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Basic Sciences: Original Investigations

Recovery of Muscle Glycogen Concentrations in Sled Dogs during Prolonged Exercise

MCKENZIE, ERICA1; HOLBROOK, TODD2; WILLIAMSON, KATHY1; ROYER, CHRISTOPHER1; VALBERG, STEPHANIE3; HINCHCLIFF, KEN4; JOSE-CUNILLERAS, EDUARD4; NELSON, STUART5; WILLARD, MICHAEL6; DAVIS, MICHAEL1

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Medicine & Science in Sports & Exercise: August 2005 - Volume 37 - Issue 8 - p 1307-1312
doi: 10.1249/01.mss.0000175086.41080.01
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Abstract

Alaskan sled dogs are elite endurance athletes, capable of running 250 to 300 km·d−1 at a pace of 15–20 km·h−1 over many consecutive days in extreme conditions (23). Racing sled dogs have a remarkably high sustained metabolic rate during competition, necessitating a large metabolizable energy intake. Energy expenditure by dogs during racing can approximate 50,000 kJ·d−1 (11.95 Mcal·d−1) (11). Sled dogs usually consume a diet high in fat (>50% of energy content) and protein (>25%) and low in carbohydrate (<20%) to maximize caloric intake and to reduce musculoskeletal injury and other syndromes that arise with low protein intake in exercising sled dogs (24).

Muscle glycogen depletion is a critical factor associated with fatigue during prolonged submaximal exercise (9). It is suggested that sustained or repeated exercise combined with minimal carbohydrate intake promotes cumulative muscle glycogen depletion and eventual fatigue (2,7). However, sled dogs appear highly fatigue resistant, and withdrawal from endurance races is frequently the result of other conditions, including musculoskeletal injury and gastrointestinal disease (16).

Several studies have examined glycogen depletion and restitution in sled dogs (22,23,29). These studies determined that there was slow repletion of muscle glycogen in sled dogs that were not administered a carbohydrate supplement immediately following exercise. Furthermore, a high-fat diet was associated with a glycogen-sparing effect. However, these studies involved single bouts of exercise performed over limited distances of 30 km or less (22,23,29). Similarly, the majority of studies of muscle glycogen metabolism in other species, including rats and humans, have also focused on the impact of single exercise bouts or repeated high-intensity sprints (8,14). The objective of this study was to determine the cumulative effects of repeated prolonged submaximal exercise on muscle glycogen stores in elite sled dogs. We hypothesized that Alaskan sled dogs are capable of maintaining muscle glycogen concentrations during prolonged endurance exercise, allowing them to run extreme distances on a repeated basis without developing fatigue related to muscle glycogen depletion.

MATERIALS AND METHODS

Dogs.

Forty-two healthy Alaskan sled dogs in training for multiday endurance racing were used in the study. Dogs ranged in age from 2 to 7.5 yr (mean 4 yr) and comprised 25 males and 17 females. Mean body weight was 22.3 ± 2.8 kg. All dogs were sexually intact. Dogs were selected by the musher based on their degree of fitness and the musher’s assessment of the dog’s ability to successfully complete the 800-km distance.

Training.

Dogs were exercised an average of 4 d·wk−1, with short training runs of 8 km in distance that progressively increased over 5 months to a maximum distance of 80 km. At the beginning of the study, the selected dogs had accumulated an average of 2314 ± 221 km of training distance (range 1464–2645). Dogs were rested from training for 3 d before the start of the trial.

Experimental design.

All procedures were approved by the Oklahoma State University Institutional Animal Care and Use Committee according to the principles outlined in the NIH Guide for the Care and Use of Laboratory Animals. The trial was performed in January in Alaska with ample snow cover. Initially, dogs were randomly divided into two teams of 18 animals that commenced running 1 h apart. Dogs pulled a lightly laden sled and a musher 80 km in approximately 5 h, which is estimated to require approximately 40% of maximal oxygen uptake (22). After completing 80 km, the dogs were fed and rested for 7–8 h at a remote location. The dogs then ran the 80-km return journey to the base station where they underwent sampling procedures including collection of jugular venous blood samples. Serum was frozen and analyzed for creatine kinase (CK) activity within 48 h of collection.

After the completion of each 160 km, six dogs were randomly selected for muscle biopsy. Following the procedure, dogs were provided a full meal and withdrawn from further running. Dogs that did not undergo muscle biopsy were provided a full meal and allowed to rest for 6–8 h before the next exercise phase.

Teams were reorganized to equalize the number of remaining dogs after removal of the six dogs randomly selected for muscle biopsy. When the number of running dogs was reduced to 16 after the third day of running, the remaining dogs were combined into a single team for the final two 160-km runs.

Dietary formulation.

All dogs consumed a similar diet. Shortly before each 160-km run, dogs received beef broth (protein: 40%; fat: 57% of energy content) providing approximately 670 kcal. At the remote location, dogs received a meal consisting of beef, fish, and commercial dried dog food (The Iams Company, Dayton, OH) providing approximately 540 kcal (protein: 37.2%; fat: 43.7%; carbohydrate: 17.5%). Shortly before commencing the 80-km return journey, dogs received beef broth again (670 kcal). After completing 160 km, dogs were fed approximately 1700 kcal (protein: 27.7%; fat: 54.6%; carbohydrate:17.7%) in the form of a beef–liver–tripe combination, commercial dried dog food, and a commercial fat supplement.

On days 4 and 5 of the trial, daily food intake of the running dogs was increased at the discretion of the musher. Prerun beef broth intake doubled (1370 kcal). The amount of beef contained in the remote location meal was increased providing a total of 695 kcal (protein: 37.8%; fat: 46.6%; carbohydrate: 13.7%), and prerun intake of beef broth at the remote location was also doubled (1370 kcal). The postrun meal of the beef-liver-tripe combination and the fat product was doubled, and the amount of dried dog food provided increased by 136 g (1 cup) so that dogs consumed 2850 kcal (protein: 27.7%; fat: 57.9% fat; carbohydrate: 14.4%) at the conclusion of each of the two final 160-km runs.

Muscle biopsy.

Dogs were sedated with a combination of acepromazine (0.025 mg·kg−1) and buprenorphine (0.01 mg·kg−1) administered intramuscularly. A small area of skin over the center of the biceps femoris muscle was clipped and aseptically prepared with the dogs in lateral recumbency. The biopsy site was desensitized via injection of 0.5 mL of 1% lidocaine into the skin and subcutis, and a stab incision was made through the skin and fascia of the biceps femoris muscle using a size 10 scalpel blade. Muscle samples were obtained from the center of the biceps femoris muscle using an 8-gauge UCH skeletal muscle biopsy needle (Dyna Medical Corp., London, Ontario, Canada) while suction was applied to the needle using a 60-mL syringe attached to a 23-inch extension set. The site of the biopsy was approximately mid-femur. Two samples of muscle tissue were taken through the initial incision, and, if inadequate muscle volume was obtained, a third sample was obtained from the biceps femoris of the opposite leg in the same location. Muscle samples were gently blotted and then immediately weighed on a microbalance to ensure a minimum of 60 mg of muscle tissue was obtained from each dog. Muscle samples for measurement of glycogen content were immediately frozen in liquid nitrogen and stored at −80°C for later analysis. Muscle samples for histopathological analysis were rolled in talcum powder to prevent freeze artifacts and dropped in liquid nitrogen. Samples were stored at −80°C until analyzed.

Sample analysis.

Muscle samples for analysis of glycogen concentrations were freeze-dried for 18 h and dissected free of blood, fat, and connective tissue under a stereomicroscope. Samples (1–4 mg) were boiled in 1 mol·L−1 HCl for 2 h to produce glucose residues that were subsequently assayed by fluorometric analysis according to the methods of Lowry and Passonneau (17).

Samples for histochemical analysis were oriented in cross-section in chilled OCT tissue medium on thin sections of cork and immediately dipped in liquid nitrogen. Ten micron thick samples were cut on a cryostat, and serial sections were stained with hematoxylin and eosin (H&E), periodic acid–Schiff (PAS) stains and for myosin ATPase activity at pH 9.8 (27). Sections stained with PAS were given a grade of 1 through 5 based on subjective staining intensity (1 = minimal intensity staining, 5 = intense staining) (5).

Statistical analysis.

The data were analyzed using commercial statistical software (PC SAS Version 8.2, SAS Institute Inc., Cary, NC) using PROC MIXED and a DIFF option in an LSMEANS statement. PAS staining intensity and muscle glycogen concentrations were compared using Spearman’s correlation.

RESULTS

On average, body weight fluctuated 1.06 ± 0.43 kg in running dogs during the five exercise days with no significant changes between days. Three dogs were prematurely removed from teams before completing their scheduled 160-km run for that day. One dog was removed during running on day 3 due to vomiting and lethargy. A muscle biopsy was obtained from this dog, but only the datum pertaining to mean biopsy mass was included in the analysis. During days 3 and day 4, one dog was removed each day due to lameness. Muscle biopsies were not obtained from these dogs.

Run times.

The dog teams averaged a pace of 17.4 ± 0.8 km·h−1 (range 15.7–18.4 km·h−1) running to the remote location, where they rested for an average of 7 h 25 ± 22 min. On the 80-km return journey to base camp, dog teams averaged a pace of 17.1 ± 1.3 km·h−1 (range 15.0– 9.2 km·h−1) and rested for an average of 7 h 29 ± 47 min before commencing another 160-km round trip.

Dogs ran the 80-km journey to the remote location in a mean time of 4 h 36 ± 14.5 min (range 4 h 20–5 h 05). The time taken for the return journey averaged 4 h 42 ± 23 min (range 4 h 10–5 h 20).

Muscle biopsy.

Muscle biopsy was performed on average 2 h 56 ± 35 min after the dogs ceased exercise. A mean of 71.6 ± 13.6 mg of muscle was obtained from each dog (range 43–101 mg). On average, 28.6 ± 10.3 mg of muscle was obtained with each needle insertion and 101 needle insertions were taken from the 42 dogs to obtain an adequate sample volume.

Muscle glycogen concentrations.

Muscle glycogen concentration was significantly greater in the resting control dogs compared to dogs that ran any distance (Fig. 1). Muscle glycogen concentrations were significantly lower in dogs after running 160 km compared to dogs that ran any further distance. Muscle glycogen concentrations did not differ between dogs that ran 320 km or more.

FIGURE 1— Muscle glycogen concentrations in Alaskan sled dogs running 160 km·d−1 for 5 d. Horizontal bars denote mean values for each group. a,b,c Groups with different superscript letters have means that are significantly different to one another.
FIGURE 1— Muscle glycogen concentrations in Alaskan sled dogs running 160 km·d−1 for 5 d. Horizontal bars denote mean values for each group. a,b,c Groups with different superscript letters have means that are significantly different to one another.

Serum CK activity.

Median serum CK activity (Fig. 2) in the 42 dogs was 163 IU·L−1 before exercise (range 75–620) and increased significantly following 160 km of running (median 2202, range 819–8830). Serum CK activity remained elevated after each subsequent 160-km run (320 km: 2464, range 754–23,730; 480 km: 2377, range 390–20,540; 640 km: 2456, range 336–12,375; 800 km: 1132, range 354–5588).

FIGURE 2— Serum creatine kinase activity in Alaskan sled dogs running 160 km·d−1 for 5 d. a,b Groups with different superscript letters have means that are significantly different to one another. 0 km:
FIGURE 2— Serum creatine kinase activity in Alaskan sled dogs running 160 km·d−1 for 5 d. a,b Groups with different superscript letters have means that are significantly different to one another. 0 km::
N = 42; 160 km: N = 36; 320 km: N = 28; 480 km: N = 21; 640 km: N = 16; 800 km: N = 10.

Histopathology and histochemistry.

Muscle samples from 36 dogs were of sufficient cross-sectional area and quality to perform histological analyses. No histopathological abnormalities were observed on microscopic examination of H&E-stained sections from any of the running (N = 30) or control (N = 6) dogs. The mean ± SD staining intensity (out of 5) for PAS per group was as follows: rest: 5.0 ± 0; 160 km: 1.2 ± 0.4; 320 km: 2.8 ± 0.4; 480 km: 3.0 ± 0.5; 640 km: 2.8 ± 0.5; 800 km: 3.1 ± 0.4. The grade of PAS staining intensity significantly correlated to muscle glycogen concentrations with an r value of 0.83 (P < 0.0001). Myosin ATPase stained sections suitable for fiber type analysis were obtained from 27 running dogs and four controls. An average of 204 fibers was counted per section (range 113–261). Type 1 fibers comprised on average 40.1% ± 4.8% of fibers counted (range 30.3–48.4%) and type 2 fibers comprised 59.9% ± 4.8% (range 51.6–69.7%). There were no significant differences in fiber type composition between the groups of dogs that rested or ran the different distances.

DISCUSSION

The remarkable feature of the Alaskan sled dogs used in the current study was that while running 160 km·d−1 for 5 d, they did not develop cumulative glycogen depletion despite a relatively limited carbohydrate intake. The first bout of exercise led to considerable muscle glycogen depletion, but muscle glycogen concentrations after four subsequent bouts of similar-intensity exercise were considerably greater than the first, and no different to each other, further supporting the hypothesis that repeated bouts of exercise prompt enhanced oxidation of noncarbohydrate substrates such as free fatty acids, intracellular lipids, ketones, and plasma glucose during prolonged exercise. Additionally, rapid restitution of muscle glycogen during recovery periods may also have prevented cumulative depletion (2). The relative contribution of each of these mechanisms to maintenance of muscle glycogen concentrations in sled dogs in the current study could not be determined due to the study design. In fasted rats subjected to three repeated bouts of brief high-intensity exercise, muscle glycogen stores after the initial bout of exercise were only partially restored, but all glycogen mobilized in the following two exercise sessions was completely replenished during recovery. This suggests that there may be a critical concentration of muscle glycogen that is protected against sustained depletion with repeated exercise (8). Increased oxidation of fats and ketones may have contributed to the maintenance of muscle glycogen concentrations during repeated exercise as higher plasma concentrations of free fatty acids and ketones were observed in the rats following subsequent bouts of exercise as compared to the first bout (8). Similarly, the dogs in the current study displayed depletion of intramuscular triglyceride accompanied by hyperglycerolemia and hyperketonemia, indicating that utilization of fat-based sources likely played an integral role in supporting continued exercise (12)

At the commencement of submaximal exercise, energy for muscular contraction is initially supplied by limited intramuscular stores of creatine phosphate and adenosine triphosphate, and anaerobic utilization of cellular glycogen. However, as exercise continues, substrate utilization during low-intensity exercise moves progressively from carbohydrate to fat-derived substrates (4). Canine skeletal muscle is composed almost completely of highly oxidative fibers (types I and II A) imparting a considerable ability to utilize fat-derived energy sources during exercise (27). Fat-based substrates available for energy metabolism during exercise include plasma fatty acids, ketone bodies, and intra- and extramuscular triglyceride. Dogs have a greater capacity to transport free fatty acids than less aerobic mammals and can potentially increase their capacity to metabolize fat in response to a high-fat diet (19,20). Consumption of a high-carbohydrate diet has negative effects on canine exercise performance (6). In contrast, consumption of a high-fat, high-protein diet preserves muscle glycogen stores during exercise and reduces the incidence of musculoskeletal injury in sled dogs (22,24). It is likely that increased fat metabolism occurred in the dogs throughout the current study that supported continued exercise without cumulative muscle glycogen depletion. Additionally, protein may be a quantitatively important energy substrate in dogs as compared to other species due to a greater inherent gluconeogenic capacity (29). Commencing exercise with depleted muscle glycogen stores has been associated with increased protein degradation in human skeletal muscle (1).

Restoration of muscle glycogen stores after exercise in the face of negligible carbohydrate intake is mediated by hepatic gluconeogenesis and muscle glyco(neo)genesis (18,26). Furthermore, transfer of glycogen from nonexercising to exercising muscle groups during recovery has been demonstrated in humans (15); however, given the quadrupedal nature of dogs, the amount of nonexercising muscle mass available to participate in the recovery processes is most likely limited. Muscle glycogen concentration has a profound regulatory effect on glucose uptake and insulin sensitivity (25) and affects the rate of glycogen resynthesis in early postexercise recovery (18,30). Low muscle glycogen concentrations prompt an increased rate of resynthesis in proportion to the degree of depletion. Enhanced glycogen repletion following prolonged exercise could be attributable to upregulation of glucose transporter 4, glycogenin, and/or interleukin 6 expression, increased sensitivity of skeletal muscle to insulin, and accelerated gluconeogenesis, although these mechanisms were not investigated in the current study (13,14).

Previous studies in sled dogs performing single bouts of exercise have found relatively slow rates of muscle glycogen repletion during recovery, although repletion rates may be comparable to those of fasted humans (18,23,29). In the current study, the rate of muscle glycogen repletion was not determined, but at the time of biopsy 2–4 h after the first bout of exercise muscle glycogen concentration was approximately 21% of resting values. However, on subsequent days of equidistant exercise, muscle glycogen concentrations were severalfold higher, at 52–65% of resting values. These findings indicate that the initial 160-km run produced intense compensatory changes directed toward replenishing and/or preserving muscle glycogen concentrations during continued exercise. Interestingly, the increase in caloric intake over days 4 and 5 had no apparent impact on postexercise muscle glycogen repletion on these days. During a study of 2 d of sustained exhaustive cycling in humans, significant differences were observed in the hormonal milieu of the subjects on the second day of exercise as compared to the first, further supporting the hypothesis that repeated bouts of exercise prompt progressively more vigorous compensatory changes to support continued exercise (3). Human athletes subject to prolonged multiday endurance exercise may potentially also limit utilization of muscle glycogen and progressively utilize alternative substrates during continued exercise. It is probable that the dog may be at an advantage in this regard given its superior oxidative capacity (19). To the authors’ knowledge, an extensive multiday study of the impact of prolonged endurance exercise on muscle glycogen metabolism in human subjects remains to be performed.

Skeletal muscle samples obtained via the muscle biopsy technique utilized in this study were comparable in weight to those obtained in a previous study using a similar technique (21). In the majority of dogs, biopsy samples were of satisfactory quality for histochemical analyses. The sled dogs in the current study had a slightly greater number of red fibers (type 1) and a lesser number of white fibers (type 2) than reported from the triceps muscle of German shepherd dogs (28), which could represent inherent breed differences, differences between the muscle groups studied, or the effects of endurance training. Reynolds et al. (23) reported that type 1 fibers comprised nearly 50% of the muscle fiber population in biopsy specimens from the semitendinosus muscle of endurance trained sled dogs.

Serum CK activity increased in all dogs with prolonged submaximal exercise and remained elevated throughout the duration of the 800 km. Elevated serum CK activity has been previously reported in racing sled dogs (10) and may reflect subclinical myonecrosis that occurs during intense, prolonged exertion, even in appropriately trained sled dogs. Serum CK activity did not appear to be associated with clinical signs of rhabdomyolysis or histopathological abnormalities in muscle tissue in any of the dogs.

The results of the current study indicate that profound homeostatic adjustments occur in sled dogs undergoing daily endurance exercise resulting in the preservation and/or replenishment of muscle glycogen. A novel finding that has not been demonstrated in any previous studies that the authors are aware of is that muscle glycogen metabolism appeared to be considerably different on the first day of sustained endurance exercise as compared to subsequent exercise days. The initial 160-km run appeared to prompt metabolic adjustments that increased reliance on noncarbohydrate substrates during subsequent exercise bouts, preserving muscle glycogen stores. These effects may have been complemented by upregulation of local processes involved in muscle glycogen repletion. Future studies will investigate the relative importance of local and systemic mechanisms involved in the regulation of muscle glycogen depletion and replenishment in sled dogs during sustained exercise.

Funded by the Defense Advanced Research Projects Agency (DARPA). Approved for public release, distribution unlimited.The technical assistance of Rick Swenson, Kelly Williams, and Mark Nordman is gratefully acknowledged, and we greatly appreciate the assistance provided by Mark Payton with the statistical analyses.

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Keywords:

FAT; CARBOHYDRATE; CANINE; MUSCLE BIOPSY

©2005The American College of Sports Medicine