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Nutrition and Performance in Sport

Christophe Hausswirth

Chapter 4. Nutrition and specific sport populations

Topic 3. Nutritional aspects of post-exercise recovery: a gender difference

Christophe Hausswirth et Yann Le Meur


Performing elevated training workloads is susceptible to yield deleterious effects if the organism is unable to recuperate completely between training sessions. In this context, the recovery phase must be considered as an inherent component of the training process and must therefore be granted the same degree of attention, in its programming and management, as the exercise sessions themselves. Given the effects of gender upon the physiological responses to exercise and during the post-exercise recovery period, it appears essential to customize nutritional recovery methods according to gender in order to optimize the processes of physiological recovery and super-compensation of glycogen, while minimizing the risks of injury (i.e. stress fracture) in the female athlete.

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1. Introduction

1The large majority of exercise physiology research has been performed exclusively on male populations. Until the 1980s, it was widely presumed that the physiological responses to exercise did not truly differ between males and females. From this assumption, the design of training programmes and the recommendations for recovery strategies have been generalized to females, without any prior determination of whether such a direct transfer was viable. Since then, numerous studies focusing on gender (Clarkson et Hubal, 2001; Tarnopolsky, 2000) have uncovered some specificities in female’s physiological response to exercise, and determined that gender is an important variable to control for in order to design robust research protocols. The Female's response to various types of exercise and physical training is now better understood. It appears that the aerobic power and muscular strength of females are naturally lower than male's, due to differences in body size and composition, hormonal status, socio-cultural influences and dietary habits (Shephard, 2000). Yet despite these factors, well-trained female athletes can deliver performances that are by far superior to those of poorly trained males. Within this context, a growing number of studies have turned their focus toward the effects of gender on recovery in sport, thereby contributing to a better comprehension of the similarities – and disparities – in the post-exercise recovery processes occurring in males and females. Nevertheless, the factors contributing to the lack of a global consensus can be attributed to differences observed in training and nutrition status, and to female's hormonal variations over the course of the menstrual cycle and the influence of the latter upon energy metabolism during exercise (Bonen et al. 1983).

2This chapter reviews some of the major gender differences in the metabolic and nutrition response to exercise and its subsequent recovery, focusing on those which may be most pertinent to the design of training programmes for athletic females specifically, in order to optimize the physiological adaptations sought for improving performance and maintaining health.

2. Recovery and maintenance of energy stores: a gender difference?

3Performance in long-duration activities that rely upon aerobic metabolism is related to the avaibility of endogenous energy reserves. In light of this, the fatigue induced by exercise can be linked to the athlete’s inability to continue supplying energy to the working muscles, due to the exhaustion of endogenous energy stores (Abbiss et Laursen, 2005). This type of fatigue can also occur in athletes training multiple times per day, even in those not necessarily specialized in endurance activities causing large quantities of energy expended (Snyder, 1998). The depletion of energy stores may set in progressively, when daily caloric intake does not compensate for the total energy expenditure linked to both basal metabolism and the practice of a sport. Recovery strategies must therefore take into account the specificities of women's metabolic response to exercise to ensure the maintenance of energy stores and to support the training workloads.

4Metabolic responses during prolonged exercise. Even though females were excluded from participating in the Olympic marathon until 1984, several studies demonstrated that they could actually perform better than males in ultraendurance events (Bam et al. 1997; Speechly et al. 1996). For instance, Speechly et al. (1996) showed that females, despite slower performances in a marathon than a given group of males, performed better than the latter when the race distance exceeded 90 km. Bam et al. (1997) showed by way of linear regression analysis that females may potentially hold an advantage over males when the race distance of a running race reaches or exceeds 66 km. For Tarnopolsky (2000), this phenomenon would be linked to gender-based metabolic differences during prolonged exercise, and more specifically to female’s greater capacity for lipid oxidation, which allows them to maintain glycaemia and preserve muscle glucose during these very long events.

5Tarnopolsky explains that the first studies to compare the metabolic responses of males and females during prolonged exercise date from the 1970s and 1980s (Friedmann et Kindermann, 1989; Froberg et Pedersen, 1984). All reported a gender effect, except that of Costill et al. (1979). These results, however, were considered with caution, as these investigations had neither accounted for the occurrence of menstrual cycles, nor evaluated precisely the training status of the subjects involved. Also, exercise intensity was determined relative to maximal oxygen consumption (O2max) without adjusting for each individual’s body mass. Since the 1990s, many studies have added to these preliminary results by factoring in these important methodological details in their protocols (Tarnopolsky et al. 1990; Tarnopolsky et al. 1997).

6Oestrogen has been repeatedly found to promote free fatty acid availability and lipid oxidation during exercise, possibly via an increased sensitivity to the lypolytic action of catecholamines (Ansonoff et Etgen, 2000; Ettinger et al. 1998). Also, even though intramuscular triglyceride content is dependent upon dietary fat consumption (Vogt et al. 2003) these intramuscular stores are generally much larger in females than males (Steffensen et al. 2002) and are utilized to a greater extent in females during prolonged exercise at a moderate intensity (90 minutes, 58% of O2max) (Roepstorff et al. 2002; Tarnopolsky et al. 2001). During this exercise trial, Roepstorff et al. (2002) demonstrated, by measuring the arterio-venous difference in non-esterifed fatty acids, that females consume 47% more non-esterifed fatty acids within the working muscles than their male counterparts. This result is verified by Mittendorfer et al. (2001) during a prolonged exercise protocol (90 minutes) of moderate intensity (50% O2max). Aside from the greater utilization of plasma nonesterifed fatty acids, Mittendorfer et al. (2001) observed greater lipolytic activity in female than male subjects that were matched by training level and fat mass percentage.

7Taken together, these findings convey that females possess larger intramuscular triglyceride stores and rely more heavily upon this substrate during exercise, as is confirmed by Tarnopolsky (2008) in a meta-analysis of the literature. The gender-based differences in whole-body substrate oxidation during exercise are reflected in the lower respiratory exchange ratio of females compared to males for a given exercise intensity and duration of exercise, as is displayed in Table 1.

Table 1: Summary of studies where whole-body substrate metabolism was reported in trained males and trained females with exercise duration > 60 min. Adapted from Tarnopolsky (2008): only data from studies using trained subjects are reported in the present table. Significant gender difference was calculated at P= 0.02 using a two-tailed independent t-test.

Table 1: Summary of studies where whole-body substrate metabolism was reported in trained males and trained females with exercise duration > 60 min. Adapted from Tarnopolsky (2008): only data from studies using trained subjects are reported in the present table. Significant gender difference was calculated at P= 0.02 using a two-tailed independent t-test.

8Tarnopolsky et al. (1990) showed that a rise in urinary nitrogen concentration (i.e. an indicator of protein utilization) occurs in males within the 24 hours following endurance exercise compared to a control day, while no significant difference is observed in females. This reveals that proportionally greater amounts of amino acids are oxidized by males during exercise than females. These results were then confirmed in a study by Phillips et al. (1993) who demonstrate that males oxidize more protein and leucine than females. These findings were completed by McKenzie et al. (2000) who showed that females utilize leucine as an energy substrate to a lesser extent than males during a 90-minute pedalling exercise at 65% O2max, both before and after a 31-day endurance training programme. Interestingly, these authors also reported that even though before the training programme, leucine oxidation doubled during exercise compared to the resting state, no differences were observed in this variable at the end of the training period.

3. Metabolic responses after prolonged exercise

9Henderson et al. (2007) showed that if a greater fatty acid mobilization occurs in females during prolonged exercise compared to males, the inverse is observed during the recovery phase. This could explain why, even though females mobilize lipids to a greater extent than males during endurance exercise (Henderson et al. 2007) they lose less fat mass than their male counterparts during a physical training programme, as several studies demonstrated (Donnelly et Smith, 2005). Some experimental data have indeed revealed that some metabolic disturbances caused by an exercise session could still be observed several hours after its completion (Henderson et al. 2007; Horton et al. 1998; Kuo et al. 2005; Phelain et al. 1997). Henderson et al. (2007) showed that the rate of lypolysis was still elevated 21 hours after a 90-minute pedalling exercise at 45% of O2max, or 60 minutes at 65% of O2max in males, whereas significant differences in lipolysis are no longer observed in females by that point (see Fig. 1).

Figure 1 (A, B): Lipid oxidation. Fatty Acid (FA) oxidation rate in males (A) and females (B). FA oxidation by a combination of tracer-derived measurement and indirect calorimetry on Day 1, and solely by indirect calorimetry on Day 2. Values are means ± SEM. Males, n= 10 for Days 1 and 2. Females, n= 8 for Day 1 and n= 6 for Day 2. CON, Control trial; 45, 4% VO2 peak trial; 65, 65% VO2 peak trial. Recovery, day 1; average from 30 min post-exercise. Recovery, Day 2; the next day following exercise bouts.

Figure 1 (A, B): Lipid oxidation. Fatty Acid (FA) oxidation rate in males (A) and females (B). FA oxidation by a combination of tracer-derived measurement and indirect calorimetry on Day 1, and solely by indirect calorimetry on Day 2. Values are means ± SEM. Males, n= 10 for Days 1 and 2. Females, n= 8 for Day 1 and n= 6 for Day 2. CON, Control trial; 45, 4% VO2 peak trial; 65, 65% VO2 peak trial. Recovery, day 1; average from 30 min post-exercise. Recovery, Day 2; the next day following exercise bouts.

*: total FAox in 45% VO 2peak trial significantly different from corresponding time points in Control trial, P<0.05. FA oxidation was significantly elevated above Control during exercise at either intensity in both genders (P<0.05). Plasma FA oxidation was elevated above Control during exercise and recovery for both exercise intensities, while other (non-plasmatic) FA oxidation was significantly elevated above (P<0.05), but not during post-exercise recovery.
#: total FAox in 65% VO 2peak trial significantly different from corresponding time points in Control trial, P<0.05. FA oxidation was significantly elevated above Control during exercise at either intensity in both genders (P<0.05). Plasma FA oxidation was elevated above Control during exercise and recovery for both exercise intensities, while other (non-plasmatic) FA oxidation was significantly elevated above (P<0.05), but not during post-exercise recovery.
Reproduced from Henderson et al. (2007), with permission from
Journal of Physiology (London).

10To further elucidate the effect of gender on the evolution of post-exercise metabolism, Henderson et al. (2008) compared the evolution of glycaemia in sedentary males and females over the 3 hours succeeding a 90-minute pedalling bout at 45% of O2max and after pedalling for 60 minutes at 65% of O2max, using labelled glucose. Because euglycaemia is influenced by the time of day, a control situation during which the sedentary subjects continued to go about their normal routine was included. Results revealed an increase in the rates of blood glucose appearance and disappearance as well as a greater metabolic clearance during the two exercise situations compared to the control setting in both genders. Differences between males and females appeared, however, when comparing the metabolic responses postexercise compared to the control situation. Three hours after stopping exercise, male subjects were found to have higher rates of blood glucose appearance and disappearance, higher metabolic clearance, and a lower glycaemia, while no differences were found in females for any of these parameters between the post-exercise and the control situations. These results suggest that compared to males, females have a greater ability to maintain glycaemia during the recovery period following prolonged exercise, which could explain why lipolysis occurs to a lesser degree in females during this phase. They also confirm their previous results (Henderson et al. 2007), which revealed a weaker reliance on postexercise lipolysis and a more precise glucoregulation in females compared to males.

11Thus, given that females mobilize lipids to a greater extent during exercise, that their lipid stores are greater and that they show a better propensity to spare glycogen, females have a greater ability than males to maintain constant energy substrate stores, during exercise, as well as during the recovery period (Henderson et al. 2008). These metabolic specificities imply the necessity for gender-specific nutritional recovery strategies (Boisseau, 2004; Tarnopolsky, 2000).

4. Strategies for nutritional recovery and repletion of energy substrates after prolonged exercise

12Most of the research performed in sports nutrition and energy metabolism during exercise has been carried out on male subjects. Nevertheless, numerous recent studies have determined some of the specificities for restoring energy parameters in female subjects.

13Carbohydrate intake. Kuipers et al. (1989) studied glycogen resynthesis following a bike ergometer exercise to exhaustion in endurance-trained athletes (i.e. seven men and nine women). During the 2.5 hours following the end of exercise, subjects consumed a 25% maltodextrin-fructose solution (carbohydrates: 471 ± 5 g and 407 ± 57 g for males and females, respectively). Glycogen repletion occurred in similar proportions in males and females.

14Different studies demonstrated improved glycogen repletion when carbohydrates (or carbohydrates + proteins) are consumed immediately after exercise instead of a few hours later (Ivy et al. 2002; Ivy et al. 1988). Tarnopolsky et al. (1997) compared the rate of glycogen resynthesis in males and females following a 90-minute exercise bout at 65% of O2max and the ingestion of three solutions: one a placebo, one containing 1 of carbohydrate, and one containing 0.7 of carbohydrate/0.1 of protein/0.02 of lipids, immediately after and an hour following exercise. Glycogen resynthesis occurred faster for both genders with both test solutions than with the placebo, with no differences between males and females (Fig. 2). Finally, a study by Roy et al. (2002) showed, in ten young females, that the post-exercise intake of 1.2 of carbohydrate, 0.1 of protein and 0.02 of lipids during a period of training (four training sessions per week) resulted in an increased time to exhaustion at 75% of O2max and tended to diminish protein oxidation over the week following the protocol. These data therefore show that, when carbohydrate intake is proportional to body mass, no significant differences appear between males and females in their capacity to replenish their glycogen stores. In light of these findings, when the time allotted between two training sessions is less than eight hours, both female and male athletes must consume carbohydrates as soon as possible after exercise in order to maximize the replenishment of glycogen stores. There is an undeniable interest to breaking up the total intake of carbohydrates into smaller portions in the early phase of recovery, especially when it is not possible or practical for the athlete to eat a full meal shortly after a training session (Ivy et al. 1988). Carbohydrate-rich meals are recommended during recovery. Adding 0.2 to 0.5 g of protein per day and per kg to carbohydrates in a 3:1 (CHO: PRO) ratio is recommended. This holds particular importance when the athlete’s training sessions occur twice daily and/or are very prolonged (Berardi et al. 2006; Ivy et al. 2002). Let us recall that no difference is observed in terms of glycogen repletion when carbohydrates are consumed in the form of solids and liquids (Burke et al. 2004). Carbohydrates with a moderate to high glycaemic index supply energy quickly for glycogen resynthesis during recovery and must therefore be prioritized in energy-replenishing snacks following exercise (Burke et al. 1993).

Figure 2: Rate of glycogen resynthesis for each trial over the first 4h post-exercise (from Tarnopolsky et al. [Tarnopolsky et al. 1997]). Open bars, males; solid bars, females.

Figure 2: Rate of glycogen resynthesis for each trial over the first 4h post-exercise (from Tarnopolsky et al. [Tarnopolsky et al. 1997]). Open bars, males; solid bars, females.

* P <0.05 compared with placebo.

15Thus, the daily intake of female athletes must reach 5 g of of body weight per day (Manore, 1999). If the training volume is high and training sessions occur least once daily, this can increase to 6 to 8 of body weight per day. Given the tendency of female athletes to limit their daily caloric intake, it appears necessary to ensure that these needs be met daily in order to maintain adequate energy balance (Manore, 2002).

16Lipid intake. Despite the importance of sufficient daily intake in essential fatty acids, many female athletes considerably limit their consumption of lipids (down to lipids only providing 10 to 15% of daily caloric intake), believing that the latter are likely to compromise performance and increase body fat mass (Larson-Meyer et al. 2002). However, in addition to compromising their health, these very low-fat diets reduce intramuscular triglyceride stores, which are crucial to supply free fatty acids to the muscles during recovery, especially for athletes in long-duration disciplines or those often training multiple times per day. Larson-Meyer et al. (2002) showed that the lipid intake for female athletes specializing in long events must reach 30% of daily caloric intake to ensure a rapid resynthesis of intramuscular triglyceride stores. If post-exercise lipid intake is insufficient, the depletion of intramuscular triglyceride stores is still observed two days following exercise (Larson-Meyer et al. 2008; Larson-Meyer et al. 2002). As some studies have demonstrated the very low lipid intake in this population (Beals et Manore, 1998), it has also been hypothesized that a very low lipid intake (i.e. 10 to 15% of caloric intake) coupled with a high-endurance training volume could be detrimental to performance by compromising intramuscular triglyceride stores (Muoio et al. 1994).

17Also, even though this study by Larson-Meyer et al. (2008) did not report any decrease in performance during a 2 hour running trial following a short-term low-lipid diet (3 days, 10% of caloric intake), this diet did yield a modification of the athletes’ lipid profiles, as had already been proven in another study by Leddy et al. (1997). They showed that a low-lipid diet increases triglyceride concentration and decreases the concentration of HDL cholesterol, leading to a lowered ratio of total cholesterol (HDL cholesterol, an adverse consequence in terms of cardiovascular health). Even though no study to date has yet demonstrated this, this observation suggests, according to Larson-Meyer et al. (2008), that endurance athletes must make sure to consume a sufficient amount of lipids daily, particularly if they, or someone in their family, have any problems linked with their lipid profiles. Future studies are needed to observe the effect of a chronic hypolipidic diet on prolonged exercise performance.

18In conclusion, it appears that while carbohydrate and protein intake should be favoured immediately post-exercise, in the scope of the athlete’s general diet lipids intake should be maintained at a sufficient level. If fat consumption supplies less than 1% of daily caloric intake, there is the risk of a deficiency in essential fatty acids and vitamin E (Manore, 2002). Female athletes should therefore be advised to consume vegetable oils, nuts and “fatty” fish, such as tuna and salmon, on a regular basis (Manore, 2002).

19Protein intake. Chronic aerobic exercise is well known to diminish amino acid utilization. However, the metabolic oxidation capacity of amino acids augments as a result of an improved activity of the limiting enzyme, glutamate dehydrogenase (Lamont et al. 1987). For this reason, male and female athletes must increase their daily protein intake.

20Concerning proteins, it is recommended that female athletes maintain a daily energy intake superior to those recommended for the standard population, in order to ensure that the mechanisms of recovery, on a structural standpoint, are able to occur (1.2 to 1.4 of body weight per day, compared to 0.8 of body weight (Manore, 1999). Phillips et al. (1993) demonstrated that a daily protein intake of 0.8 leads to a negative nitrogen balance in female athletes. Many studies performed on female athletes hightlight the fact that this intake is often at the lower end of these recommendations, if not below them, particularly in amenorrhoeic athletes (Howat et al. 1989; Pettersson et al. 1999). For female athletes specializing in strength sports, these recommendations reach 1.4 to 1.8 of body weight, given the extent of muscular damage caused by this type of activity. Foods containing proteins with a high biological availability (a high retention and utilization rate by the body) should be emphasized. Meats, fish, eggs and dairy products offer complete sources of protein (providing all essential amino acids), and it is particularly important for vegetarian or vegan athletes to pay attention to their protein sources to ensure that all essential amino acid requirements are met, usually by combining different sources such as nuts, whole grains, and legumes (Hoffman et Falvo, 2004). Also, protein-rich animal foods are an important source of dietary iron, the latter helping to limit the risk of anaemia, a problem of particular concern for female athletes (Akabas et Dolins, 2005). Volek et al. (2006) also consider that female athletes should be aware of the fact that animal protein sources provide vitamin B-12 and D, thiamin, riboflavin, calcium, phosphorus, iron and zinc (Manore, 2005).

5. Metabolic responses during and following brief intense exercise

21During brief, high-intensity exercise, the work performed by skeletal muscle relies heavily upon the breakdown of phosphocreatine (PCr) stores and the recruitment of glycolysis to ensure the resynthesis of energy. Under these conditions, the resulting decrease in intramuscular pH and the accumulation of inorganic phosphate (Pi) play an important role in the development of muscular fatigue (Allen, 2009). For this reason, it has been suggested that a rapid clearance of lactate and H+ ions after intense exercise is essential for recovery in order to restore work capacity quickly, particularly in the context of sports activities involving repetitive short and intense exercise bouts (Ahmaidi et al. 1996). Several studies performed on the effect of gender upon the metabolic response during and post-exercise contribute interesting clues regarding the methods of recovery that must be prioritized in athletic females after such brief, high-intensity exercise.

22The pre-exercise phosphagen (ATP, ADP, PCr) concentrations do not differ between genders (Esbjornsson-Liljedahl et al. 2002). Still, Ruby et Robergs (1994) reported a greater glycolytic activity in males compared to females during exercise. In this regard, Jacobs et al. (1983) had already shown that men reach higher concentrations of intramuscular lactate than females following anaerobic exercise tests. These results were then confirmed by the in vivo study of Russ et al. (2005), which showed males relying more heavily upon glycolysis than females, even though their reliance upon the flux of PCr and aerobic pathways for force production did not show parallel gender effects. This difference could be explained by a greater cross-sectional area of Type II muscle fibers (Coggan et al. 1992) and/or a greater glycolytic enzyme activity (Coggan et al. 1992). Recently, Wüst et al. (2008) reinforced this hypothesis by demonstrating that men’s lower resistance to fatigue would be more strongly linked to gender differences in muscle fiber type distribution than to differences in motivation, muscular size, oxidative capacity or local blood flow.

23In this context, Esbjörnsson-Liljedahl et al. (2002) showed that over three all-out 30 second sprints separated by 20 minutes of passive recovery, females were able to maintain a steadier level of performance than males. Despite similar fitness levels (physically active, non-competitive) females showed a lower accumulation of metabolic products than males, particularly within the Type II fibers (Esbjornsson-Liljedahl et al. 2002). During the recovery phase, females have a greater capacity for recycling their ATP supply than males, granting them a better aptitude to take on the next intense, brief exercise bout.

6. Chronic fatigue and management of daily energy balance

24In female athletes, the maintenance of energy balance is a topic in need of particular attention, due to the frequently observed concerns with physical appearance and the social pressures pushing them to maintain a low percentage of fat mass (Burke, 2001; Manore, 1999, 2005; Volek et al. 2006). A positive energy balance is indeed necessary to ensure optimal metabolic recovery and to promote the muscular regeneration processes in order to withstand training loads (Snyder, 1998). However, the literature reports the daily caloric intake as often insufficient in high-level female athletes, particularly those involved in sports in which a thin silhouette confers an advantage (Deutz et al. 2000; Manore, 2002). Figure 3, from an article by Deutz et al. (2000) shows that the energy balance of high-level gymnasts remains almost always negative throughout the day. Maintaining the equilibrium between daily energy intake and expenditure by way of well-adapted nutritional recovery methods concerns all athletes in any sport who must train daily or multiple times per day.

Figure 3: Comparison of within-day energy balance in four groups of elite athletes (from Deutz et al. 2000). Each group has 24 bars, beginning with waking and ending 24 hours later. The bars represent 4 h for each hour in the day. Energy surpluses and deficits are represented, respectively, by variations above and below the zero (0) energy-balance line.

Figure 3: Comparison of within-day energy balance in four groups of elite athletes (from Deutz et al. 2000). Each group has 24 bars, beginning with waking and ending 24 hours later. The bars represent 4 h for each hour in the day. Energy surpluses and deficits are represented, respectively, by variations above and below the zero (0) energy-balance line.

25A negative energy balance is associated with a chronic state of fatigue, decreased alertness, sleep disturbances and a rise in protein catabolism, which may compromise the mechanisms for muscle resynthesis (Snyder, 1998). It therefore appears necessary to inform female athletes of the importance of maintaining an adequate daily energy intake, especially since two thirds of them express the desire to lose weight and to limit their daily caloric intake (Hinton et al. 2004). These dietary behaviours are not always, however, associated with weight loss (due to a decrease in resting metabolism [Deutz et al. 2000]), but rather to disturbances in the menstrual cycle (Loucks, 2003).

26The majority of female athletes require a minimum of 2300 to 2500 (9263 to 10460 kJ) in order to maintain their body mass (45 to 50 (Manore, 1999, 2002). Those involved in endurance sports, such as marathon running or triathlon, have energy needs susceptible to reach as much as 4000 (16736 kJ) (Manore, 2002). The American Dietetic Association, Dieteticians of Canada and the American College of Sports Medicine revealed that a relatively high-carbohydrate intake is usually recommended for athletes during the recovery period, independently of gender, due to the role of carbohydrates in maintaining glycogen stores (Rodriguez et al. 2009). However, increasing the daily caloric intake of female athletes solely via increased carbohydrate consumption does not appear to be an optimal solution (Boisseau, 2004). A female athlete consuming about 2000 kcal per day is not able to increase significantly her glycogen stores significantly solely by increasing the percentage of carbohydrates composing her diet. In fact, she would have to boost her caloric intake by 30% over the course of four days in order to reach a carbohydrate intake superior to 8 (Tarnopolsky et al. 2001). From a practical standpoint, this is neither habitual nor acceptable among athletes watching their weight constantly. Moreover, such a large shift of caloric sources toward carbohydrates is likely to lead to deficiencies in some essential proteins and lipids, and compromise nitrogen balance, necessary for maintaining normal sexual steroid hormone levels (Volek, 2005). In this context, several authors (Larson-Meyer et al. 2002; Volek et al. 2006) recommend a lipid intake of 30% of daily energy needs for female athletes.

7. Recovery from exercise-induced bone damage

27Bone turnover and stress fracture. The majority of physical activities exert strong pressures upon the skeletal system, thereby increasing bone cell turnover. The mechanisms for osteogenesis and bone recovery are largely dependent upon calcium intake and overall caloric intake (Manore, 1999; Nattiv, 2000), as well as hormonal status (Kameda et al. 1997; Weitzmann et Pacifici, 2006).

28Howat et al. (1989) report that the diets of female athletes are frequently poor in calcium, especially when dairyproduct consumption is low or non-existent. This contributes to compromising their bone health and increasing their risk for stress fractures (Manore, 1999; Nattiv, 2000). It therefore seems essential, during recovery, to promote calcium consumption to aid the bone remodelling processes (Nattiv, 2000). In spite of this, female athletes often fail to maintain a sufficient calcium intake, especially when dairy products are not included in their diet. Several studies have thus shown that daily calcium intake can vary between 500 and 1623 in female athletes, with most of them not even reaching 1000 (Kopp-Woodroffe et al. 1999). By contrast, the recommended daily intake of calcium is 1300 for females between 9 and 18 years old, and 1000 for females between 19 and 50 years old. The results of a recent study by Josse et al. (2010) illustrate the beneficial impact of milk consumption on bone turnover in young females, over the course of a twelve-week strength training programme. Five times per week, subjects consumed either twice 500 ml of fat-free milk (MILK, 1200 mg. day-1 of calcium and 360 IU. day-1 of vitamin D), or an isoenergetic carbohydrate drink immediately and 1hour after each strength-training session (Fig. 4A and 4B). The MILK group showed a larger rise in serum 25-hydroxyvitamin D (vitamin D acting to promote calcium absorption and bone turnover) levels than the CON group, while parathyroid hormone (responsible for bone resorption by enhancing the release of calcium into the bloodstream) levels decreased in MILK only. The greater lean mass gains observed in the MILK group also suggest larger gains in bone mass, and finally, fat mass decreased in the MILK group only. These results emphasize the important role of calcium as part of nutritional strategies for optimal bone health and recovery.

Figure 4 (A, B): Evolution of fat mass (A, left) and lean mass (B, right) before and after 12 weeks of strength training in groups having consumed milk following training sessions (MILK, n= 10) or an isoenergetic carbohydrate drink (CON, n= 10) (from Josse et al. 2010).

Figure 4 (A, B): Evolution of fat mass (A, left) and lean mass (B, right) before and after 12 weeks of strength training in groups having consumed milk following training sessions (MILK, n= 10) or an isoenergetic carbohydrate drink (CON, n= 10) (from Josse et al. 2010).

* Significantly different from CON in the pre-to post-training difference (P<0.05). Values are mean ± SE.

29Inadequate caloric intake also undermines bone health by suppressing hypothalamic-pituitary gonadal axis activity, resulting in low estrogen production and causing menstrual-cycle disturbances (De Souza et Williams, 2005; Laughlin et Yen, 1996). Oestrogen plays a multi factorial role in maintaining bone health in premenopausal women, both by slowing bone resorption (Kameda et al. 1997) and stimulating its formation (Weitzmann et Pacifici, 2006). The elevated occurrence of osteopaenia and increased rate of bone fractures is well documented in premenopausal athletic females with hypothalamic amenorrhoea and in anorexic females (Grinspoon et al. 1999; Marcus et al. 1985). Athletes who restrict caloric intake despite important training loads compromise the hormonal processes involved in bone remodelling, placing themselves at a risk for bone loss comparable to post-menopausal females. In this regard, maintaining adequate energy availability holds particular importance through puberty and until late adolescence, when females reach their peak bone mass (Eastell, 2005).

30Vitamin D status is another important factor to preserving bone health. Athletes living in Nordic countries and training mostly indoors often show a poor vitamin D status; a level ≥ 80 nM is necessary to maintain good bone health (Grant et Holick, 2005). Studies show that the daily supply in vitamin D averages 5 µ g per day (200 IU. day-1) in females between 19 and 50 years of age. It is therefore advisable to compensate for this deficit with a well-adapted diet, or by way of luminotherapy. Finally, adequate protein intake should be included in the nutritional recovery strategies aiming to preserve bone health, in order to limit, over the short term, the risks of stress fractures, and over the long term, the onset of osteoporosis.

8. Evaporation and hydration strategies for recovery

31Sweat loss during exercise. In their review of the literature on the effects of gender upon thermoregulation during exercise, Kacibua-Uscilko and Grucza (2001) report that females differ from males in their exogenous heat storage, their thermolytic capacities as well as their endogenous heat production during exercise. These differences are mainly attributed to a lower body mass to surface area ratio, to greater subcutaneous fat stores and a lower exercise capacity in females. A higher fat mass percentage augments thermal stress by increasing the metabolic cost of performing a given exercise task (Bar-Or et al. 1969; Nunneley, 1978). In addition, the larger subcutaneous fat layer in females increases the distance between the active, heat-producing tissues (i.e. skeletal muscle) and the skin, reducing the rate of non-evaporative heat loss, and decreasing the body-surface-area to body-weight ratio (Saat et al. 2005).

32Nevertheless, when these differences are accounted for in research studies, differences between the genders are still observed. Females sweat less than males when for an identical subjective thermal rating, while maintaining the same body temperature as males due to a greater efficiency of the sweat evaporation process. Grucza (1990) also showed that females sweat less than males, without demonstrating a greater concomitant rise in rectal and body temperature. This author has put in evidence the fact that this difference can be explained by a greater amount of evaporated sweat (58.7% vs. 52.0% of total sweat lost, respectively) and a lower amount of dripping sweat in females compared to males (21.2% vs. 34.1%) of total sweat loss in females and males, respectively).

33Even though these experimental data suggest that the extent of water loss associated with exercise is proportionally lower in females, they should, nonetheless, compensate for these losses with well-adapted rehydration strategies.

34Post-exercise rehydration strategies. Recommendations for post-exercise rehydration are similar in males and females, and aim to compensate for the water and electrolyte losses occurring during exercise. Few studies have, however, compared the hydration strategies adopted by both genders. On this topic, Broad et al. (1996) have quantified the sweat losses and fluid intake of female soccer players. These authors reported that females drank, on average 0.4 l.h-1 during training and competition periods, which is lower than that reported for males. This difference may be mainly linked to morphological differences between genders, but also to lower metabolic heat production rates in females. However, electrolyte losses measured in the sweat of soccer players younger than 21 years old and senior on a British team over the course of one practice and one game appeared identical to those measured in their male counterparts (Shirreffs et al. 2006).

35In light of these results, it appears that the same recommendations for rehydration during recovery given to menmay be well adapted to females. Burke et al. (2001) do not bring forth any post-exercise hydration strategy specific to females. We therefore note that in the post-exercise period, it is necessary to replace, as rapidly as possible, the fluids lost during exercise. In subjects having lost 3% of body mass due to dehydration, Shirreffs et al. (2006) showed that ingesting, in small fractions of a 23-mM sodium solution, 150 to 200% of the water volume deficit. To speed the rehydration process in the context of multiple practices or competitions performed in one day, it appears advantageous to consume cool water (i.e. 12 to 15°), slightly flavoured and containing 2% of carbohydrates and 1.15 g.l-1 of sodium (Maughan et Shirreffs, 1997). When the amount of time separating the performances is greater, the fluid recovery of female athletes can occur via a combination of water and solid food intake. In this context, urine clarity may serve as the most practical method for athletes to evaluate their hydration status.


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