R., Gundberg C. M., Zizic T. M., Hagberg J. M., Pratley R. E., Hurley B. F. Strength training increases regional bone mineral density and bone remolding in middle-aged and older men. J. Appl. Physiol. 1993; 74:2478-2484 ^{[Abstract/Free Full Text]}
• Mertz W. Chromium in human nutrition: a review. J. Nutr. 1993; 123:626-633
• Miller J., Pratley R. E., Gordon P., Rubin M., Treuth M., Ryan A., Hurley B. F., Goldberg A. P. Strength training increases insulin action in healthy 50-65 year old men. J. Appl. Physiol. 1994; 77:1122-1127 ^{[Abstract/Free Full Text]}
• Miller W. J., Sherman W. M., Ivy J. L. Effect of strength training on glucose tolerance and post-glucose insulin response. Med. Sci. Sports Exer. 1984; 16:539-543 [Medline]
• National Research Council (1989) Recommended Dietary Allowances. National Academy of Sciences, Washington, DC.
• Page T. G., Southern L. L., Ward T. L., Thompson, D. L. Jr. Effect of chromium picolinate on growth and serum and carcass traits of growing-finishing pigs. J. Anim. Sci. 1993; 71:656-662 [Abstract]
• Rowe J. W., Minaker K. L., Pallotta J. A., Flier J. S. Characterization of the insulin resistance of aging. J. Clin. Invest. 1983; 71:1581-1587
• Ryan A. S., Treuth M. S., Rubin M. A., Miller J. P., Nicklas B. J., Landis D. M., Pratley R. E., Libanati C. R., Gundberg C. M., Hurley B. F. Effects of strength training on bone mineral density: hormonal and bone turnover relationships. J. Appl. Physiol. 1994; 77:1678-1684 ^{[Abstract/Free Full Text]}
• Seals D. R., Hagberg J. M., Hurley B. F., Ehsanni A. A., Holloszy J. O. Effects of endurance training on glucose tolerance and plasma lipid levels in older men and women. J. Am. Med. Assoc. 1984; 252:645-649 [Abstract/Free Full Text]
• Shimokata H., Muller D. C., Fleg J. L., Sorkin J., Ziemba A. W., Andres R. Age as independent determinant of glucose tolerance. Diabetes 1991; 40:44-51 [Abstract]
• Smutok M. A., Reece C., Kokkinos P. F., Dawson P., Shulman R., DeVane-Bell J., Patterson J., Charabogas C., Goldberg A. P., Hurley B. F. Aerobic vs strength training for risk factor intervention in middle-aged men at high risk for coronary heart disease. Metabolism 1993; 42:177-184 [Medline]
• Tonino R. P. Effect of physical training on the insulin resistance of aging. Am. J. Physiol. 1989; 256:E352-E356 [Abstract/Free Full Text]
• Treuth M. S., Ryan A. S., Pratley R. E., Rubin M. A., Miller J. P., Nicklas B. J., Sorkin J., Harman S. M., Goldberg A. P., Hurley B. F. Effects of strength training on total and regional body composition in older men. J. Appl. Physiol. 1994; 77:614-620 ^{[Abstract/Free Full Text]}
• Vallerand A. L., Cuerrier J. P., Shapcott D., Vallerand R. J., Gardiner P. F. Influence of exercise training on tissue chromium concentrations in the rat. Am. J. Clin. Nutr. 1984; 39:402-409 [Abstract/Free Full Text]
• Veillon C., Patterson K. Y., Rubin M. R., Moser-Veillon P. B. Determination of natural and isotopically encriched chromium in urine by isotope dilution gas chromatography-mass spectrometry. Anal. Chem. 1994; 66:856-860
• Wilmore J. H., Vodak P. A., Parr R. B., Girandol R. N., Billing J. E. Further simplification of a method for determination of residual lung volume. Med. Sci. Sports Exer. 1980; 12:216-218 [Medline]

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