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The Journal of Clinical Endocrinology & Metabolism Vol. 89, No. 7 3377-3384
Copyright © 2004 by The Endocrine Society

Lipid Profile Disorders Induced by Long-Term Cessation of Physical Activity in Previously Highly Endurance-Trained Subjects

Cyril Petibois, André Cassaigne, Henri Gin and Gérard Déléris

University of Bordeaux 2; Institut National de la Santé et de la Recherche Médicale, Unité 577, Bio-Organic Chemistry Group (C.P., G.D.); and Faculty of Sport Sciences and Physical Education (C.P.); Department of Medicinal Biochemistry and Molecular Biology, Laboratory of Biochemistry (A.C.), and Department of Nutrition-Diabetology, Hospital of Haut-Levèque (H.G.); Bordeaux Centre Hospitalier Universitaire, 33076 Bordeaux, France

Address all correspondence and requests for reprints to: Dr. Cyril Petibois, Université Victor Segalen Bordeaux 2, Institut National de la Santé et de la Recherche Médicale, Unité 577, Groupe de Chimie Bio-Organique, 146 rue Léo Saignat, 33076 Bordeaux, France. E-mail: cyril.petibois{at}bioorga.u-bordeaux2.fr.


   Abstract
Top
 Abstract
Introduction
 Subjects and Methods
 Results
 Discussion
 References
 
The objective of this study was to describe long-term detraining effects on lipid profile in previously highly endurance-trained athletes. The study design was longitudinal, with a 2-yr follow-up study of changes in lipid profile during hard training and detraining. Ten subjects trained for 2 yr (22 h/wk; two 47-wk training periods with a 5-wk recovery period), and the 10 others stopped training after wk 47. Main blood lipid profile parameters, energy intake, and body composition were measured at baseline (wk 1) and at wk 24, 47, 52, 76, and 99. Although food caloric intake was reduced (2411 ± 256 vs. 5697 ± 455 kcal/d, detraining vs. training), detraining induced a decrease in high density lipoprotein cholesterol and increases in fat mass (by 6.5 ± 1.1 kg), body mass index, leptin, low density lipoprotein cholesterol, low density lipoprotein/high density lipoprotein ratio, and apolipoprotein B, although insulin resistance (determined by homeostasis model assessment) stabilization had previously occurred. Further disorders appeared in triglycerides (TG) metabolism during detraining, with a persistent increase in TG (from 1.0 ± 0.3 to 1.4 ± 0.3 mmol/liter), whereas glycerol decreased (from 88 ± 9 to 73 ± 8 µmol/liter), and very low density lipoprotein-TG, chylomicrons, and apolipoprotein C3 remained stable. Plasma lipoprotein lipase activity decreased whereas hepatic lipase activity remained stable. As well as a rapid loss of endurance-training benefits for the cholesterolemic profile, detraining also induced disorders in TG metabolism, possibly as a result of the elevated TG turnover acquired with long-term hard training.


   Introduction
Top
 Abstract
 Introduction
Subjects and Methods
 Results
 Discussion
 References
 
IT IS WELL accepted that endurance physical activity is good for health and favorably prevents most metabolic disorders, such as obesity, type 2 diabetes, and atherosclerosis (1). However, to date little attention has been given to detraining effects on such benefits. The main metabolic benefits of regular physical activity are a rise in high density lipoprotein cholesterol (HDL-C) levels, a lowering of triglycerides (TG) and low density lipoprotein cholesterol (LDL-C) levels, and higher insulin sensitivity to fasting glucose. In addition, exercise training increases plasma clearance of postprandial lipoproteins, such as chylomicrons (2). Chylomicrons transport dietary lipids from the intestine into the systemic venous system. During their circulation, chylomicrons are rapidly depleted of dietary TG by the catalytic action of plasma lipoprotein lipase (Pl-LPL). Favorable effects have been found for endurance training on both LPL activity and TG-rich lipoprotein turnover (1). Pl-LPL activity is higher in aerobically fit individuals, suggesting higher dietary TG turnover and metabolism (2). A schematic view of endurance-training effects on the regulation of LPL activities within compartments of the human body is that increased muscle LPL mass after exercise may replenish intramyofibral stores of TG, which are depleted with endurance exercise, and these stores are greater in trained individuals. The postexercise increase in muscle LPL mass coincides with the postexercise acute fall in circulating TG typically observed in subjects regularly performing endurance exercise. Thus, the low fasting TG levels often seen in highly trained individuals are due in part to their high levels of muscle LPL activity, producing subsequent fatty acid oxidation (3).

Endurance exercise also increases fat oxidation, enhances dietary TG turnover, and increases HDL-C concentrations (4). However, several studies found that after the acute metabolic effects of exercise, i.e. 60 h after the last training session, there was no further effect of training on postprandial lipidemia, insulin sensitivity, and Pl-LPL activity (5). Therefore, frequent exercise is needed to maintain metabolic benefits of endurance training (6). Metabolic effects of training and detraining have been studied in obese (7), sedentary (8), lean (9, 10), and aerobically fit subjects (11). Several studies revealed that beneficial outcomes of regular physical activity were diminished or disappeared after a few weeks or months (5, 9). Several parameters of lipid metabolism appeared strongly dependent on the training level of athletes, namely leptin concentration (12), fatty acid oxidation level (3, 13), LPL activity (14), and lipoprotein levels and contents (4). However, the metabolic consequences of several years of hard endurance training (>10 yr and >20 h/wk) on lipid profile during detraining, i.e. when elite athletes definitively stop their sports careers, have not been extensively investigated. Due to metabolic disorders such as insulin resistance and lipoprotein redistribution, sedentary, aerobically fit subjects who stop physical activity for several months regain the body fat mass they maintained a a persistently low level during training (15) despite a reduction of energy intake and the percentage of calories from dietary fat (16). Although not yet demonstrated, this suggests that highly endurance-trained subjects experience more profound metabolic disorders than only regaining fat after cessation of physical activity.

The aim of this study was to monitor changes in the lipid profile of highly endurance-trained subjects during training and detraining. Ten of 20 athletes with long term endurance-training experience (>10 yr) were studied before and after they choose to definitively stop their sports careers.


   Subjects and Methods
Top
 Abstract
 Introduction
 Subjects and Methods
Results
 Discussion
 References
 
Experimental subjects

Twenty endurance-trained rowers (age, 28 ± 2 yr; range, 25–33 yr) participated in this study. All subjects were recruited because they had endurance-training experience of at least 10 yr, with a minimal training activity of eight training sessions per wk (>15 h) for 45 wk/yr. All subjects had been weight stable (±2 kg) for at least 6 months before the study. No subject had evidence of cardiovascular disease, diabetes (fasting glucose, >7 mmol/liter), hypertension (blood pressue, >160/90 mm Hg), or hyperlipidemia (TG, >1.8 mmol/liter; cholesterol/HDL-C, >5). Subjects were separated into two groups. Subjects who continued training (trained; n = 10) trained 47 wk/yr for 2 yr. The 2 training yr were interspaced by a 5-wk recovery period without regular physical activity (off-season). Subjects who stopped training (detrained; n = 10) trained only the first year. They were selected for the study because they had previously decided to definitively stop their sports careers after a last sports season. Detrained subjects were instructed to reduce physical activity to less than 4 h/wk. All subjects were informed about the possible risks involved in the experiments before their voluntary written consent was obtained. The study was approved by the ethical committee of University Hospital Group of Bordeaux.

Training

Subjects trained together during the study for 11 sessions, 2 h/wk. Seventy percent of training sessions included rowing exercises, and the other 30% included endurance weight-lifting. Rowing exercises were endurance exercises, as 80–85% were performed at intensities between 60–75% of maximal oxygen consumption (VO2max). An incremental test to exhaustion was performed the day after blood sampling on a rowing ergometer (Concept II, Morrisville, NJ; rowing velocity starting at 3.0 m/s, with a 0.33 m/s increment every minute) to determine VO2max. VO2 and CO2 volume (VCO2) were determined continuously during the test (Vmax; Sensor Medics, Paris, France), and the respiratory exchange ratio (RER: VCO2/VO2) was calculated. Attainment of VO2max was considered exhaustion. Weight-lifting exercises were performed at intensities between 60–80% of maximal power output. The annual training program was the same for the 2 yr of the study.

Diet

To avoid the confounding effects of differences in diet among the subjects, they were counseled by a dietitian with the objective to reach defined proportions of carbohydrates, lipids, and proteins (carbohydrate, ~55%; fat, ~25%; protein, ~20%) for at least 4 wk before the study. Compliance was controlled by analysis of 7-d food records at the onset of every 2 months during the study. Nutrient intake was controlled for at least 4 d before metabolic testing by providing each subject a weight-maintaining diet. Caloric intake was estimated by the recording of daily food intake and by calculating calories using food exchange lists and food composition tables.

Sampling and analyses

Venous blood samples were taken from the right arm after a 12-h overnight fast. Blood samples were drawn by antecubital venipuncture of the right arm using a Teflon catheter. Blood taken for Fourier-transformed infrared spectrometry measurements (17) was drawn in gel-barrier collection tubes (6 ml; Vacutainer, BD Biosciences, Franklin Lakes, NJ) and immediately centrifuged for 10 min at 4000 x g. Serum was then collected in other tubes and stored at –20 C before analysis. Serum concentrations of glucose, lactate, TG, glycerol, free fatty acids, cholesterol, apolipoprotein A1 (Apo-A1), Apo-B, and Apo-C3 were determined by Fourier-transformed infrared spectrometry according to methods previously described (17, 18, 19). For quantitation of LPL activity, a methodology described previously was used (20). Study participants were injected in the postabsorptive state with 100 IU heparin (Novo, Copenhagen, Denmark)/kg body weight so as to release LPL and hepatic lipase (HL) into the circulation. Postheparin plasma was collected 10 min after the heparin injection. Lipases were then selectively measured using an immunological method. Activity is expressed in units, corresponding to 1 µmol fatty acids released/min (20, 21, 22, 23). Plasma insulin was determined by monoclonal immunoradiometric assay (CIS Bio International, Gif sur Yvette, France). The index of insulin resistance was calculated on the basis of fasting values of glucose and insulin [fasting insulin x (fasting glucose/22.5)], according to the homeostasis assessment method (24). Serum chylomicrons were isolated before density gradient ultracentrifugation of other lipoprotein classes according to the method of Terpstra (25). Very low density lipoprotein (VLDL) was separated from serum by centrifugation (18 h, 105,000 x g) at a density of 1.006 g/ml. After removing VLDL, LDL was precipitated from the supernatant (HDL and LDL) with dextran sulfate 500,000-magnesium chloride (26). Lipoprotein cholesterol and TG contents were determined enzymatically on an autoanalyzer (Cobas Mira, Roche, Basel, Switzerland). The plasma leptin concentration was determined using an RIA kit (Linco Research, Inc., St. Charles, MO). Height was measured at the onset of each training year. Body weight and fat mass were measured using a bioelectrical impedance apparatus (BodyMaster, Calor-Tefal, France). Body mass index (BMI) was calculated as weight in kilograms divided by height in meters squared. All analyses were performed at Department of Medicinal Biochemistry and Molecular Biology, Laboratory of Biochemistry, Bordeaux University Hospital, and calibration standards were systematically used for quality control of procedures.

Statistics

Data are expressed as the mean ± SD. Repeated measures ANOVA within and between groups were performed to determine the significance of changes over time and between trained and detrained subjects. Significance was assessed at a value of P < 0.05. All statistics were performed using the Statistica 5.0 software package (StatSoft, Maisons-Alfort, France).


   Results
Top
 Abstract
 Introduction
 Subjects and Methods
 Results
Discussion
 References
 
Training

The total annual training time was 1,046 h the first year, with 74% of the time spent in rowing sessions (774 h) and 26% spent in endurance weight-lifting. Subjects performed 12,350 rowing km at a mean intensity of 71% VO2max. (VO2max, 74 ± 5 ml O2·kg/min at wk 47). Resting VO2 at baseline and after 47 wk were 4.7 ± 1.1 and 5.1 ± 0.9 ml O2·kg/min, and RER (VCO2/VO2) were 0.76 ± 0.06 and 0.73 ± 0.07. Only RER measurements showed a significant difference between baseline and the 47th training wk (P = 0.03). There was no difference between trained and detrained subjects in training contents, resting RER and VO2, and VO2max. During the second year, trained subjects exercised 1,051 h, with 73% of the time spent in rowing sessions (768 h) and 27% of the time spent in endurance weight-lifting (283 h). They performed 12,310 rowing km at a mean intensity of 70% of VO2max (VO2max, 75 ± 6 ml O2·kg/min at wk 99). Resting VO2 at wk 52 and 99 were 4.9 ± 1.0 ml O2·kg/min (RER, 0.75 ± 0.07) and 5.0 ± 0.6 ml O2·kg/min–1 (RER, 0.73 ± 0.05). For the same year, detrained subjects reported no week with physical activity for more than 4 h (VO2max, 58 ± 6 ml O2·kg/min at wk 99; P = 0.001 with trained subjects). Physical activity was 1.1 ± 0.4 h/wk (range, 0–2 h/wk). Resting VO2 at wk 52 and 99 were 5.1 ± 1.1 ml O2·kg/mMin (RER, 0.75 ± 0.06) and 5.6 ± 0.6 ml O2·kg/min (RER, 0.79 ± 0.05). Differences were found for trained subjects at wk 76 and 99 (P = 0.05 and P = 0.05 for VO2; P = 0.04 and P = 0.03 for RER, respectively).

Anthropometrical parameters

Height (189 ± 8 cm; range, 179–197 cm) did not change for any subject during the 2 yr of the study (Table 1Go). Weight and BMI decreased significantly from wk 1 to 24 (n = 20; P = 0.011), and no difference was found between trained and detrained subjects during the first year (P = 0.47). Cessation of physical activity between wk 47 and 52 induced a significant increase in weight, BMI, and fat mass (n = 20; P < 0.05 for both), whereas lean body mass decreased (n = 20; P < 0.05 for both). Furthermore, detrained subjects increased their fat mass from 10.5 ± 1.6 to 17.3 ± 1.3 kg, i.e. from 12.8 ± 1.7 to 20.2 ± 1.4% of total body weight. BMI increased up to 24.8 ± 1.7 kg/m2 at the end of the study, whereas lean body mass decreased after 29 wk of detraining (P = 0.04; wk 47 vs. 99).


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  		TABLE 1. Anthropometrical parameters with training and detraining

 
Diet

Seven-day food records at the onset of the study revealed no difference between trained and detrained subjects, with estimated proportions for carbohydrates, lipids, and proteins of approximately 54% carbohydrates, 24% lipids, and 22% protein. During the first training year, all subjects were active in training, and proportions remained stable with approximately 55% carbohydrates, 23% lipids, and 22% protein, on the average. Caloric intake was 5697 ± 455 kcal/d. During the second year, approximate proportions of carbohydrates, lipids, and proteins as well as food caloric intake remained stable for subjects who continued training (~54% carbohydrates, 23% lipids, and 23% protein and 5504 ± 379 kcal/d), and no significant difference was found compared with records for the first training year. For subjects who stopped training, approximate proportions of carbohydrates, lipids, and proteins remained globally stable (~53% carbohydrates, 24% lipids, and 22% protein), but food caloric intake was significantly diminished (2511 ± 256 kcal/d).

Lipid profile during the first training year

After 24 training wk, significant decreases were found for TG (P = 0.014) and insulin resistance (determined by the homeostasis model assessment; P = 0.019), whereas only the glycerol concentration increased (P = 0.019; Table 2Go). These evolutions were much more marked at wk 47. Total cholesterol (TC) decreased after 24 wk (P = 0.027) and remained stable thereafter. In contrast, LDL-C decreased at wk 47 (P = 0.031; Table 2Go) concomitant to an increase in HDL-C (P = 0.021). The LDL/HDL ratio decreased significantly with training (P = 0.031 and P = 0.016, wk 1 vs. 24 and 47, respectively). The chylomicron blood content increased significantly during the second part of the year (wk 24 vs. 47, P = 0.031). The leptin concentration decreased significantly after 24 wk (P = 0.004) and remained globally stable thereafter (Table 3Go). No significant change was found for Apo-A1, whereas Apo-B decreased after 24 wk (P = 0.017) and 47 wk (P = 0.021). Inversely, Apo-C3 increased slightly, but significantly, after 24 wk (P = 0.041) and 47 wk (P = 0.039). Increases were also found in Pl-LPL activity after 24 wk (P = 0.022) and 47 wk (P = 0.027), whereas HL decreased after 47 wk (P = 0.044).


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  		TABLE 2. Energetic and lipoproteic parameters during the first training year

 

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  		TABLE 3. Apolipoprotein and enzymatic parameters during the first training year

 
Training vs. detraining: evolution of lipid profile during the second year

Metabolic parameters (Table 4Go). No significant difference was found between groups at wk 52, and results were in accordance with those obtained from wk 1 (P > 0.05 for all data; n = 20). As observed during the first training year, the TG concentration decreased in trained subjects (P = 0.019, wk 52 vs. 99; n = 10). Inversely, TG increased significantly in detrained subjects (P = 0.006, wk 52 vs. 99; n = 10), with a 49% concentration increase on the average. Significant differences were found between groups at wk 76 and 99 (P = 0.027 and P = 0.011, respectively). The same pattern of changes was observed for TC concentration and insulin resistance, but insulin resistance remained stable after 29 wk of detraining. Significant differences were found between groups at wk 76 and 99 (TC: P = 0.013 and P = 0.007, respectively; insulin resistance: P = 0.041 and P = 0.016, respectively). Inversely, the glycerol concentration increased in trained subjects (P = 0.029 and P = 0.016 at wk 76 and 99), whereas it decreased in detrained subjects (P = 0.031 and P = 0.022 at wk 76 and 99). Thus, significant differences were found between groups at wk 76 and 99 (P = 0.027 and P = 0.008, respectively). Positive relationships were found between the evolution of insulin resistance and that of TG (P = 0.031) and cholesterol (P = 0.044) concentrations during the first part of the detraining period (wk 47–76), but a negative relationship was found with glycerol (P = 0.021) at the same time. No significant relationship was found thereafter.


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  		TABLE 4. Energetic parameters during the second training year

 
Lipoproteins (Table 5Go). No significant difference was found between groups at wk 52, and results were in accordance with those obtained at wk 1 (P > 0.05 for both). The same pattern of concentration changes as those during the first training year was observed for trained subjects, i.e. significant decreases in LDL-C (P = 0.012 on wk 99) and in the LDL/HDL ratio (P = 0.022 and 0.019 for wk 76 and 99), and increases in HDL-C, VLDL-TG, and chylomicrons (P < 0.05 for all data from wk 99). For detrained subjects, LDL-C increased by approximately 13% between wk 52 and 99 (P = 0.015), whereas HDL-C decreased by 19% at the same time (P = 0.006). As a consequence, the LDL/HDL ratio increased significantly (P = 0.02 and 0.011 at wk 76 and 99). Significant differences were found between groups at wk 76 and 99 (P < 0.01 for both). On the other hand, plasma VLDL-TG remained unchanged for detrained subjects, whereas it increased for trained subjects (P = 0.021). Thus, a significant difference was found between groups, but only at wk 99 (P = 0.017). The same pattern of changes and differences from trained subjects was observed for chylomicrons (P = 0.024 at wk 99). Moreover, at wk 52, 76, and 99, positive relationships were found between fat mass increase and chylomicron blood contents (P = 0.001, 0.001, and 0.002, respectively) for detrained subjects, i.e. the higher the fat mass increase during detraining, the higher the chylomicron concentration.


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  		TABLE 5. Lipoproteic parameters during the second training year

 
Apo concentrations and enzymatic activities (Table 6Go). For trained subjects, evolution of apolipoproteins and enzymatic parameters during the second training year were comparable to results obtained during the first year (P < 0.05 for all data). In brief, the Apo-A1 concentration remained unchanged, whereas that of Apo-B decreased (P = 0.023 and 0.019 at wk 76 and 99) and that of Apo-C3 increased (P = 0.037 and 0.031 at wk 67 and 99). Pl-LPL activity increased again with training (P = 0.029 and 0.022 at wk 67 and 99), whereas that of HL was decreased at wk 99 (P = 0.047). Leptin concentration decreased again by 50% between wk 52 and 99 (P = 0.008). For detrained subjects, Apo-A1 and Apo-C3 remained stable. However, at wk 52, 76, and 99, positive relationships were found between fat mass increase and Apo-C3 concentration (P = 0.01, P = 0.001, and P = 0.001, respectively), i.e. the higher the fat mass increase during detraining, the higher the Apo-C3 concentration (Fig. 1Go). Apo-B increased significantly (P = 0.031 and P = 0.011 at wk 76 and 99) to reach values about 52% higher than those for trained subjects. Pl-LPL activity decreased by 11% between wk 52 and 99. HL activity increased significantly (P = 0.006), leading to a difference from that in trained subjects (P = 0.004). At wk 52, 76, and 99, inverse relationships were found between changes in fat mass and decrease in HL activity for detrained subjects (P = 0.01, P = 0.001, and P = 0.001, respectively), i.e. the higher the fat mass increase during detraining, the higher the HL activity increase (Fig. 2Go). The leptin concentration increased (P = 0.03) and reached values 68% higher than those in trained subjects at wk 99.


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  		TABLE 6. Apo and enzymatic parameters during the second training year

 


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  		FIG. 1. Relationship between changes in fat mass and Apo-C3 concentration change (difference values) between 47 and 99 wk. Regression line: y = 0.0095x – 0.0785 (r = 0.97; P = 0.001).

 


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  		FIG. 2. Relationship between changes in fat mass and HL activity change (difference values) between 47 and 99 wk. Regression line: y = –1.94x + 67.4 (r = 0.93; P = 0.001).

 

   Discussion
Top
 Abstract
 Introduction
 Subjects and Methods
 Results
 Discussion
References
 
The aim of this study was to monitor lipid profile changes in highly endurance-trained subjects during training and detraining. During training, subjects exercised approximately 4 h/d, and caloric intake was about 5700 kcal/d. Energy expenditure during high intensity endurance exercise usually reaches 13 kcal/min in male subjects (27). Indeed, daily energy expenditure for training was about 3200 kcal/d. During detraining, subjects increased their body fat mass by approximately 70%, i.e. from 12% to 20% of total body mass, and BMI reached about 25 kg/m2. For sedentary men, overweight is defined as a BMI between 25 and 30 kg/m2 with a fat mass greater than 20%. Therefore, detrained subjects had reached the morphological profile of overweight sedentary subjects after 52 wk of detraining (28). However, during detraining, subjects had reduced their caloric intake by 55% compared with that during the training regimen. A regular diet in a normal 70-kg male adult subject is thought to be 2000–2200 kcal/d (i.e. 30 kcal/kg·d), with a mean distribution of 59% carbohydrate, 28% fat, and 13% protein (29). Regarding the weight of our subjects (extremes of 82 and 88 kg on the average during the study) and with a caloric intake of about 2500 kcal/d (53% carbohydrate, 25% fat, and 22% protein), detrained subjects also had a mean caloric intake of approximately 30 kcal/kg·d. Therefore, the fat mass increase we observed in these subjects could not solely be attributed to overfeeding after training cessation. The findings of our study suggest that metabolic disorders may also explain the continuous fat mass gain after training cessation.

Detraining-induced changes in cholesterolemic profile

The first important result of our study was the inverse side-effects of training and detraining on the cholesterolemic profile of highly endurance-trained subjects. Such a rapid inversion of training benefits on lipid profile by detraining had been shown in previous studies (2, 5, 6, 9). Our subjects presented low HDL-C levels at baseline, which increased after training. Such low HDL-C levels have been described with short-term detraining in previously highly endurance-trained subjects, and these levels also decline with age (30). Nevertheless, HDL-C concentrations increase with regular endurance exercise, as was observed for our subjects, and this contributes to a lower risk of coronary heart disease in physically active individuals compared with sedentary subjects. However, training benefits on the cholesterolemic profile are usually acute, as a short-term interruption of training is sufficient to affect lipoproteins (2), notably by increasing Apo-B, LDL-C, and TC blood contents. Indeed, a return to the cholesterolemic profile of healthy sedentary subjects may occur within a few weeks after cessation of physical activity (5, 6). Our results were in accordance with these studies, because 5 wk of detraining (wk 47–52) were sufficient to increase Apo-B, LDL-C, TC, and TG, whereas HDL-C decreased. However, we found that the inversion of training benefits on the cholesterolemic profile lasted longer than a few weeks. The alteration in cholesterolemic profile continued after 52 detraining wk, suggesting chronic alterations in cholesterol synthesis, transport, storage, and metabolism. Furthermore, the LDL/HDL ratio shifted from 3.4 after training to 5.6 with long-term detraining. This LDL/HDL ratio increase is alarming, because combined hypertriglyceridemia, elevated LDL cholesterol, and high LDL/HDL cholesterol ratio (>5) are thought to increase the risk of coronary heart disease risk by 6-fold (31). Therefore, total cessation of physical activity in previously highly trained subjects leads quite rapidly to a cholesterolemic profile that is assumed to have potent cardiovascular risks.

Detraining-induced changes in TG metabolism

Another important finding of our study was the alteration in TG metabolism that persisted over 1 detraining yr and independently of insulin resistance stabilization (after 6–7 months). Apo-C3, VLDL, and chylomicron blood contents did not change with detraining, whereas TG increased, and Pl-LPL activity decreased. These results suggest that the TG transport level remained stable during detraining, whereas TG metabolism decreased. A significant TG concentration increase is usually associated with low levels of HDL and high levels of LDL particles and Apo-C3 (32). Endurance training is associated with a lower TG response after a fatty meal (11) and increased fatty acid turnover (33) and whole body lipolysis (3). These training effects are often associated with persistent low body fat mass, i.e. less than 15%. However, it is difficult to maintain this low fat mass after high intensity endurance training, even if moderate training and controlled caloric intake are consented (15). We observed that training lowered body fat mass in a highly reversible manner, because a few weeks of detraining were sufficient to induce a significant increase in fat (wk 47–52). Most previous studies of regaining of fat mass after hard training showed a rapid fat regain (within a few weeks) before stabilization (34). This rapid fat regain was assumed to be a response to the negative lipid balance the athletes maintained during hard endurance training, i.e. when fatty acid metabolism was highly solicited, and there was limited adipose tissue fat deposition. In turn, once a positive lipid balance was possible, i.e. with detraining, fat stores could be more tightly regulated by leptin, hormone-sensitive lipase, and insulin, leading to greater adipose tissue fat deposition (1, 6). Leptin is associated with satiety, stimulates lipid metabolism, and increases energy expenditure. Leptin is considered a major regulator of energy homeostasis, which may serve to limit excess energy storage. As plasma leptin concentrations are tightly coupled with fat mass in humans, decreases in adipose mass with weight loss coincide with decreased concentrations of circulating leptin (35). During the training condition, leptin levels remain low in athletes as long as fat mass remains low (1, 12). An increase in leptin inhibits adipose tissue hormone-sensitive lipase activity, allowing higher TG peripheral storage and lower fatty acid metabolism (36). A decrease in TG metabolism while body fat increases induces higher carbohydrate oxidation (1). This was suggested by calorimetric data, as higher VO2 and RER values were found in detrained subjects. The leptin concentration increased throughout the detraining period, suggesting decreased lipid metabolism, whereas Pl-LPL and HL activities decreased. Therefore, it can be hypothesized that the low body fat mass of athletes was maintained during the training period by a high fat oxidation level, which stimulated Pl-LPL and HL activities and lowered insulin resistance. Cessation of physical activity inversed this regulation, as fat oxidation was strongly diminished with the lack of endurance training exercises as well as at rest, as shown by resting calorimetric data (VO2 and RER). Furthermore, TG still increased after stabilization of insulin resistance, suggesting that fat mass regain through TG and cholesterol storage is at least partially independent of insulin resistance. Normally, insulin resistance is associated with more lipolysis (37). Therefore, mechanisms other than fat oxidation and fat mass regain might explain the persistence of TG metabolism disorder during detraining in previously highly trained subjects.

Significant relationships were found between an increase in fat mass and Apo-C3 and chylomicron changes as well as an inverse correlation with the decrease in HL activity. Whatever the initial HL activity level (before detraining), the higher the fat mass increase, the higher the HL activity decrease. The presence of chylomicron within fasting plasma is usually the result of hypertriglyceridemia, which was not observed in these subjects (TG, ~1.0 mM). Thus, these apparent chylomicrons could be large VLDL particles containing large amounts of TG. Nevertheless, Apo-C3 plays a central role in controlling the plasma metabolism of TG-rich lipoproteins (VLDL and chylomicrons). A persistently elevated blood concentration of Apo-C3 is thought to contribute to hypertriglyceridemia by releasing TG to peripheral tissues and lowering Pl-LPL activity, which is also favorable to the storage of TG. Elevated serum TG is commonly associated with insulin resistance and represents a valuable clinical marker of the metabolic syndrome. The metabolic syndrome is globally characterized by atherogenic dyslipidemia (elevated TG, increased small dense LDL, and decreased HDL), insulin resistance, obesity, and possibly hypertension (38). However, it is likely that detrained subjects do not experience this metabolic syndrome because stabilization of insulin resistance occurred before ending the fat mass increase, and there was parallel stabilization of Apo-C3 and chylomicron blood contents. These results show that TG transport to peripheral tissues remained elevated after training cessation, suggesting that detraining induced long-term alterations in TG metabolism. Furthermore, in the absence of elevated Pl-LPL activity and with sufficient physical activity to augment fat oxidation, this phenomenon could increase TG storage within peripheral tissues to avoid persistent blood TG accumulation (39). Finally, in previously highly endurance-trained subjects, a 1-yr total detraining altered their lipid profile from a situation of insufficient body fat content toward a profile that presented potent cardiovascular risks for the future.

In conclusion, detraining induced a rapid loss of endurance training benefits on lipid profile. Highly trained subjects did not seem to take advantage of their physical activity level compared with moderately trained or recreational athletes. These subjects also presented long-term lipid profile alterations that probably resulted from the elevated TG turnover acquired during hard endurance training. This study has shown that highly trained athletes may experience long-term lipid profile alterations at cessation of their sports careers if they do not maintain a sufficient physical activity level.


   Footnotes
 
Abbreviations: Apo, Apolipoprotein; BMI, body mass index; HDL-C, high density lipoprotein cholesterol; HL, hepatic lipase; LDL-C, low density lipoprotein cholesterol; LPL, lipoprotein lipase; Pl-LPL, plasma lipoprotein lipase; RER, respective respiratory exchange ratio; TC, total cholesterol; TG, triglycerides; VLDL, very low density lipoprotein; VCO2, CO2 volume; VO2max, maximal oxygen consumption.

Received August 1, 2003.

Accepted March 18, 2004.


   References
Top
 Abstract
 Introduction
 Subjects and Methods
 Results
 Discussion
 References
 

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