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Copyright © by ESPEN LLL Programme 2015 1
Nutrition and Sport Topic 37
Module 37.2
Nutrition for Endurance Sports
Anja Carlsohn
PhD, Nutritionist,
University of Education, Institute of Health Sciences,
Schwaebisch Gmuend, 73525, Germany
Learning Objectives
To demonstrate differences in physique, physiological demands, energy and nutrient
requirements in endurance athletes;
To apply recent recommendations for nutrient and fluid intake during habitual
endurance training periods as well as before, during and after endurance
competitions;
To critically argue pros and cons of using dietary supplements in endurance sports;
To be alert to potential clinical issues associated with nutrition in endurance sports
and to provide recommendations to reduce the risks.
Contents
1. The endurance athlete
1.1 Physique and physiological demands of endurance athletes
1.2 Energy requirements of endurance athletes in general training periods
1.3 Summary
2. Nutritional demands during general training periods
2.1 Recommendations for macronutrient intake
2.2 Fluids and electrolytes during the training process
2.3 Requirements of vitamins and minerals
2.4 Summary
3. Nutritional in specific situations: before, during and after endurance competitions
3.1 Nutritional competition preparation of the endurance athlete
3.2 Recommendations for food and fluid intake during endurance competitions
3.3 Nutrition for recovery from competition or exhausting training sessions
3.4 Summary
4. Dietary supplements used by endurance athletes
4.1 Supplements to support macronutrient intake
4.2 Vitamin, mineral and vitamin-mineral supplements
4.3 Ergogenic aids in endurance sports
4.4 Summary
5. Clinical issues concerning the nutrition of endurance athletes
5.1 Weight management, female athlete triad and eating disorders
5.2 Gastrointestinal distress
5.3 Hyponatraemia
5.4 Iron deficiency and iron deficiency anaemia
5.5 Summary
6. Summary
7. References
Copyright © by ESPEN LLL Programme 2015 2
Key Messages
Energy requirements of endurance athletes may considerably vary depending on the
sports discipline, exercise period, sex and individual anthropometric characteristics.
During habitual training, endurance athletes should ingest at least 3-5 g of
carbohydrates per kg body mass per day, which may increase up to 8-12 g/kg/d
during intensive training periods;
The requirement for protein is increased in elite endurance athletes with 1.6 g/kg/d,
whereas moderate-intensity endurance athletes (up to 5 sessions of 45-60 min per
week) require 1.2 g/kg/d of protein. Recreational athletes exercising up to 5 times a
week for 30 min do not have protein requirements different from RDA (0.8-1.0
g/kg/d);
Fat intake should approximate 20-35 % of energy intake;
Optimized glycogen stores before competition, may improve endurance performance
by enabling maintenance of exercise intensity (=speed) to the end of a race.
Carbohydrate loading protocols include increased carbohydrate intake and tapered
exercise;
During long distance events, a carbohydrate intake of 30-90 g/h depending on
exercise duration may improve exercise performance. Using multiple transportable
carbohydrates (e.g. glucose-fructose mixture) significantly increases exogenous
carbohydrate oxidation;
To recover from exercise, rehydration and glycogen resynthesis should be
nutritionally supported. For each kilogram of body mass lost, 1.5 L of sodium-rich
fluids should be ingested. Glycogen resynthesis is elevated, when 1.2-1.5 g of
carbohydrates per hour are ingested during the first few hours post-exercise;
The efficacy, risks and benefits of using dietary supplements need to be carefully
assessed. Approximately 15% of dietary supplements worldwide were found to be
contaminated or laced with doping substances;
Health professionals and coaches should be aware of clinical issues such as the
female athlete triad, disordered eating, gastrointestinal complaints, hyponatraemia
and iron deficiency that may occur in endurance athletes.
Copyright © by ESPEN LLL Programme 2015 3
1. The Endurance Athlete 1.1. Physique and Physiological Demands of Endurance Athletes
Endurance athletes may be involved in different sports such as running, cycling,
swimming, triathlon, canoe racing, skiing, skating, walking and others. Within these
sports, there are different disciplines. In conclusion, there are considerable differences in
the physiological and energy demands of endurance athletes. For example, running
1500 m (~3.5 - 4 min), 10.000 m (~26 - 30 min), marathons (~2.00 -2.25 hours),
ultra-marathons (> 6 hours), mountain runs (~45 min - >6 hours at altitudes of 1500-
4000 m above sea level) or steeplechase (~8-10 min) presents athletes with varying
training volumes (km per week), exercise intensities (highly aerobic vs. anaerobic
metabolism), different demands for high-intensity and long-lasting low-intensity training
or for accompanying (non-specific) exercise sessions such as technical training, strength
and power sessions or exercises in other sports.
It should also be taken into consideration that elite competitive athletes may have other
nutritional demands compared to recreational athletes or persons involved in endurance
sports for health reasons. Recently, there seems to be a consensus that athletes
exercising less often than five times a week for 30-45 min do not have nutritional
requirements different from the sedentary population, as this relatively small amount of
exercise may be seen as normal physical activity (1, 2).
Typically, endurance athletes have a low body mass and normal to low body mass index
compared to sedentary people and athletes from other sports such as strength athletes
(3). Table 1 provides average anthropometric data of endurance athletes.
Table 1
Anthropometric characteristics of elite endurance athletes
Sport Height [m] Weight [kg] Body fat [%]
or sum of
skinfolds
Reference
1500 m run
(9 females)
1.65 ± 0.12 52.40 ± 6.96 51.4 ± 10. 8
(6 skinfolds)
(4)
Marathon (11
females)
1.58 ± 0.18 45.58 ± 6.82 44.4 ± 7. 7
(6 skinfolds)
(4)
1500 m run
(16 males)
1.78 ± 0.05 65.69 ± 3.94 36.9 ± 5. 1
(6 skinfolds)
(4)
Marathon
(17 males)
1.72 ± 0.04 59.85 ± 3.34 33.2 ± 5. 5
(6 skinfolds)
(4)
Rowing & canoeing
(9 females)
1.75 ± 0.07 69.3 ± 11.0 18.5 ± 4.0 (5)
Rowing & canoeing
(8 females)
1.93 ± 0.07 92.9 ± 10.0 12.7 ± 2.0 (5)
Triathletes
(10 females)
1.67 ± 0.07 56.4 ± 6.1 25.9 ± 9.4
(4 skinfolds)
(6)
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1.2. Energy Requirements of Endurance Athletes in General Training
Periods
Energy requirements of endurance athletes may vary substantially between individuals
and between different training periods. The total energy expenditure (TEE) of endurance
athletes depends on their body mass, body composition, age, sex, their non-exercise
activity and the frequency, duration and intensity of exercise.
Total TEE of endurance athletes is typically 1.8 to 2.3-fold as high as the individual’s
resting energy expenditure (7), but may be higher (up to 4-fold) in professional
endurance athletes during short periods (8). Using the doubly labelled water technique
(DLW), Westerterp et al. observed a mean TEE of 3490±250 kcal/d in elite male Kenyan
runners during an intensive period of training (9). In ultra-endurance triathletes a mean
energy expenditure of 2630 ± 160 kcal/d was calculated from heart-rate monitoring
during competition (10). In elite female light-weight rowers, Hill et al. measured a mean
TEE of 3875 kcal/d using DLW during an intensive training period (11).
1.3. Summary
Endurance athletes represent a variety of sporting disciplines with different physiological
and metabolic demands. Therefore, only general nutritional recommendations are
available and should be provided in terms relative to body mass or energy expenditure to
account for the different physique of endurance athletes. As a rough estimation, energy
expenditure of endurance athletes is approximately twice as high as the resting energy
expenditure.
2. Nutritional Demands During General Training Periods 2.1. Recommendations for Macronutrient Intake
Meeting the energy demands of athletes is the major goal in endurance athletes.
Especially in females the energy intake is often observed to be considerably below the
estimated TEE. With low energy intake, even a high proportion of carbohydrates might be
insufficient to support adequate glycogen resynthesis during intensive training periods.
Vice versa, an athlete who consumes a moderate proportion of protein (~ 15 % of EI) in
a high energy diet may exceed the upper limit of intake for protein. Therefore,
recommendations for nutrients should be provided in absolute terms related to body
mass (i.e. g/kg/d) instead of proportions relative to energy intake.
Carbohydrate-rich foods (cereals, vegetables, legumes and products thereof) should be
the major source to account for elevated energy demands (2,7). During low-intensity
training periods (low-intensity or skill-based activities for less than 1 hour /day), a
carbohydrate intake of 3-5 g/kg/d seems to be appropriate to meet the demands of
endurance athletes (12).
In case of moderate training programmes (~ 1 h/d), 5-7 g/kg/d of carbohydrates are
recommended (12). For elite endurance athletes exercising 1-3 h/d or > 4 h with high-
to-moderate intensity a carbohydrate intake of 6-10 g/kg/d (8-12 g/kg/d, respectively) is
recommended to avoid glycogen depletion and negative effects on performance
outcomes or immune function (12). However, these recommendations need to be fine-
tuned considering the individual TEE, specific training needs and the individual’s feedback
from training performance (12).
Nitrogen balance studies in competitive endurance athletes suggest that athletes should
aim to ingest 1.2-1.4 g/kg/d of proteins (13, 14). Elite endurance athletes might require
up to 1.6 g/kg/d, whereas the protein requirement of recreational endurance athletes
(exercising 4-5x/week for 30 min) seems not to be higher than that of sedentary people
with 0.8-1.0 g/kg/d.
Copyright © by ESPEN LLL Programme 2015 5
Regarding fat intake, endurance athletes should follow the recommendations for the
general population, i.e. 20-35 % of EI should be provided by fat. Here, the proportion of
energy from fatty acids is recommended to be 10 % saturated, 10 % monounsaturated
and 10 % polyunsaturated (7).
2.2. Fluids and Electrolytes in the Training Process
Sweat losses during exercise may considerably vary between endurance athletes and
depend on individual sweat rates, type, duration and intensity of exercise, sex, fitness
level and environmental factors such as heat or humidity (15). In the literature, typical
sweat rates of 1.49 L/h (range 0.75-2.23 L/h) for male half-marathon runners during
winter competitions and of 1.77 L/h (range 0.99-2.55 L/h) for cross-country running
during summer training are given (16, 17).
There is strong evidence that dehydration increases the physiologic strain and the
perceived effort to perform an exercise. A dehydration >2 % of body mass can adversely
affect exercise performance (15, 18). Thus, it is recommended to avoid dehydration >2
% of body mass by regular intake of fluids during exercise and to support adequate
hydration by regular meal consumption spread over the day (15, 18, 19). However, to
reduce the risk for exercise-induced hyponatremia overdrinking (i.e. weight gain during
exercise) should be avoided (15) (see chapter 5.3).
Sodium (~900 mg/L), potassium (~ 200 mg/L), calcium (~18 mg/L), zinc (~0.6 mg/L),
copper (~ 0,1 mg/L) and magnesium (~1,4 mg/L) are the major minerals found in
human sweat during exercise, with a huge intra-individual variety (20, 21). As there is
evidence that sodium loss may be linked to exercise-induced muscle cramps (21),
athletes prone to heavy sodium loss (“salty sweaters”) should consume sodium-
containing drinks during exercise lasting >90 min (18).
In case food intake is adequate, no additional electrolytes or minerals are required in the
sports drink during habitual training, except for “salty sweaters”, who might need
beverages containing 400-1000 mg/L of sodium (18, 19, 22).
2.3. Requirements of Vitamins and Minerals
There are no special micronutrient intake recommendations available for endurance
athletes. Recently, there is no evidence to assume that recommended daily allowances
(RDAs) for micronutrient intake do not cover the demands of athletes (7, 23). However,
there are some micronutrients that might be crucial, especially when the athlete’s diet is
restricted and/or losses are elevated.
For antioxidants such as vitamins C and E, an increased requirement due to exercise-
induced production of reactive oxygen species has been postulated (24, 25). However,
there is no prove for detrimental effects on health or performance in case of marginal
deficiencies (26, 27). In contrast, more recent studies suggest that supplementation of
athletes with vitamin C and/or E may adversely affect health and training adaptation for
both health-oriented and elite athletes (28, 29, 30, 31).
Prevalence of iron deficiency is high (~50 - 70 %) among athletes, especially among
females (32, 33, 34). Iron status may be adversely affected by endurance exercise (34,
35). Thus, an elevated requirement is anticipated, but no general recommendation
exists. There is strong evidence that iron deficiency anaemia reduces aerobic capacity
(36, 37), but the effect of iron deficiency without anaemia is still unclear (38). Another
exception where requirements might be in some cases higher than the RDAs for the
general population is sodium (see chapters 5.3 and 5.4)
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2.4. Summary
Meeting the energy requirement is the major nutritional goal in endurance athletes.
Carbohydrate needs to avoid glycogen depletion vary from 3-5 g/kg/d during low-
intensity training periods, 5-7 g/kg/d in moderate training-periods to 8-12 g/kg/d in
periods of high-intensity high-volume training.
Both dehydration and sodium loss may be linked to exercise-induced muscle cramps.
Avoiding a dehydration >2 % of body mass by regular ingestion of sodium beverages
(400-1000 mg/L) and/or proper hydration before exercise are recommended.
Requirements for vitamins and minerals seem not to be higher than recommended daily
allowances for sedentary people, except for iron (esp. females) and sodium (esp. in salty
sweaters).
3. Nutrition in Specific Situations: Before, During and after Endurance Competitions Dietary concepts as well as single foods, fluids and/or sports supplements should not be
used at the day of competition for the first time. Individual preferences in taste and/or
palatability should be considered to avoid gastrointestinal discomfort and to achieve an
optimal voluntary intake of fluids and nutrients.
3.1. Nutritional Competition Preparation of the Endurance Athlete
Depletion of glycogen stores in liver and muscle are a major cause of fatigue during
endurance exercise (39). Therefore, glycogen status should be optimized before
competition. Increased carbohydrate intake and tapered exercise or rest are a
prerequisite for glycogen storage (40, 41, 42).
Glycogen synthesis is known to follow a biphasic manner, with an initial rapid phase
(insulin-independent, fast rate of glycogen-synthesis during the first 4-24 hours after
exercise) followed by a slow phase (insulin-dependent, slow rate of glycogen synthesis,
up to several days following exercise) (43, 44). Depleted glycogen stores support an
effective glycogen resynthesis (43, 44). Normally, 24 hours of rest accompanied by a
carbohydrate intake of 7-10 g/kg/d are adequate to normalize glycogen stores (45, 46).
There are different carbohydrate loading protocols available to maximize glycogen stores
before events lasting >90 min. The original carboloading protocol, also known as “Saltin
diet” was established in the 1970ies and included a 3-4 days depleting phase (glycogen
depleting exercise combined with low carbohydrate intake) and a 3-4 days loading phase
with tapered exercise and high carbohydrate ingestion (47, 48).Sherman et al. observed
that glycogen supercompensation also occurs within 3-4 days without depleting phase,
when 3-4 days of exercise rest are combined with a high carbohydrate intake (49). More
recently, Bussau et al. observed that one day of rest is sufficient to maximize glycogen
stores, when the carbohydrate intake is ~10 g/kg/d (50).
All these carbohydrate loading protocols are still used by athletes, as all protocols have
advantages and disadvantages. Short carboloading protocols that require exercise rest
may not be suitable for all athletes, especially for those who need a ‘fine tuning’ of
training or an activity stimulus in the days before competition. Others might be afraid of
gaining weight due to excessive carbohydrate consumption over several days, so the
shorter protocol (50) might be more appropriate for those athletes. The original
carboloading protocol by Karlsson and Saltin requires hard training in the week before
competition at already depleted glycogen stores. The decreased training performance due
to low glycogen availability shortly before a competition and the potentially adverse
effects on the immune function (51) are regarded the major disadvantages of this early
protocol.
Recently, a carbohydrate intake of 10-12 g/kg/d for 36-48 hours before competitions
lasting >90 min is recommended (12). Carbohydrate-rich foods and fluids low in fiber
Copyright © by ESPEN LLL Programme 2015 7
and fat spread over several meals and snacks may be helpful to achieve the
carbohydrate intake goals. Performance benefits from carbohydrate loading (i.e.
maintaining the speed at the end of the race) seem to persist even when carbohydrates
are consumed during the competition (52, 53).
For the pre-exercise meal some general aspects should be followed: the meal should
provide sufficient fluids to ensure euhydration before starting the exercise, it should be
low in fat and fibre to reduce gastrointestinal complaints and improve gastric emptying
and should be familiar to the athlete (7). Pre-exercise meals that are ingested 3-4 hours
before competition may have a carbohydrate content of 200-300 g. Depending on the
individual needs and palatability, 1-4 g of carbohydrate per kg body mass 1-4 hours
before exercise are recommended (12). Carbohydrate-rich pre-exercise meals that have
a low glycemic index promote the availability of sustained carbohydrates during exercise
and should therefore be preferred (54).
3.2. Recommendations for Food and Fluid Intake during Endurance Competitions
During endurance events, carbohydrates, fluids and sodium should be ingested
depending on the exercise duration, intensity and environmental conditions.
In the 2009 Joint Position statement of the American College of Sports Medicine, the
American Dietetic Association and the Dietitians of Canada, evidence for performance
benefits is provided (55-56), when endurance athletes consume 0.7 g/kg/h
carbohydrates (~30-60 g/h) during exercise (7). This recommendation takes into
account that the oxidation rate from exogenous glucose is ~ 1 g/min, even at high rates
of intake (57).
However, more recent studies have shown that the carbohydrate oxidation rate may be
increased up to 1.75 g/min, when multiple transportable carbohydrates using different
intestinal transporters are ingested (56). Recently, a mixture of glucose (using sodium-
dependent glucose transporter-1 [SGLT-1]) and fructose (using glucose transporter 5
[Glut5]) is recommended for ingestion during distance events (56).
Maximum carbohydrate oxidation rate form exogenous sources may be achieved by
ingesting glucose and fructose (ratio 2:1) at amounts of 1.8 g/min, i.e. ~70 g/h of
glucose and 35 g/h of fructose during exercise (56). The administration form of the
multiple transportable carbohydrate mixture does not influence the oxidation rate, thus
athletes may combine beverages, carbohydrate bars or gels during long-distance events
(58, 59). Co-ingestion of proteins during endurance exercise seems not to have beneficial
effects on muscle protein synthesis rate (60). To achieve an optimal balance between the
requirements for carbohydrate absorption and fluid delivery, carbohydrate concentration
should range between 5-10 %, with the lower concentration when fluid delivery is more
important than carbohydrate absorption (i.e. in hot and humid environments) (15).
For endurance competitions of shorter duration, the finding that carbohydrate mouth
rinsing improves exercise performance in endurance events lasting 30-75 min may be of
interest. Although the potential mechanisms are not fully understood, there seems to be
a receptor-mediated effect of carbohydrate mouth rinsing on the brain that reduces
fatigue and leads to performance benefits besides the metabolic advantages (61- 63).
However, it seems that carbohydrate ingestion during relatively short (<30 min) high-
intensity exercises does not improve exercise performance (64).
Fig. 1 summarizes recent recommendations for carbohydrate intake during exercise.
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Fig. 1 Carbohydrate intake recommendations for highly-trained, competitive endurance
athletes during exercise (modified from (65)).
3.3 Nutrition for Recovery from Competition or Exhausting Training Sessions
Adequate nutrition may support post-exercise recovery, especially rehydration and
glycogen resynthesis following endurance events with a certain degree of dehydration
and glycogen depletion.
Shirreffs et al. (1997) analysed the effect on fluid restoration of differently concentrated
sodium solutions in amounts equivalent to 50 %, 100 %, 150 % and 200 % of exercise-
induced body mass loss (66). They found that high-sodium solutions (~60 mmol/L or
~1330 mg/L) at amounts of 150 % of body mass loss are most effective in restoration of
fluid losses. Thus, expert panels recommend to ingest 1.5 L of a sodium-containing fluid
for each kg of body mass lost during exercise to support rapid recovery from dehydration
(15). Voluntary drinking after exhausting exercise may be supported by adding palatable
flavour and carbohydrates (19).
Immediate consumption of carbohydrates following glycogen-depleting exercise can
enhance glycogen resynthesis rates (43, 64). A carbohydrate ingestion of 1.2 -1.5 g/h
per kg body mass during the first few hours following exercise was shown to significantly
increase glycogen restoration (43, 68). Although carbohydrates with high glycemic index
(GI) have been supposed to promote glycogen resynthesis (54), more recent studies
failed to show a performance enhancing effect when a high GI recovery diet was
consumed compared to a low GI diet (67). This might be explained by the sufficient
carbohydrate intake during the first few hours after exercise, where glycogen resynthesis
is insulin-independent (see chapter 3.1).
Adding proteins to recovery beverages might be helpful (69-70), although no additional
increase in glycogen resynthesis rate was observed when carbohydrate intake exceeds
1.2 g/kg/h (71). In case a high carbohydrate intake cannot be achieved, a reduced
carbohydrate ingestion (~0.8 g/kg/h) is as effective as 1.0-1.2 g/kg/h carbohydrate,
when ~0.2-0.4 g/kg/h of protein is co-ingested (43, 68).
Exercise duration
30-75 min
1-2 hours
2-3 hours
> 2.5 hours
Carbohydrate intake recommendations during exercise
Mouth rinsing or small amounts of single or multiple transportable carbohydrates
30 g/h of single or multiple transportable carbohydrates.
60 g/h of single or multiple transportable carbohydrates.
90 g/h of multiple transportable carbohydrates (i.e. glucose-fructose mixture with glucose:fructose relation of 2:1)
Copyright © by ESPEN LLL Programme 2015 9
As fat is known to delay carbohydrate absorption due to delayed gastric emptying (72)
post-exercise meals and snacks should be low in fat.
To achieve these nutritional targets, athletes may consume beverages or non-liquid foods
that are rich in carbohydrates, spread over smaller dosages every 15-20 min. A
combination of carbohydrate containing fluids and foods might be a prudent choice to
support muscle glycogen recovery.
3.4. Summary
Supporting rehydration and glycogen resynthesis are the major nutritional goals during
recovery from exercise. Rehydration is most effective when a fluid volume equivalent to
150 % of sweat loss is ingested (i.e. 1.5 L for each kg of body mass lost). Recovery
beverages should be high in sodium to support fluid retention in the body. For the first 2-
4 hours post-exercise, ingestion of carbohydrates at amounts of 1.2-1.5 g/kg/h spread
into smaller dosages (fluids or low-fat snacks) every 15-20 min is recommended. In case
such a high carbohydrate intake cannot be achieved, adding ~ 0.4 g/h of protein (e.g.
milk-based recovery beverage) may support glycogen resynthesis.
4. Dietary Supplements Used by Endurance Athletes
As for the general population, using supplements increases the athlete’s risk to exceed
the tolerable upper level of intake for the given nutrient(s). In addition, supplements
may be contaminated or faked with doping substances, with a worldwide prevalence of
~15 % of supplements containing WADA (World anti-doping association) banned
substances without declaration (73). Despite the risks and contraindications of dietary
and ergogenic supplements used by athletes (73-75), there might be a few supplements
that may be useful for some endurance athletes in certain conditions.
In general, athletes use supplements to support recovery from exercise, to improve
health and performance, to prevent or treat illness and because they believe not to have
a balanced diet. Most often, vitamins, minerals and protein supplements are used (74).
Considering the risks of consuming undeclared WADA banned substances and/or
exceeding tolerable levels of intake, a thorough risk-benefit assessment must be
conducted before using dietary supplements.
4.1. Supplements to Support Macronutrient Intake
In training periods where a high carbohydrate intake is required (chapters 3.1 to 3.3)
athletes might have difficulties to achieve the nutritional goals (76). Here, concentrated
carbohydrate sources (i.e. carbohydrate-rich beverages, gels or bars) can help to
increase carbohydrate intake. Although carbohydrate-rich supplements may not have a
performance benefit compared to meals, athletes might regard them more convenient
(i.e. no effort to prepare a meal, palatable, convenient storage).
For athletes with restricted availability of foods and/or elevated energy demands,
carbohydrate, protein or liquid meal supplements may be helpful during short periods to
achieve the macronutrient and energy requirements.
4.2. Vitamin, Mineral and Vitamin-mineral Supplements
As detailed in chapter 2.3, there is recently no additional micronutrient requirement for
endurance athletes quantified that generally justifies vitamin and/or mineral supplement
use by athletes. In situations where requirements cannot be met by food intake (i.e.
athletes during travelling, in periods of restricted food intake, during training camps with
limited availability of fresh and balanced food or athletes with food intolerances etc.)
vitamin and/or mineral supplements can be considered as a short-term alternative that
should be discussed with a health-professional (i.e. physician, nutritionist) (74).
Copyright © by ESPEN LLL Programme 2015 10
4.3. Ergogenic Aids in Endurance Sports
There are only few dietary supplements that may have ergogenic effects to endurance
athletes, which includes caffeine, buffering substances (i.e. sodium bicarbonate, or
sodium citrate) and creatine.
For caffeine (which was removed from the WADA prohibited list in 2004), a stimulating
effect on fatty acid utilization resulting in a glycogen sparing effect was anticipated (77).
However, more recent data suggest that the primary performance enhancing effect of
caffeine is caused by a reduction of perceived ratings of fatigue and/or to central nervous
system stimulation (78-79). The magnitude of performance benefits increases with
increased duration of the exercise task (79). These performance benefits may be
achieved with relatively small doses of caffeine (1-3 mg/kg body mass) before or during
exercise (80-81). Side effects of caffeine intake (i.e. insomnia, headache, gastrointestinal
complaints or increased urinary flow) should be outweighed before using caffeine as an
ergogenic aid (74).
Buffering agents are used by endurance athletes involved in medium-term (1-60 min),
high-intensity exercise. Ingestion of 0.3-0.5 g/kg sodium bicarbonate or sodium citrate
was shown to have a moderate performance benefit in different endurance sports, with a
positive association between level of acidosis achieved during exercise and beneficial
effects of the buffering agent (82). Side effects (gastrointestinal complaints such as
diarrhoea, cramping) should be considered (7).
Creatine was found to enhance glycogen synthesis and may therefore be helpful in
situations where a fast recovery of glycogen stores is required (83). However, there is no
evidence that creatine supplementation results in performance enhancement in
endurance athletes. In contrast, side-effects such as weight gain may be a contra-
indication for endurance athletes in weight-bearing sports.
4.4. Summary
There is no evidence that endurance athletes have higher macro- or micronutrient
demands that essentially require dietary supplements. Dietary supplements (vitamins,
minerals or macronutrients) may however be a short-term option to achieve dietary
goals in periods where food intake is limited. There is little evidence for ergogenic effects
of supplements in endurance sports, except for caffeine and buffering agents. In the
recent Consensus Statement, the International Olympic Committee (IOC) clearly reveals
that supplements may not compensate for poor food choices and inadequate diets (22).
5. Clinical Issues Concerning the Nutrition of Endurance Athletes
5.1 Weight Management, Female Athlete Triad and Eating Disorders
In both male and female endurance athletes energy intake levels below estimated energy
expenditure has been reported (9, 84-85). Reducing body mass and body fat is often
seen as an competitive advantage by athletes (3, 86).
However, the purpose to reduce body mass for a competitive advantage may result in
dieting and/or in disordered eating or eating disorders. Rosendahl et al. reported a
prevalence of eating disorders in 10 % of endurance athletes (87). In Norway, an
increase of the prevalence of eating disorders among elite athletes from 20 % in 1990 to
28 % in 2002 was observed (86). For athletes, there are different risk factors identified:
predisposing factors (family background, individual factors), precipitating factors (e.g. a
comment on body shape) and perpetuating factors such as initial performance benefits
(88).
Body mass and body composition of elite endurance athletes may vary from those
observed in the general population with lower body mass, body mass index and body fat
content as a result of high exercise-induced energy expenditure (see chapter 1.1).
However, long-term restricted eating or low energy availability may have adverse effects
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Female
athlete triad
Disordered eating /Eating disorder orinadequate food intake, low energy availibility
Amenorrheaor
Subclinical disruptions ofmenstrual cycles
Osteoporosisor
osteopenia, failure to achievepeak bone mass
on both health and performance (88). This includes cardiovascular, endocrine,
reproductive, gastrointestinal and renal disturbances and the central nervous system
(88).
Dieting athletes may slip into disordered eating and severe eating disorders, which in
turn may lead to abnormal menstrual cycles and impaired bone remodelling leading to
premature osteopenia or osteoporosis (86). The term “female athlete triad” denotes the
occurrence of all three symptoms (disordered eating, amenorrhea and osteoporosis, or
subclinical presentations thereof, Fig. 2) (88-89).
The prevalence of the female athlete triad varies between 4-27 % in elite athletes,
depending on whether all three or only two out of three criteria needed to be met for
diagnosis (90). Long-term health consequences (impairment of reproductive function,
premature osteoporosis) may not be excluded.
Fig. 2 Components of the female athlete triad (modified from (89)).
Similar health problems may occur in male endurance athletes with restricted diets.
Rector et al. analysed body fat and bone mineral density in recreational male cyclists and
63% of them were diagnosed with osteopenia (91). To reduce the risk of detrimental
effects on health and performance, athletes should follow a diet and training regime that
ensures an energy availability of 30-45 kcal/kg fat-free mass per day. Here, energy
availability denotes the remaining energy from dietary intake for the body after
subtracting exercise-related energy expenditure (92) (Fig. 3).
Fig. 3 Energy availability to maintain health and performance in athletes
energy intake
Energy spent forexercise
energy availabilty
(without exercise)
Should not fall below30-45 kcal/kg FFM/d
Copyright © by ESPEN LLL Programme 2015 12
5.2. Gastrointestinal Distress (“Runner’s Diarrhoea”)
There is a high prevalence (30-50 %) of gastrointestinal (GI) complaints during long-
distance events reported by runners, triathletes and other endurance athletes (93). The
complaints include stomach or intestinal cramping, vomiting, diarrhoea or nausea (94).
Dehydration, delayed gastric emptying, redistribution of the blood-flow and movements
of the gut during exercise are regarded the main causes for GI complaints during
endurance exercise (94).
To reduce GI distress athletes should be encouraged to consume well-tolerated foods and
fluids low in fat and fibre sufficiently before the onset of exercise. During exercise,
approximately 0.5 L/hour of a beverage containing carbohydrates and sodium is
recommended. To avoid additional delay in gastric emptying, hyperosmolar solutions
should be avoided (94). Carbohydrate concentration in sports beverages should not
exceed 6% (95).
5.3. Hyponatraemia
Exercise-induced hyponatremia (EIH) was reported in marathons and other (ultra-)
endurance events and is characterized by a plasma-sodium level below 135 mmol/l (96 -
99). Incidence of hyponatremia in ultra-endurance events ranges from 0.3% to 27 %
(100).
EIH is a life-threatening condition with symptoms that may be taken for symptoms of
hypoglycaemia, heat stroke, exercise exhaustion or exercise-associated collapse when
laboratory assessment is not available (100). Known causes for EIH include overdrinking
(i.e. drinking in excess of fluid losses via sweat or urinary losses), overexpression of
arginine vasopressin during exercise and inadequate exchange during osmotic and non-
osmotic sodium stores in the body (101). A hot and humid environment, events lasting
>4 hours, female sex, slower finishing times and the use of nonsteroidal anti-
inflammatory drugs are considered additional risk factors for EIH (100).
To prevent EIH, athletes should be advised to follow a moderate hydration regime (~500
ml per exercise hour or less) instead of following old recommendations to drink as much
as tolerable (15, 95). Consuming carbohydrate-electrolyte solutions is recommended
during long-distance events (95). Athletes should avoid gaining weight during exercise
(i.e. avoid overdrinking) (15).
5.4. Iron Deficiency and Iron Deficiency Anaemia
Iron deficiency is the most prevalent nutrient deficiency worldwide. In the literature,
results are controversial whether or not athletes have a higher prevalence of iron
deficiency (102-104) or, in contrast, a better iron status (105 - 106).
Risk factors for iron depletion in endurance athletes include poor iron intake, poor iron
availability (due to high carbohydrate intake), foot strike haemolysis, increased iron loss,
altered intestinal absorption, vegetarian diets, altitude training and female sex (7, 28).
Iron requirements in endurance athletes (esp. runners) may be increased by
approximately 70 % (107).
It is non-controversial that iron deficiency anaemia adversely affects endurance
performance (108 - 109). However, the effect of iron deficiency without anaemia on
exercise performance remains equivocal, at least at early stages of iron depletion (98,
110-111). Athletes at risk should be individually counselled how to increase dietary iron
intake and iron availability from food. Iron supplementation must be supervised by a
health professional. Recently, a regular screening for iron deficiency in endurance
athletes accompanied by a supervised iron supplementation to correct for iron depletion
is recommended (7, 83, 112).
Copyright © by ESPEN LLL Programme 2015 13
5.5. Summary
Prevalence of restricted or disordered eating and eating disorders is high among
endurance athletes, especially among females. The female athlete triad is a symptom
complex consisting of restricted or eating disorders, amenorrhea and osteoporosis and
subclinical presentations thereof. Energy availability (i.e. energy intake – energy spent
for exercise) should not fall below 30-45 kcal/kg FFM/d.
Gastrointestinal complaints are often reported by endurance athletes, esp. in runners. To
reduce gastrointestinal stress, sufficient gaps between food intake and exercise, intake of
well-tolerated foods and fluids and a moderate fluid intake during exercise (~0.5 L /h) is
recommended.
Exercise-induced hyponatremia is a life-threatening condition reported in endurance
events lasting >4 hours. Athletes should be encouraged to temper their fluid
consumption not allowing for weight gain during exercise and to consume sodium
beverages such as commercial carbohydrate-electrolyte drinks.
Iron deficiency and iron deficiency anaemia are common nutrient deficiencies among
athletes, especially females. Athletes at risk should be counselled to increase iron intake
and/or to reduce inhibitors of iron absorption and need to be regularly screened for
depleted iron stores and anaemia.
6. Summary (overall)
Endurance athletes represent a variety of sporting disciplines with different physiological
and metabolic demands. Meeting the energy requirement is the major nutritional goal in
endurance athletes. General carbohydrate needs to avoid glycogen depletion vary from
3-5 g/kg/d during low-intensity training periods, 5-7 g/kg/d in moderate training-periods
to 8-12 g/kg/d in periods of high-intensity high-volume training.
Exercise-induced hyponatremia is a life-threatening condition reported in endurance
events lasting >4 hours. Athletes should be encouraged to temper their fluid
consumption not allowing for weight gain during exercise and to consume sodium
beverages such as commercial carbohydrate-electrolyte drinks.
Both dehydration and sodium loss may be linked to exercise-induced muscle cramps.
Avoiding a dehydration >2 % of body mass by regular ingestion of sodium beverages
(400-1000 mg/L) and/or proper hydration before exercise are recommended.
Supporting rehydration and glycogen resynthesis are the major nutritional goals during
recovery from exercise. Rehydration is most effective when a sodium containing fluid
volume equivalent to 150 % of sweat loss is ingested (i.e. 1.5 L for each kg of body mass
lost). For the first 2-4 hours post-exercise, ingestion of carbohydrates at amounts of 1.2-
1.5 g/kg/h spread into smaller dosages every 15-20 min is recommended.
Requirements for vitamins and minerals seem not to be higher than recommended daily
allowances for sedentary people, except for iron (esp. females) and sodium (esp. in salty
sweaters). Dietary supplements may be contaminated with banned substances and may
not compensate for poor food choices and inadequate diets.
Prevalence of restricted or disordered eating and eating disorders is high among
endurance athletes, especially among females. Energy availability (i.e. energy intake –
energy spent for exercise) should not fall below 30-45 kcal/kg FFM/d to avoid health
consequences such as symptoms of the female athlete triad.
Copyright © by ESPEN LLL Programme 2015 14
7. References
1. Garber CE, Blissmer B, Deschenes MR, et al. American College of Sports Medicine.
American College of Sports Medicine position stand. Quantity and quality of exercise
for developing and maintaining cardiorespiratory, musculoskeletal, and neuromotor
fitness in apparently healthy adults: guidance for prescribing exercise. Med Sci
Sports Exerc 2011;43(7):1334-59.
2. Mettler S, Mannhart C, Colombani PC. Development and validation of a food pyramid
for Swiss athletes. Int J Sport Nutr Exerc Metab 2009;19(5):504-18.
3. O'Connor H, Olds T, Maughan RJ; International Association of Athletics Federations.
Physique and performance for track and field events. J Sports Sci 2007;25 Suppl
1:S49-60.
4. Arrese AL, Ostáriz ES. Skinfold thicknesses associated with distance running
performance in highly trained runners. J Sports Sci 2006;24(1):69-76.
5. Carlsohn A, Scharhag-Rosenberger F, Cassel M, Mayer F. Resting metabolic rate in
elite rowers and canoeists: difference between indirect calorimetry and prediction.
Ann Nutr Metab 2011;58(3):239-44.
6. Laurenson NM, Fulcher KY, Korkia P. Physiological characteristics of elite and club
level female triathletes during running. Int J Sports Med 1993;14(8):455-9.
7. Rodriguez NR, DiMarco NM, Langley S; American Dietetic Association; Dietitians of
Canada; American College of Sports Medicine: Nutrition and Athletic Performance. J
Am Diet Assoc 2009;109(3):509-27.
8. Westerterp KR. Physical activity and physical activity induced energy expenditure in
humans: measurement, determinants, and effects. Front Physiol 2013;4:90.
9. Fudge BW, Westerterp KR, Kiplamai FK et al. Evidence of negative energy balance
using doubly labelled water in elite Kenyan endurance runners prior to competition.
Br J Nutr 2006;95(1):59-66.
10. Barrero A, Erola P, Bescós R. Energy balance of triathletes during an ultra-endurance
event. Nutrients 2014;7(1):209-22.
11. Hill RJ, Davies PS. Energy intake and energy expenditure in elite lightweight female
rowers. Med Sci Sports Exerc 2002;34(11):1823-9.
12. Burke LM, Hawley JA, Wong SH, Jeukendrup AE. Carbohydrates for training and
competition. J Sports Sci 2011;29 Suppl 1:S17-27.
13. Phillips SM, Moore DR, Tang JE. A critical examination of dietary protein
requirements, benefits, and excesses in athletes. Int J Sport Nutr Exerc Metab
2007;17 Suppl:S58-76.
14. Tipton KD, Witard OC. Protein requirements and recommendations for athletes:
relevance of ivory tower arguments for practical recommendations. Clin Sports Med
2007;26(1):17-36.
15. American College of Sports Medicine, Sawka MN, Burke LM et al. American College of
Sports Medicine position stand. Exercise and fluid replacement. Med Sci Sports Exerc
2007;39(2):377-90.
16. Godek SF, Bartolozzi AR, Godek JJ. Sweat rate and fluid turnover in American
football players compared with runners in a hot and humid environment. Br J Sports
Med 2005;39(4):205-11; discussion 205-11.
17. Burke LM, Wood C, Pyne DB, Telford DR, Saunders PU. Effect of carbohydrate intake
on half-marathon performance of well-trained runners. Int J Sport Nutr Exerc Metab
2005;15(6):573-89.
18. Maughan RJ, Shirreffs SM. Development of individual hydration strategies for
athletes. Int J Sport Nutr Exerc Metab 2008;18(5):457-72.
19. Sharp RL. Role of whole foods in promoting hydration after exercise in humans. J Am
Coll Nutr 2007;26(5 Suppl):592S-596S.
20. Stofan JR, Zachwieja JJ, Horswill CA, Murray R, Anderson SA, Eichner ER. Sweat and
sodium losses in NCAA football players: a precursor to heat cramps? Int J Sport Nutr
Exerc Metab 2005;15(6):641-52.
21. Montain SJ, Cheuvront SN, Lukaski HC. Sweat mineral-element responses during 7 h
of exercise-heat stress. Int J Sport Nutr Exerc Metab 2007;17(6):574-82.
Copyright © by ESPEN LLL Programme 2015 15
22. Shirreffs SM, Sawka MN. Fluid and electrolyte needs for training, competition, and
recovery. J Sports Sci 2011;29 Suppl 1:S39-46.
23. IOC consensus statement on sports nutrition 2010. J Sports Sci 2011;29 Suppl 1:S3-
4.
24. Sen CK. Antioxidants in exercise nutrition. Sports Med 2001;31(13):891-908.
25. Margaritis I, Palazzetti S, Rousseau AS, Richard MJ, Favier A. Antioxidant
supplementation and tapering exercise improve exercise-induced antioxidant
response. J Am Coll Nutr 2003;22(2):147-56.
26. van der Beek EJ, van Dokkum W, Schrijver J et al. Thiamin, riboflavin, and vitamins
B-6 and C: impact of combined restricted intake on functional performance in man.
Am J Clin Nutr 1988;48(6):1451-62.
27. van der Beek EJ, van Dokkum W, Schrijver J, Wesstra A, Kistemaker C, Hermus RJ.
Controlled vitamin C restriction and physical performance in volunteers. J Am Coll
Nutr 1990;9(4):332-9.
28. Bjelakovic G, Nikolova D, Gluud C. Antioxidant supplements and mortality. Curr Opin
Clin Nutr Metab Care 2014;17(1):40-4.
29. Gomez-Cabrera MC, Ristow M, Viña J. Antioxidant supplements in exercise: worse
than useless? Am J Physiol Endocrinol Metab2012 15;302(4):E476-7.
30. Ristow M, Zarse K, Oberbach A, et al. Antioxidants prevent health-promoting effects
of physical exercise in humans. Proc Natl Acad Sci U S A 2009;106(21):8665-70.
31. Gomez-Cabrera MC, Domenech E, Romagnoli M, et al. Oral administration of vitamin
C decreases muscle mitochondrial biogenesis and hampers training-induced
adaptations in endurance performance. Am J Clin Nutr 2008;87(1):142-9.
32. Hinton PS. Iron and the endurance athlete. Appl Physiol Nutr Metab
2014;39(9):1012-8.
33. Beard J, Tobin B. Iron status and exercise. Am J Clin Nutr 2000;72(2 Suppl):594S-
7S.
34. Auersperger I, Škof B, Leskošek B, Knap B, Jerin A, Lainscak M. Exercise-induced
changes in iron status and hepcidin response in female runners. PLoS One.
2013;8(3):e58090.
35. Reinke S, Taylor WR, Duda GN, et al. Absolute and functional iron deficiency in
professional athletes during training and recovery. Int J Cardiol 2012 19;156(2):186-
91.
36. Gledhill N, Warburton D, Jamnik V. Haemoglobin, blood volume, cardiac function,
and aerobic power. Can J Appl Physiol 1999;24(1):54-65.
37. Wilkinson JG, Martin DT, Adams AA, Liebman M. Iron status in cyclists during high-
intensity interval training and recovery. Int J Sports Med 2002;23(8):544-8.
38. DellaValle DM, Haas JD. Impact of iron depletion without anemia on performance in
trained endurance athletes at the beginning of a training season: a study of female
collegiate rowers. Int J Sport Nutr Exerc Metab. 2011;21(6):501-6.
39. Ormsbee MJ, Bach CW, Baur DA. Pre-exercise nutrition: the role of macronutrients,
modified starches and supplements on metabolism and endurance performance.
Nutrients. 2014 29;6(5):1782-808.
40. Ivy JL. Muscle glycogen synthesis before and after exercise. Sports Med
1991;11(1):6-19.
41. Jentjens RL, Cale C, Gutch C, Jeukendrup AE. Effects of pre-exercise ingestion of
differing amounts of carbohydrate on subsequent metabolism and cycling
performance. Eur J Appl Physiol 2003;88(4-5):444-52.
42. Robergs RA. Nutrition and exercise determinants of postexercise glycogen synthesis.
Int J Sport Nutr 1991;1(4):307-37.
43. Millard-Stafford M, Childers WL, Conger SA, Kampfer AJ, Rahnert JA. Recovery
nutrition: timing and composition after endurance exercise. Curr Sports Med Rep
2008;7(4):193-201.
44. Jentjens R, Jeukendrup A. Determinants of post-exercise glycogen synthesis during
short-term recovery. Sports Med 2003;33(2):117-44.
45. Burke LM, Collier GR, Beasley SK, et al. Effect of coingestion of fat and protein with
carbohydrate feedings on muscle glycogen storage. J Appl Physiol (1985).
1995;78(6):2187-92.
Copyright © by ESPEN LLL Programme 2015 16
46. Costill DL, Sherman WM, Fink WJ, Maresh C, Witten M, Miller JM. The role of dietary
carbohydrates in muscle glycogen resynthesis after strenuous running. Am J Clin
Nutr 1981;34(9):1831-6.
47. Karlsson J, Saltin B. Diet, muscle glycogen, and endurance performance. J Appl
Physiol 1971;31(2):203-6.
48. Bergström J, Hermansen L, Hultman E, Saltin B. Diet, muscle glycogen and physical
performance. Acta Physiol Scand. 1967;71(2):140-50.
49. Sherman WM, Costill DL, Fink WJ, Miller JM. Effect of exercise-diet manipulation on
muscle glycogen and its subsequent utilization during performance. Int J Sports Med
1981;2(2):114-8.
50. Bussau VA, Fairchild TJ, Rao A, Steele P, Fournier PA. Carbohydrate loading in
human muscle: an improved 1 day protocol. Eur J Appl Physiol 2002;87(3):290-5.
51. Gleeson M, Williams C. Intense exercise training and immune function. Nestle Nutr
Inst Workshop Ser. 2013;76:39-50.
52. Widrick JJ, Costill DL, Fink WJ, Hickey MS, McConell GK, Tanaka H. Carbohydrate
feedings and exercise performance: effect of initial muscle glycogen concentration. J
Appl Physiol (1985). 1993;74(6):2998-3005.
53. Rauch LH, Rodger I, Wilson GR, et al. The effects of carbohydrate loading on muscle
glycogen content and cycling performance. Int J Sport Nutr 1995;5(1):25-36.
54. Siu PM, Wong SH. Use of the glycemic index: effects on feeding patterns and
exercise performance. J Physiol Anthropol Appl Human Sci 2004;23(1):1-6.
55. Coggan AR, Coyle EF. Carbohydrate ingestion during prolonged exercise: effects on
metabolism and performance. Exerc Sport Sci Rev 1991;19:1-40.
56. Currell K, Jeukendrup AE. Superior endurance performance with ingestion of multiple
transportable carbohydrates. Med Sci Sports Exerc 2008;40(2):275-81.
57. Jeukendrup AE, Jentjens R. Oxidation of carbohydrate feedings during prolonged
exercise: current thoughts, guidelines and directions for future research. Sports Med
2000;29(6):407-24.
58. Pfeiffer B, Stellingwerff T, Zaltas E, Jeukendrup AE. CHO oxidation from a CHO gel
compared with a drink during exercise. Med Sci Sports Exerc 2010;42(11):2038-45.
59. Pfeiffer B, Stellingwerff T, Zaltas E, Jeukendrup AE. Oxidation of solid versus liquid
CHO sources during exercise. Med Sci Sports Exerc 2010;42(11):2030-7.
60. Beelen M, Zorenc A, Pennings B, Senden JM, Kuipers H, van Loon LJ. Impact of
protein coingestion on muscle protein synthesis during continuous endurance type
exercise. Am J Physiol Endocrinol Metab 2011;300(6):E945-54.
61. Carter JM, Jeukendrup AE, Jones DA. The effect of carbohydrate mouth rinse on 1-h
cycle time trial performance. Med Sci Sports Exerc 2004;36(12):2107-11.
62. Rollo I, Williams C, Gant N, Nute M. The influence of carbohydrate mouth rinse on
self-selected speeds during a 30-min treadmill run. Int J Sport Nutr Exerc Metab
2008;18(6):585-600.
63. Jeukendrup AE. Carbohydrate and exercise performance: the role of multiple
transportable carbohydrates. Curr Opin Clin Nutr Metab Care 2010;13(4):452-7.
64. Jeukendrup AE, Hopkins S, Aragón-Vargas LF, Hulston C. No effect of carbohydrate
feeding on 16 km cycling time trial performance. Eur J Appl Physiol
2008;104(5):831-7.
65. Jeukendrup A. The new carbohydrate intake recommendations. Nestle Nutr Inst
Workshop Ser. 2013;75:63-71.
66. Shirreffs SM, Taylor AJ, Leiper JB, Maughan RJ. Post-exercise rehydration in man:
effects of volume consumed and drink sodium content. Med Sci Sports Exerc
1996;28(10):1260-71.
67. Moore LJ, Midgley A, Vince R, McNaughton LR. The effects of low and high glycemic
index 24-h recovery diets on cycling time trial performance. J Sports Med Phys
Fitness 2011;51(2):233-40.
68. Beelen M, Burke LM, Gibala MJ, van Loon L JC. Nutritional strategies to promote
postexercise recovery. Int J Sport Nutr Exerc Metab 2010;20(6):515-32.
69. Ivy JL, Goforth HW Jr, Damon BM, McCauley TR, Parsons EC, Price TB. Early
postexercise muscle glycogen recovery is enhanced with a carbohydrate-protein
supplement. J Appl Physiol (1985). 2002;93(4):1337-44.
Copyright © by ESPEN LLL Programme 2015 17
70. Williams M, Raven PB, Fogt DL, Ivy JL. Effects of recovery beverages on glycogen
restoration and endurance exercise performance. J Strength Cond Res
2003;17(1):12-9.
71. van Hall G, Shirreffs SM, Calbet JA. Muscle glycogen resynthesis during recovery
from cycle exercise: no effect of additional protein ingestion. J Appl Physiol (1985).
2000;88(5):1631-6.
72. Collier G, O'Dea K. The effect of coingestion of fat on the glucose, insulin, and gastric
inhibitory polypeptide responses to carbohydrate and protein. Am J Clin Nutr
1983;37(6):941-4.
73. Geyer H, Parr MK, Koehler K, Mareck U, Schänzer W, Thevis M. Nutritional
supplements cross-contaminated and faked with doping substances. J Mass
Spectrom 2008;43(7):892-902.
74. Maughan RJ, Depiesse F, Geyer H; International Association of Athletics Federations.
The use of dietary supplements by athletes. J Sports Sci 2007;25 Suppl 1:S103-13.
75. Carlsohn A, Cassel M, Linné K, Mayer F. How much is too much? A case report of
nutritional supplement use of a high-performance athlete. Br J Nutr
2011;105(12):1724-8.
76. Burke LM, Cox GR, Culmmings NK, Desbrow B. Guidelines for daily carbohydrate
intake: do athletes achieve them? Sports Med 2001;31(4):267-99.
77. Tarnopolsky MA. Caffeine and endurance performance. Sports Med 1994;18(2):109-
25.
78. Davis JM, Zhao Z, Stock HS, Mehl KA, Buggy J, Hand GA. Central nervous system
effects of caffeine and adenosine on fatigue. Am J Physiol Regul Integr Comp Physiol
2003;284(2):R399-404.
79. Doherty M, Smith PM. Effects of caffeine ingestion on rating of perceived exertion
during and after exercise: a meta-analysis. Scand J Med Sci Sports 2005;15(2):69-
78.
80. Cox GR, Desbrow B, Montgomery PG, et al. Effect of different protocols of caffeine
intake on metabolism and endurance performance. J Appl Physiol (1985)
2002;93(3):990-9.
81. Kovacs EM, Stegen JHCH, Brouns F. Effect of caffeinated drinks on substrate
metabolism, caffeine excretion, and performance. J Appl Physiol (1985)
1998;85(2):709-15.
82. Matson LG, Tran ZV. Effects of sodium bicarbonate ingestion on anaerobic
performance: a meta-analytic review. Int J Sport Nutr 1993;3(1):2-28.
83. Robinson TM, Sewell DA, Hultman E, Greenhaff PL. Role of submaximal exercise in
promoting creatine and glycogen accumulation in human skeletal muscle. J Appl
Physiol (1985) 1999;87(2):598-604.
84. Beals KA, Manore MM. Nutritional status of female athletes with subclinical eating
disorders. J Am Diet Assoc 1998;98(4):419-25.
85. Drinkwater BL, Nilson K, Chesnut CH 3rd, Bremner WJ, Shainholtz S, Southworth
MB. Bone mineral content of amenorrheic and eumenorrheic athletes. N Engl J Med
1984;311(5):277-81.
86. Sundgot-Borgen J, Torstveit MK. Aspects of disordered eating continuum in elite
high-intensity sports. Scand J Med Sci Sports 2010;20 Suppl 2:112-21.
87. Rosendahl J, Bormann B, Aschenbrenner K, Aschenbrenner F, Strauss B. Dieting and
disordered eating in German high school athletes and non-athletes. Scand J Med Sci
Sports 2009;19(5):731-9.
88. Nattiv A, Loucks AB, Manore MM, et al. American College of Sports Medicine position
stand. The female athlete triad. Med Sci Sports Exerc 2007;39(10):1867-82.
89. De Souza MJ, Williams NI. Physiological aspects and clinical sequelae of energy
deficiency and hypoestrogenism in exercising women. Hum Reprod Update
2004;10(5):433-48.
90. Torstveit MK, Sundgot-Borgen J. The female athlete triad exists in both elite athletes
and controls. Med Sci Sports Exerc 2005;37(9):1449-59.
91. Rector RS, Rogers R, Ruebel M, Hinton PS. Participation in road cycling vs running is
associated with lower bone mineral density in men. Metabolism 2008;57(2):226-32.
Copyright © by ESPEN LLL Programme 2015 18
92. Loucks AB, Kiens B, Wright HH. Energy availability in athletes J Sports Sci 2011;29
Suppl 1:S7-15.
93. Rehrer NJ, Beckers EJ, Brouns F, ten Hoor F, Saris WH. Effects of dehydration on
gastric emptying and gastrointestinal distress while running. Med Sci Sports Exerc
1990;22(6):790-5.
94. de Oliveira EP, Burini RC. Food-dependent, exercise-induced gastrointestinal distress.
J Int Soc Sports Nutr 2011 28;8:12.
95. Jeukendrup AE, Currell K, Clarke J, Cole J, Blannin AK. Effect of beverage glucose
and sodium content on fluid delivery. Nutr Metab (Lond) 2009;6:9.
96. Almond CS, Shin AY, Fortescue EB et al. Hyponatremia among runners in the Boston
Marathon. N Engl J Med. 2005;352(15):1550-6.
97. Speedy DB, Noakes TD, Rogers IR, et al. Hyponatremia in ultradistance triathletes.
Med Sci Sports Exerc 1999;31(6):809-15.
98. Holtzhausen LM, Noakes TD, Kroning B, de Klerk M, Roberts M, Emsley R. Clinical
and biochemical characteristics of collapsed ultra-marathon runners. Med Sci Sports
Exerc 1994;26(9):1095-101.
99. Noakes TD, Norman RJ, Buck RH, Godlonton J, Stevenson K, Pittaway D. The
incidence of hyponatremia during prolonged ultraendurance exercise. Med Sci Sports
Exerc 1990;22(2):165-70.
100. Hsieh M. Recommendations for treatment of hyponatraemia at endurance events.
Sports Med 2004;34(4):231-8.
101. Beltrami FG, Hew-Butler T, Noakes TD. Drinking policies and exercise-associated
hyponatraemia: is anyone still promoting overdrinking? Br J Sports Med
2008;42(10):796-501.
102. Dubnov G, Constantini NW. Prevalence of iron depletion and anemia in top-level
basketball players. Int J Sport Nutr Exerc Metab 2004;14(1):30-7.
103. Diehl DM, Lohman TG, Smith SC, Kertzer R. Effects of physical training and
competition on the iron status of female field hockey players. Int J Sports Med
1986;7(5):264-70.
104. Sinclair LM, Hinton PS. Prevalence of iron deficiency with and without anemia in
recreationally active men and women. J Am Diet Assoc 2005;105(6):975-8.
105. Risser WL, Lee EJ, Poindexter HB, et al. Iron deficiency in female athletes: its
prevalence and impact on performance. Med Sci Sports Exerc 1988;20(2):116-21.
106. Nuviala RJ, Castillo MC, Lapieza MG, Escanero JF. Iron nutritional status in female
karatekas, handball and basketball players, and runners. Physiol Behav
1996;59(3):449-53.
107. Whiting SJ, Barabash WA. Dietary Reference Intakes for the micronutrients:
considerations for physical activity. Appl Physiol Nutr Metab 2006;31(1):80-5.
108. Gardner GW, Edgerton VR, Senewiratne B, Barnard RJ, Ohira Y. Physical work
capacity and metabolic stress in subjects with iron deficiency anemia. Am J Clin Nutr
1977;30(6):910-7.
109. Haas JD, Brownlie T 4th. Iron deficiency and reduced work capacity: a critical
review of the research to determine a causal relationship. J Nutr 2001;131(2S-
2):676S-688S.
110. Peeling P, Blee T, Goodman C, et al. Effect of iron injections on aerobic-exercise
performance of iron-depleted female athletes. Int J Sport Nutr Exerc Metab
2007;17(3):221-31.
111. Zhu YI, Haas JD. Response of serum transferrin receptor to iron supplementation
in iron-depleted, nonanemic women. Am J Clin Nutr 1998;67(2):271-5.
112. Ljungqvist A, Jenoure P, Engebretsen L, et al. The International Olympic
Committee (IOC) Consensus Statement on periodic health evaluation of elite athletes
March 2009. Br J Sports Med 2009;43(9):631-43.