Physical Performance and Metabolic Recovery

Physiology and Biochemistry

317

Physical Performance and Metabolic Recovery Among Lean, Healthy Men Following a Prolonged Energy Deficit 8.C. Nindl. K. E. Friedl, F! N. Frykman, 1.1. Marchitelli, R. L. Shippee, 1. E Patton

8.C. Nindl K. E. Ftiedl. I? N. Frykman, LJ.Marchitelli, R. L Shippee,J. I? Parron, Physical Performance and Metabolic Recovery

Introduction

Among Lean, Healthy Men Following a Prolonged Energy Deficit, Int. J. Sports Med.. Vol. 18, pp. 317 -324.1997.

The Minnesota Starvation Study was one of the first concerted efforts to examine recovery from severe weight loss. Dr. Ancel I 0.05). the marginal difference in ability to elevate the body from the ground can most likely be attributed to the large gain in fat mass (Table 2 and Fig. 3). Fig. 4 illustrates the relationship between percent change in fat-free mass and percent change in maximal lift capacity (Fig. 4A), explosive power (Fig.4 B) and vertical jump (Fig. 4 C) for the individual data points from pre to recovery. It can be observed that this relationship is an individual characteristic and that for some subjects physical performance measures had not yet returned to normal at a time when their fat-free mass had already recovered. In addition, for other individuals who had not yet fully regained their pre value for fat-free mass. a greater percentage of their physical performance had yet to be recovered.

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< 10%.Hormonal markers were measured using commercially available radioimmunoassay kits: insulin-like growth factor (IGF-I) (Allegro. Nichols Institute Diagnostics, San Juan Capistrano, CA), triiodothyronine (T3) and thyroxine (T4) (ICN Biomedical~Inc., Costa Mesa, CA), thyroid binding globulin (TGB) (Nichols Institute Diagnostics), thyroid-stimulating hormone (TSH) (3rd generation immunoassay with a limit of detection of 0.04 mlU/L. Allegro HS-TSH, Nichols lnstitute Diagnostics), luteinizing hormone (LH) (ICN Biomedicals Inc.). sex hormone binding globulin (SHBG) (Farmos Diagnostica. Oulunsalo. Finland), and testosterone (Diagnostic Products Corp.. Los Angeles, CA).

Int.]. Sports Med. 18 (1997)

R. 1. Shippee,J. E


u IGF-1

'

FINAL

4dlTIAL

I

RECOVERY

I

W

"

T3

TBG

T4

FINAL

RECOVERY

~FINAL ~

RECOVERY

TSH

Fig.1 a and b Percent of baseline values for testosterone (Test), luteinizing hormone (LH). sex hormone binding globulin (SHBG), and insulin-like growth factor 1 (IGF-1) and triiodothyronine (T3), thyroxine (T4). thyroid binding globulin (TBG) and thyroid-stimulating hormone (TSH) pre. post, and recovery timepoints. 'denotes statistical significance from baseline (p < 0.05).

3

k

~

~

I

~

Fiq,3a,b and c Individual values for strength (3a), power (3b), and vertical jump (3c) for pre. post, and recovery timepoints.

Table 2 Relative body composition and physical performance changes (mean [range]). Variable L .

INITIAL

FINAL

RECOVERY

Fig. 2 Pre, post and recovery values for body mass, fat-free mass (FFM), and fat mass (FM).

% Change from % Change from Post to Recovery Pre to Recovery

- 11.3 (- 8.1 to - 14.3) - 6.6 (- 2.6 to - 8.8) -42.6 (- 22.5 to - 63.4)

20.8 (1 1.4 to 30.2) 8.8 (2.8 t o 15.9) 190.3 (81.4 t o 337.4)

7.1 (- 2.1 to 15.3) 1.6 (- 3.4 t o 8.3) 61.7 (2.4 to 138.5)

27.9 (1 1.8 to 45.5) 29.5 (24.8 to 37.7) 16.5 (2.9 to 26.8)

- 0.30 (- 6.7 to 6.7) - 5.4 (- 1.3 t o 13.2) 0.42 (- 17.4 t o 9.7)

Body Composition Body Mass

From Fig.l it can be seen that most of the hormones returned to pre levels. T3 and IGF-1 increased to greater than pre levels (p < 0.05) in response to the high rate of overfeeding/repletion that occurred during the recovery period. These changes most likely reflect high anabolic activity including protein synthesis, mitotic cell growth, and substrate fluxing. At 5 weeks of recovery, all hormones were within the normal range. With the exception of lactate, all metabolic markers had returned to pre values or were in the normal range (Table 3). Transferrin and glycerol did not differ (p > 0.05) at any time period. Lactate values were similar at the pre and post timepoints, but showed a significant rise (12 mmol/L) in recovery.

% Change from Pre to Final

Fat-free Mass Fat Mass Physical Performance

-

21.2 Maximal Lift Capacity (- 10.5 to - 26.7) Explosive Power - 22.3 (- 13.0 to - 31.7) VerticaIJump - 17.5 (- 2.5 t o - 29.9)


SHBG

Int. 1. Sports Med. 18 (1997)

Physical Performance and Metabolic Recovery

Table 3 Pre, post. and recovery values (means+SD) for metabolic markers. Metabolic Markers

Pre

Post

Transferrin (pmol/L)

37.8? 3.0a 1.9 f O.ga 26.8*4.Oa 90.3k 21 .ga 0.4 f O.Za

3 6 . 7 f 2.3' 3.6k l.Zb 21.3f 2.7b 131.1 f 45.2a 0 . 9 f 0.3b

37.6f2.8' 1.1 +0.6( 26.8+2.ga 132*46.0a 0.1 + 0 . l C

High Density Lipoproteins (rnrnol/L)

1.2 f 0.4a

2 . 3 f O.sb

1 . 2 f 0.2'

Lactate (rnmol/L)

2.4 f 0.7'

2.6+0.5d

4.7+0.7b

Ferritin (prnol/L) Prealbumin (mg/dL) Glycerol (kmol/L)

s -el

-B

-6

-4

-2

I 0

2

4

6

% Change in Fat-free Mass

8

Nonesterfied Fatty Acids (mmol/L)

I

Recovery

.,a

-8

-4 -2 0 2 4 6 % Change in Fat-free Mass

-6

lying solely on monitoring tissue mass to assess malnutrition in an energy deficit state or to assess recovery after intervention. This conclusion has been reached by others advocating the use of muscle function testing to more accurately assess malnutrition (17,36,37,38),

8

As a consequence of these physiological changes. physical per-

-8

-6 -1 -2 '0 2 4 6 % Change In Fat-free Mass

8

I

Fig.4a. 4 b and 4 c The relationship between percent change in fat-free mass and percent change in maximal lift capacity (4a). explosive power (4b). and vertical jump ( 4 c ) for individual data points from pre to recovery.

Dietary in take Energy intake after Ranger school was approximately 68% higher than before Ranger school (4488 812 vs. 2664 k 536 calories). Fat intake as a proportion of the caloric intake increased (30%vs. 35%,pre- and post-Ranger Course).

+

Discussion

The recovery from this catabolic state was more rapid than described in previous studies with somewhat similar levels of catabolism (24,2526). The accretion of fat mass occurred more rapidly than fat-free mass, and both of these appear to recover more rapidly than physical performance. While the relationship between the degree of fat-free mass recovery and physical performance recovery exhibits individual variation (6),our data suggest that caution should be exercised when re-

formance was also hampered at the conclusion of the course. Decrements in performance due to weight loss have been reported previously (16.21,26,30.31,34). Five weeks post-Ranger training all physiological, morphological, and physical performance measures were restored or had rebounded over pre values. Elevated lactate values in recovery were the only measure considered to be outside the "normal range". These restorations were primarily due to food intake. Subjects ate ad libitum after the Ranger Course, and the dietary recall data revealed that food intake was approximately 68%greater in recovery than before Ranger training. Interviews also revealed that the eating habits after the course were characterized by overconsumption of all foods, but especially "cravings" for fatty foods from fast food restaurants and foods tasting "sweet" (39). The reduced physical activity by subjects after Ranger training was associated with feelings of fatigue, diarrhea, sleep irregularities and loss of motivation. These effects could be linked to the elevated lactate values in recovery. Acidosis has been related to carbohydrate rnalabsorption. Ad tibitum oral feeding has been shown to be the critical factor that results in clinical D-lactic acidosis (23). The lethargy reported by the subjects in recovery warrants further investigation and makes it unlikely that improvements in physical performance during recovery are the result of exercise or training (39). Our findings differ from the Minnesota Starvation Study. which demonstrated that muscle function and body mass had yet to be restored 12 weeks after semi-starvation (24,25). The present study also differs from the Minnesota Starvation Study in that our subjects lost body mass at a faster rate. It should be noted that subjects in that study lost -25%of body mass over a 24-week period and were subjected to controlled refeeding after semi-starvation (compared to a 11.5%loss of body mass over an 8-week period and ad libitum feeding in recovery for the present study). In an earlier Ranger study (10,11.31), one Ranger lost 23%of his body mass in 8 weeks (almost meeting the Minnesota Starvation Study's goal for 24 weeks).


Different letters denote statistical significance (p 3000 kcallday (This caloric intake is higher than the average soldier in a non-training environment). The primary cause of the energy deficit was the very high energy expenditure. The daily energy expenditure from U. S. Army Ranger training (-4200 kcallday) (18) is higher than that estimated for unmechanized farm labor (-3500 kcal/day) (40). but lower than that previously reported for Norwegian and French military training (between 5000 and 8000kcal/day over -5 days) (1,13.34). This resulting energy deficit from the Ranger Course induced catabolism reflected by declines in testosterone, T3.T4, and IGF-I and substantial losses of body mass, fat-free mass, and fat mass. These changes are normal starvation-like responses and represent adaptive changes to an energy deficit that are in agreement with previous reports (1.10.12.13,14,22,26, 31,32,33,39). While we were not concerned with aerobic capacity in this study, the Minnesota Starvation Study and others demonstrated that aerobic capacity recovers at a slower rate than did muscular strength (2,24.25). An earlier Ranger study which did examine aerobic capacity found it to be still depressed 3 days after training (20). To our knowledge no previous studies have reported the recovery of physical performance emphasizing strength/power after a period of extended weight loss similar to Ranger training. LeBlanc et al. (29) reported that after 17 weeks of bed rest in which there was an 1.8-kg increase in body mass and differential effects on isokinetic strength (peak torque showed greater declines at 60 degreeslsec than at 120 or 180 degreeslsec), recovery of muscle strength was also rapid and complete. Studies involving short-term weight loss (--5%) have reported no decrement in anaerobic or power measures (6,7,27). Other studies following recovery from weight loss of a magnitude similar to the loss experienced in the present study have shown muscle function (i.e., altered force-frequency curve, slower relaxation rate, low frequency fatigue) of the adductor pollicis to be restored in refeeding (37). The present performance recovery findings that are more functional in nature offer obvious advantages over previous studies whether applied to real world athletic or military performance. As discussed previously, the impairment in physical perform-

ance while closely associated with losses of fat-free mass are also affected by metabolic and neural factors. Likewise, the improvements of physical performance in recovery involves other factors than the repletion of fat-free mass. In recovery. neural factors do not seem to be a limiting factor. as speed and coordination have been shown to be rapidly restored (24, 25). In 5 weeks of recovery, most individuals in the present study had regained a greater percentage of their fat-free mass than their strength, power, or vertical jump height. Correlational analyses did not reveal any associations between the return of body composition variables and the physical performance measures in recovery. These resuIts could partially be explained by the small sample size, but a more probable explanation is that improvements in physical performance during recovery are more dependent on the increase in intracellular electrolytes (potassium and calcium), acid-base balance, and water than on nitrogen accretion (36,37,38). During recovery.

C. Nindl. K. E. Friedl, P N. Frykmon. 1.1. Morchitelli, R. L. Shippee.]. E

Potton

anabolic growth factors (i.e.. testosterone, IGF-I, and T3) may first promote restoration in quantitative aspects of muscle and then sustain qualitative aspects such as expression of myosin heavy chain isoforms resulting in improved maximal shortening velocity and increased power capability of muscle (3). These anabolic hormones appear to be more sensitive to the effects of semi-starvation and refeeding than several of the other metabolic markers measured in this study-Transferrin, although commonly used as an indicatorof nutritional status, did not demonstrate any significant changes throughout the study, and prealbumin experienced smaller relative changes than IGF-1, testosterone, and T3.This suggests that serum concentrations of selected hormones can be sensitive detectors of nutritional status (5). The finding that fat mass recovered at an accelerated rate when compared to the other measures is in agreement with the Minnesota Stamation Study (24.25). This finding raised important questions concerning the composition of tissue repletion after substantial weight loss (6). The mechanism for this "rebound fatness" may involve other factors in addition to overeating. In fact, during the refeeding phase of Minnesota Starvation Study in which experimental groups received fewer calories in recovery than pre-starvation levels, the same trend was seen for an undue proportion of weight gain as fat mass. A contributing factor to this greater proportional gain in fat mass may be a depressed resting metabolic rate (RMR) that endures even during recovery. RMR has been shown to remain depressed for up to 8 weeks after a massive weight loss among obese females (16). The Minnesota Starvation Study showed that RMR normalized per square meter of body surface area had not recovered among lean men even after 6 weeks of refeeding (24). A rise in T3 and T4 during refeeding was observed for this study, but RMR recovery probably takes a longer period of time. At least part of this may be related to down regulation of T3 receptors (22). Self-reports of dietary intake were characterized by a somewhat larger percentage of calories obtained from fats in the recovery period than prior to Ranger training. Studies have shown that overfeeding with fat leads to a smaller increase in energy expenditure than does overfeeding with carbohydrate (19). Presumably, the transfer of dietary fat to adipose tissue is a less energy consuming process than the synthesis of adipose tissue from carbohydrate. The self-reported hyperphagia is also indicative of an insatiable "gorging" pattern of consumption. This gorging pattern of eating allows adipose tissue to become more sensitive to the lipogenic effects of insulin. In addition, an enhanced "feeding efficiencyw.associated with increased lipoprotein lipase activity, has been shown to be independent of food intake during refeeding (28). Cleary et al. (4) suggested that plasma triglycerides are "preferentially" pulled into adipose tissue rather than skeletal muscle. This finding could help explain the accelerated accretion of fat mass when compared to fat-free mass. Subsequent to a rebound in weight and fat gain, both an earlier ranger study and the Minnesota Starvation Study have shown that much later in recovery, body composition eventually returns to baseline levels (25.31). In summary, in the context of a large energy surplus, all of the above mentioned factors, depressed RMR during recovery. increased caloric contribution from fats, increased sensitivity to insulin, increased lipoprotein lipase activity. and a gorging pattern of eating, leads to a propensity to weight gain and, most notable, fat mass gain.



Physical Performance and Metabolic Recovery

Acknowledgement We gratefully acknowledge the assistance of Ms. Elaine Christensen, Ms. Joanne Arsenault, Ms. Deborah Jezior, and the Ranger cadre at 4th Ranger Training Battalion, Fort Benning. GA, where these studies were conducted. We are indebted to the volunteers from Ranger Class 11 -92 whose participation made this study possible. The views, opinions, and/or findings in this report are those of the authors, and should not be construed as an official Department of the Army position, policy or decision. unless s o designated by other official documentation. Human subjects participated in these studies after giving their free and informed voluntary consent. Investigators adhered to AR 70- 25 and USAMRMC Regulation 70-25 o n the Use ofVolunteers in Research. References Aakvaag, A., Sand,T., Opstad, P. K., Fornum. F.: Hormonal changes in young men during prolonged physical strain. EurJAppl Physiol 39: 283 -291,1978. Barac-Nieto, M., Spurr, C., Dahners, H. W., Maksud. M. G.: Aerobic work capacity and endurance during nutritional repletion of severely undernourished men. Am)Clin Nutr33: 2268- 2275.1980. Caiozzo, V. J., Herrick, R E., Baldwin, K. M.: Response ofslow and fast muscle to hypothyroidism: maximal shortening velocity and myosin isoforms.JAppl Physiol263: C86 -C94,1992. Cleary. M. P.,Vasselli, J. R., Greenwood. M. R. C.: Development of obesity in Zucker obese (fafa) rats in absence of hyperphagia.J N ~ t 113: r 1150- 1156.1983. Donahue. 5. P.. Phillips, L S.: Response of IGF-1 to nutritional support in malnourished hospital patients: a possible indicator of short-term changes in nutritional status. Am ] Clin Nutr 50: 962 - 969,1989. Dullo, A. C., Jacquet, J., Girardier. L: Autoregulation of body composition during weight recovery in human: the Minnesota Experiment revisited. I n t j Obes 20: 393 -405.1996. Fogelholm. C. M.: EfFeas of bodyweight reduction on sports performance. Sports Med 18: 249-267.1994. Fogelholm, G. M.. Koskinen, R., Laakso,J., Rankinen.T.. Ruokonen. I.: Gradual and rapid weight loss: effects of nutrition and performance in male athletes. Med Sci Sports Exerc 25: 371 -377, 1993. Friedl, K. E., DeLuca. 1. P.. Marchitelli, L. J.. Vogel. J. A: Reliability of body-fat estimations from a four-compartment model using density, body water. and bone-mineral measurements. Am J Clin Num 55: 764-770,1992.

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