SESSION 6: NUTRITION FOR MAINTENANCE OF HEALTH DURING TRAINING

The Concept of Energy Homeostasis for Optimal Health During Training

Wim H.M. Saris

Catalog Data

Saris, W.H.M. (2001) . The concept of energy homeostasis for optimal health during train­ing. Can. J. Appl. Physiol. 26(Suppl.): SI67-S 175. ©2001 Canadian Society for Exercise Physiology.

Key words: athletes, nutrition, energy homeostasis, leptin, body weight control Mots-cles: athletes, nutrition, homeostasie energetique, leptine, controle de la masse corporelle

Albstrac�eSUDne

From all nutritional variables optimal energy supply is considered as most vital for human performance. It is postulated that lack of energy homeostasis is the basic problem in the development of overtraining. Most if not all clinical symptoms are directly or indirectly related to the physiological mechanisms of energy homeostasis. The rapidly increasing knowl­edge in the field of body weight control with several new regulatory neuro-peptides such as leptin, will give new opportunities to tackle this unbalance between training load and en­ergy availability. The central role of leptin and insulin as adiposity signals has focussed attention on the anti-obesity aspects of leptin. However as member of the cytokine family, leptin is also closely linked to the immune and reproductive system. New data indicates clearly the dual function of leptin at both ends at the energy balance; starvation vs. over­feeding. It links also nutrition to the reproductive system. Lack of available energy has a much greater impact on leptin levels than exercise stress. It is suggested that application of the rapidly increasing knowledge in the obesity field will benefit the research on the mecha­nisms involved in the derailment of the delicate balance between training load and energy homeostasis in athletes.

Quoique des records soient continuellement brises, les contraintes biologiques ont encore un impact sur la performance humaine. L' etat nutritionnel est probablement Ie plus important facteur environnemental de la performance maximale en competition ou a I ' entrafnement. Une source optimale d'energie est la plus vitale de toutes les variables nutritionnelles. II

The author is with the Nutrition and Toxicology Research Institute Maastricht at Maastricht University, Maastricht, The Netherlands.

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S168 • Saris

semble qu ' une faille au niveau de I' homeostasie energetique soit a la base du probleme de surentrafnement. Tous les signes cliniques ou presque sont directement ou indirectement relies aux mecanismes physiologiques de l ' homeostasie energbique. Grace au rapide approfondissement des connaissances sur Ie controle de la masse corporelle et sur les neu­ropeptides de regulation comme la leptine, if est maintenant d' etudier Ie desequilibre entre

la charge d'entrafnement et la disponibilite des sources d'energie. Le role essentiel joue par la leptine et I 'insuline dans Ie developpement du tissu adipeux a amene plus de chercheurs a s 'interesser a la leptine et a son action contre I ' obesite. M embre de la famille des cytokines, la leptine est etroitement associee auxfonctions immunitaires et reproductrices. Des etudes recentes confirment le double role de la leptine aux deux extremites de I ' equilibre energetique (famine - suralimentation) et la relient au systeme reproducteur. Les taux de leptine sont plus affectes par le manque d ' energie que par Ie stress de l ' exercice. Ainsi, les applications decoulant des nouvelles connaissances dans Ie domaine de I ' obesite vont profiter aux etudes sur les mecanismes de defaillance du difficile equilibre entre la charge d'entrafnement et l 'homeostasie energhique chez les athletes.

Introduction

Today's athletes prefer the modem Olympic motto, citius, altius, fortius, which translates as "swifter, higher, stronger."

Athletic performances have been improving steadily since the modem sports became popular beginning of the last century. The mechanisation of occupational work has reduced daily energy demands drastically, leading to a rapidly growing interest of a wide segment of the popUlation for the limits of human performance. A triathlon instead of the marathon, runners running 100 or more miles, and climb­ers attacking Mount Everest without benefit of supplementary oxygen.

Although athletic records continue to be broken, constraints on human physi­ology inevitably imply overall limits to physical achievement. Among the impor­tant environmental variables is the nutritional status of the athlete. This is not only the case before, during or just after the competition but certainly also during the training period when the workload stresses the athlete in order to provide the stimuli for adaptation to the challenges encountered during competition. Exposing the athlete to exercise levels slightly greater than already adapted to has been called overload training (Kuiper and Keizer, 1988). To achieve a maximal training stimulus one should pay attention to optimise the dietary strategies. From observation studies some nutritional risks have been identified and will be reviewed in this paper.

Essential for athletic performance is an optimal energy homeostasis. Espe­cially in this research area exiting new discoveries has been published in the last five years. Most are directly related to the problem of obesity. But these new find­ings will certainly promote future research more specific on the topic of an opti­mal energy supply during training and competition.

Unbalanced Macro- and Micro-Nutrient Intake

The first and most clear difference in nutritional needs between athletes and non­athletes is energy. Physical exercise by means of training or competition will increase the daily energy expenditure by 2 to 4 MJ per hour, depending on physical fitness, duration, type and intensity of the sport. For this reason athletes must adapt the

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Energy Homeostasis • S 169

energy intake by an increased food consumption to meet the energy needs. This increased food intake should be well balanced with respect to the macro- and mi­cro-nutrient intake. A number of constraints make this task more complex then one might expect. Training load and time differs from day to day, resulting in much more variation in amount to be eaten and eating moments. Also the intensity of the exercise has a negative effect on appetite, digestion and absorption. If the total training load is high, athletes tend to ingest a large number of "in between meals or snacks" up to 40% of the total energy compared to about 25% in the general popu­lation (v. Erp-Baart et al., 1989). All these factors will has an effect on the food selection and ultimately on the energy and nutrient intake. Especially adapted food and fluids, which are easily digestible and rapidly absorbable, may solve this problem.

Energy intake, especially by female's athletes is often extremely low (WIlmore and Costill, 1994). Energy expenditure in average sedentary subjects ranges be­tween 1 .4 and 1 .6 Basal Metabolic Rate (BMR), while reported energy intake of top gymnasts usually ranges far below this level, despite the fact that they train for several hours per day. This can probably be explained by two factors: underreporting of the dietary intake and the urge to limit food intake, the first being the result from the latter. As a consequence the intake of micro-nutrients becomes at risk due to the fact that the intake of these nutrients is strongly related to the energy intake. For example in the nation wide study of van Erp-Baart et al. (1989b) with over 400 elite athletes in different sports disciplines, the linear regression analysis resulted in a correlation coefficient between iron intake and energy intake of R= 0.86 (Iron (mg) = 1 . 1 3 energy intake (MJ) +3. 10).

As a consequence a minimal energy intake of about 10.5 MJ is needed to reach the recommended dietary allowance for iron of 15 mg per day. A large num­ber of female athletes are below this energy intake level. As a consequence they are at risk for a chronic low intake of several vitamins and minerals and may benefit from nutritional supplementation.

Making and Gaining Weight

Whether the nutritional habits are realistic or not many athletes often limit their food intake in order to control body weight. There are four major reasons for this behaviour (Fogelholm and Saris, 1998).

1. Most athletes in weight-class events compete far lighter that their natural weight. Examples are wrestling, judo and lightweight -rowing.

2. Reduction of body weight and fat mass may be considered advantageous for esthetical reasons. A typical example is gymnastics.

3. Reduced body weight or relative fat mass is expected to bring a physiologi­cal edge, that is, to improve physical performance. This is an important rea­son for weight reduction in for instance, running and cross-country skiing.

4. Increased body mass preferably increased fat free mass, on order to increase absolute power output to resist the inertia of another body, or to overcome an external object. Most striking example are the Sumo wrestlers.

Athletes cut down their weight rapidly (less then one week) or gradually. The difference is that a negative energy balance accomplishes gradual weight re­duction, whereas dehydration is a necessary part of rapid weight loss. A large number

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Table 1 Effects of Rapid Weight Reduction on Athletic Performance

Max aerobic power Submax aerobic power Anaerobic power Muscle endurance and strength Recommended maximal limits

Fogelbolm and Saris, 1998

Period of rehydration

0-3 hr 5-24 hr

.l. .l. .l. .l.

4% BW

? ?

� �

8% BW

of techniques have been described to loose rapidly water. Among others, fluid restriction in combination with exercise and/or food restriction, rubber suit, sauna, diuretics and even vomiting (Steen and Brownell, 1990). Fogelholm and Saris (1998) have reviewed the literature on the negative effects of rapid weight reduc­tion by dehydration methods on different aspects of performance. In Table 1 the results are tabulated taken the time for rehydration after stopping the dehydration procedure (mostly at the moment of weight-in) into consideration. Especially in the fIrst hours all aspects of performance are negatively influenced. In contrast, a 5 to 24 hour recovery and rehydration period seems to be sufficient to recover most, if not all, indicators of performance.

Reduction of dietary energy intake is the primary technique for gradual weight reduction. Not surprisingly the lower the energy intake, the faster the weight loss. Diets with < 100 kJ/kglday result in weight reduction of > 1 kglwk. A more mod­erate energy restriction with an energy intake of 105 -135 kJ/kglday leads to a weight reduction of approximately 0.5 kglwk (Fogelholm and Saris, 1 998).

In contrast to rapid weight loss, the health hazards of gradual weight reduc­tion are minimal. Heavy training and an energy restriction might stress the female endocrine system originating from suppression in the Hypothalamic - Pituitary -gonadal Axis (HPA; Wade et al., 1996). This often leads to menstrual disorders. In contrast to the common belief, a fIxed "critical" amount or percentage of body fat, needed for regular menstruation, has not been established in athletics (Loucks, 1989). Other health risks are mostly related to chronic defIcient intake of certain vitamins and minerals such as iron and calcium in women. All other health risks are directly related to the chronic energy restriction, which will lead to a number of metabolic abnormalities especially when the training load is high. This "energy homeostasis" concept is not only of importance in reaction to athletic performance but is also the physiological basis of weight control.

Of particular concern in relation to graduate weight loss are aspects of growth and biological maturation in children and adolescents. So far these aspects are not well documented. It is especially difficult to distinguish between genetic predispo­sition and effects of training load and energy restriction. There are no indications that participation in sports interfere with growth even at elite level.

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Energy Homeostasis • S 171

A special category of athletes are those who want to gain weight especially muscle mass. A large number of nutritional ingredients have been proposed and evaluated. Among the most popular supplements advertised to increase muscle mass are protein, amino acids, chromium, vanadyl sulfate, boron, creatine and beta hydroxy-beta-methyl butyrate (HmB) . Only for protein and creatine is there some scientific evidence of a moderate effect on weight gain, For the other pro­moted ingredients the evidence is weak or nonexistent (Clarkson, 1 998).

Energy Homeostasis

Research in sport nutrition in the past three decades has been very successful in analysing the different aspects of muscle metabolism and performance. This effort has resulted in a large number of recommendation and sports nutrition products with a solid scientific background. Reviewing these developments it becomes clear that all the effective dietary manipulations are directly related to an optimal ATP production in the muscle. Impairment of the energetic flow is by far the most important factor for detrimental effects on performance.

As a consequence all aspects related to this energy homeostasis or energy availability are of importance. With the discovery of leptin in 1 994 (Zhang et al., 1994), a spectacular development started in the unravelling of the regulation of the energy homeostasis and in particular body weight control. Leptin is a 1 6-kDa pro­tein that is produced mainly by adipose tissue at concentrations paralleling the amount of fat reserve and acts at the hypothalamic level as a satiety factor (Schwartz et al., 2000). Together with the pancreatic hormone insulin, leptin is a very potent adiposity signal. Different mechanisms underlie the association of insulin and leptin with body fat content. However several observations indicate that leptin has a more important role than insulin in the CNS control of homeostasis. Several dis­tinct hypothalamic neuro-peptide containing pathways have emerged as candidate mediators of leptin and insulin action in the CNS . Neuro-Peptide Y (NPY) stimu­lates food intake while peptides such as a-Melanocyte-Stimulating Hormone (a­MSH) as well as Corticotropin Releasing Hormone (CRH), Thyrotrophin-Releas­ing Hormone (TRH), Cocaine- and Amphetamine-Regulated Transcript (CART) and Interleukin - 1 r3. promote satiety instead of hunger.

The initial view, that leptin functions primarily as an anti-obesity hormone has been revised both by new data and by theoretical considerations. Leptin and the leptin receptor tertiary structure resemble that of cytokines and lactogenic hor­mones linking its role to both the immune and the reproductive system. On a theo­retical level a potent anti-obesity signal would be subject to a negative genetic selection during the course of evolution. Flier ( 1 998) suggested for the first time the role of leptin as a starvation signal. Under energy restriction the human body will adapt metabolism to save energy to survive. Several studies have demon­strated that leptin levels fall rapidly out of proportion to the loss of fat stores. It suggests that leptin acts as a sensor of energy balance. More convincing is the recent finding that injection of leptin during a severe energy restriction period results in additional weight loss (Hukshom et al., 2001) . It also explains the direct link of leptin to the reproductive system and the important connection between nutrition and reproduction. It is likely that leptin exerts its effect through the CNS, specifical ly within the hypothalamu s acting on the NPY / AgRP and

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Dual action of leptin

Leptin J,

1 � ..

overfeeding

• • starvatIon

Ada�� . � to starvation . Thyroid l .------. Immune suppreSSIOn

Reproduction J, ./ Stress axis t '/ Growth J,

Figure 1.

Leptin t

1 Resistance to obesity Food intake I Energy expenditure J, ?

Pro-OpioMelanoCortin (POMC) neurons as well as on the Hypothalamic Pitu­itary-gonadal Axis (HPA) and the thyroid axis, all directly involved in the energy homeostasis and reproduction. This perspective makes it clear that leptin has a dual function in energy homeostasis with several important regulatory links to other important physiological functions all directly depending on the energy bal­ance (Figure 1).

Training, Overtraining, and Energy Homeostasis

Many athletes are obsessed with training. This can easily leads to overtraining, a situation when the training stress exceeds the capacity to recover. A number of characteristic symptoms have been described collectively referred to as overtrain­ing syndrome (see Table 2).

Linking the physiological systems and more in particular the regulatory hor­mones, it becomes clear that most of these symptoms are directly or indirectly related to the problem of energy availability. All tabulated biomarkers are major players in the complex system of energy homeostasis. This observation forced us to re-evaluate the problem of early recognition of the overtraining syndrome and the therapeutic measures.

Important hormonal regulators such as the leptin/insulin adiposity/cachexia signals could play an important role in the recognition of an early derailment of the energy homeostasis and consequently additional physiological function such as reproduction. So far the studies evaluating whether exercise per se or an energy deficiency is the critical factor on the regulation of leptin are limited. Van Aggel­Leijssen et al. ( 1999) showed that acute exercise decreases the nocturnal peak and average 24-h plasma leptin concentration. Positive or negative energy balance gave a much higher fluctuation. A short-term training program (12 weeks) did not

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Energy Homeostasis • S 173

Table 2 Clinical Symptoms and Central Acting Physiological Systems

Involved in Overtraining

Symptom Physiological system Biomarkers

Decrease appetitelbody weight Energy homeostasis Leptin ,J.., E i, NE i, loss Cortisol i, TRH i, Insulin ,J.. Sleep disturbance Circadian rhythm Orexins ?, (3-endorphin i Elevated HR and BP SNS E i, NE i, Dopamine i,

Cortisol i N ausea/gastro-intestinal GI hormonal CCK i

problems

Prone to infection Immune system ll..- 1 i, lNF- ex i, CRF i, Leptin ,J.., ll..-6 ?

Menstrual irregularities Reproductive system GnRH/LH pulsatility ,J.., Testosteron J.., Leptin ,J..

influence leptin levels corrected for changes in fat mass (Thong et al., 2000). How­ever in a long-term training program (16 months) a significant inverse relation was found between leptin levels and hours of training corrected for changes in insulin and body fat percentage (Pasman et al., 1998). In an elegant designed study, Hilton and Loucks (2000) dissected the exercise stress from the energy availabil­ity. Low energy availability profoundly suppressed the average 24-h and ampli­tude of the diurnal rhythm of leptin where as exercise has no effects. The effect of low energy availability caused by increased exercise energy expenditure was smaller than those caused by dietary energy restriction. The altered fuel selection in the muscle, saving carbohydrate might be a plausible explanation for this effect on leptin. This study demonstrated the importance of energy availability in compari­son to exercise stress on leptin as an important biomarker of energy homeostasis. It focussed the importance of adequate nutrition to secure an optimal energy sup­ply during training and competition.

Conclusions

Based on the available literature it becomes clear that the energy availability has a much greater impact on leptin levels than exercise per se. It also points to the dual function of leptin at both ends of the energy balance scale; starvation vs. overfeed­ing. In addition it links nutrition to the reproductive and immune system.

More specific research is needed, taken the rapidly increasing knowledge in the research field of energy homeostasis and body weight control into consideration.

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It will certainly gives us more insight in the mechanisms involved and more im­portantly, how to prevent even under intense physical training stress impairment of the energy flux to generate in time the requested ATP production for maximal performance.

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