Nutritional needs in the professional practice of swimming: a review

[Purpose] Swimming requires developing a high aerobic and anaerobic capacity for strength and technical efficiency. The purpose of this study was to establish the nutritional requirements and dietary strategies that can optimize swimming performance. [Methods] Several related studies retrieved from the databases, Dialnet, Elsevier, Medline, Pubmed, and Web of Science, through keyword search strategies were reviewed. [Results] The recommended carbohydrate intake ranges between 6-10-12 g/kg/d, protein 2 g/kg/d, and fat should surpass 20-25% of the daily intake. [Conclusion] Performance can be optimized with a hydration plan, as well as adequate periodization of supplements, such as caffeine, creatine, sodium bicarbonate, B-alanine, beetroot juice, Vitamin D, bovine colostrum, and HMB.


Journal of Exercise Nutrition & Biochemistry
With the goal of maximizing the high energy phosphagen system in swimming, it is necessary to develop a specific high-intensity training program 8 , as well as one focused on improving maximal oxygen consumption (VO2max). In addition to interval training sessions to help improve the high energy phosphagen metabolism, the anaerobic glycolysis, and the VO2max, the swimmers must perform continued long duration with low-intensity training, in order to improve both the efficiency and efficacy of their swimming technique 1 .
During longer distance competitions 9 and interval training sessions 10 , the glycogen stores in the muscles can be depleted, possibly causing a decrease in performance, and consequently lowering training adaptation. Furthermore, there may be a resulting increase in proteolysis 11 , compromising nitrogen balance, propulsive strength capacities, and the super compensation processes.
It has been suggested that by identifying the limiting factors of performance in a sport modality, like swimming, nutritional strategies and goals can be developed, to help establish a nutritional intervention plan for the sport 12 . An adequate nutritional and supplementation plan, that takes into account the characteristic of the sport modality, can help improve the health and performance of the athletes 13 . The aim of this review is to establish nutritional objectives and strategies to help optimize swimming performance by identifying factors that limit performance in swimming.

METHODS
The present literature review has been performed after thorough search of the following databases: Dialnet, Elsevier, Medline, Pubmed, and Web of Science through keyword search strategies. The terms included in the browsers can all be found in the Thesaurus Medical Subject Headings (MeDH) developed by the U.S. National Library of Medicine. The terms were: swim, swimmer, swimming, and aquatic sport in combination with supplement, nutrition, sport nutrition, and ergogenic aids.

Energy requirements and macronutrients
One of the main focuses in swimming training is high volume training 3 that includes 1-3 daily sessions. Training sessions are performed both in the pool and on land with strength training, core, or cross training 14 .
Occasionally, the high training volume results in below adequate energy intake for the swimmer to maintain adequate energy balance, with intake that can reach the 2400 kcal/day on extreme training periods 15 . It is worth mentioning here, that energy deficits maintained for long periods of time, could result in decreased basal metabolic rate, cause alterations in hormonal functions, disrupt menstrual cycles in women, as well as increase the risk of injury and disease 16,17 . It has recently been found that high level female swimmers who experience menstrual dysfunctions show a decrease in thyroid hormones and growth factors, coupled with a decrease in speed in the 400-m test after a 12-week training period 18 .
Regarding carbohydrate intake, it is necessary to point out that a 10% reduction in daily carbohydrate intake has been shown to lower performance in a 365-m freestyle test in swimmers, while an increase of 10% led to improvements in both tests of 91.5 and 365 m 19 . Although these results may suggest a need to follow a diet rich in carbohydrates, it is worth highlighting another study that did not observe any differences in performance among a group of swimmers who followed a diet of 6 g/kg/day compared to a 12 g/kg/day carbohydrate diet intake, after following a moderate training volume 20 . Carbohydrate requirements should be periodized according to training demands [14]. Beginning a training session with low carbohydrate availability (due to low carbohydrate intake since the last training session), causes a higher metabolic stress that can optimize training adaptations 3, 16 , as long as the training sessions are of moderate intensity.
Therefore, for athletes who follow a moderate-to high-intensity training program, carbohydrate intake should be kept in ranges of 6-8 g/kg/day on days when training sessions are of high volume and low intensity, or high intensity and very low volume. On days of moderate or high volume with high intensity, carbohydrate intake should be 10-12 g/kg/day 21 . It is important to point out that when engaging in high intensity sessions with the recommended amount of carbohydrate intake, it will keep the immune system in a better state through an increase in the salivary immunoglobulin response 22 , decreasing the risk of respiratory tract infection 23 . However, these general recommendations should be fine-tuned with individual consideration of total energy needs, specific training needs, and feedback from training performance Recommendations for carbohydrate timing are the same as in other sport modalities, except before high-intensity sessions, where training sessions require high CHO-availability 3 . Following the recommendations of other sports modalities, it could be recommended that 200-300 g 24 or 1-2 g/kg be consumed 3-4 hours prior to the training sessions 25 . Carbohydrates, especially high on the glycemic index must not be ingested 45 minutes prior to exertion, to avoid reactive hypoglycemia 26 .
Carbohydrate intake during exercise favors glycogen oxidation in the muscle, keeping blood sugar levels stable, while preserving glycogen stores during longer periods of time, and avoiding protein catabolism 27 . Therefore, carbohydrate intake during high-intensity training sessions should be favored with intakes up to 90 g/hour 28 in a 2:1 ratio of glucose and fructose 29 .
Studies have shown that open water competitions have the capacity to deplete muscle glycogen storages 9 . Because intake of carbohydrates during competition is difficult, athletes are recommended to eat a super-compen-sation carbohydrate diet 10 . Athletes should consume 10-12 g/kg/day of carbohydrates 48 hours prior to a competition, the same amounts as recommended prior to high-intensity interval sessions 30 . Then, 4 hours before a competition the intake should be at 1-4 g/kg/ day.
Protein requirements for the athletes range between 1.2-2 g/kg/day 31 . Due to the strength requirements in swimming, the recommended intakes should be on the higher limit that is 2/g/kg/day. The dietary protein intake, which only provides a very small amount to the energy metabolism, especially in situations where glycogen stores are depleted 3, 16 , is necessary for the synthesis of new myofibrillar tissue, as a response to strength training, as well as sarcoplasmic, and mitochondrial proteins in response to endurance, and interval training 32 .
It must be emphasized, that the protein food must be of high bioavailable value, and protein timing must be prescribed in relation to the exertion effort 16 . With the aim of optimizing protein synthesis in swimmers, an intake of 0.3 g/kg of high bioavailable protein must be consumed after finishing a competition, strength training, or interval training session 14 .
It should be noted, that amounts higher than 0.3 g/kg do not increase the protein synthesis rate 33 . Additionally, athletes should be encouraged to ingest this amount of protein in 4-5 times during the day 34 . These recommendations are based on a study that showed a higher protein muscle synthesis response when athletes consumed 4 intakes of 20 g of high-quality protein in 3-hour intervals after training, compared to 2 intakes of 40 g or 8 intakes of 10 g in similar conditions 34 . However, it is important to note that these studies were not in aquatics sports.
Regarding nutrient timing, especially carbohydrate intake, it must be noted that after 2-4 hours of training, a higher muscular glycogen resynthesis potential exists, thanks to a higher sensitivity to insulin action during this period, together with a higher activity of the glycogen synthase enzyme activation 35 . The activation occurs because of the increment in the presence of calcium from the successive action potentials that take place during the effort 36 . The higher glycogen synthesis rate takes place when carbohydrates intake reaches 1 g/kg/hour 3, 16 . When the goal between training sessions is to recover muscle glycogen stores, as well as favor protein synthesis, 1 g/kg of carbohydrate together with 20-25 g of protein should be ingested 36 . On the contrary, when the goal of the training sessions is to achieve maximal efficacy of fat and carbohydrate metabolism, 0.3 g/kg of protein alone should be consumed. Lower amounts of carbohydrates (6-8 g/kg/day versus 10-12 g/kg/day) should also be consumed, once the period of glycogen synthesis is promoted, which will cause incomplete muscle glycogen stores. The state of incomplete muscle glycogen storage is optimal for lower intensity sessions 37 , due to the fact that the transcription of genes that underlie the trainings gets favored, with the objective of improving fat and carbohydrate metabolism efficiency 38 .
Regarding fat intake, we must consider that these, besides their energetic function, play an important immunologic role 39 . In this way, a diet with a low-fat content, can increase inflammatory cytokine levels, decrease antioxidant potential and negatively affect blood lipoprotein levels 40 . The fat content in the diet is adjusted once the protein and carbohydrate content has been adjusted, although, the fat intake should represent at least a 20-25% of the energy intake 13 , since, it would be difficult for diets with lower fat content to reach the essential fatty acids and liposoluble vitamin requirements 41 . Furthermore, as it has been proved an association between the injury rates in women athletes and the lipid intake 42 , it is possible that a deficient fat intake could cause sport injuries, although these data correspond in female runners and non-swimmers.
A diet higher in fat content during periods of high volume and low-intensity training could maximize the contribution and efficiency of fatty acid metabolism during exercise 31, 43 . During low-intensity training session, it would be recommended to increase the intake of fats, up to 35% of daily energy intake. With respect to the type of fatty acids, saturated fatty acids should not exceed 10% of daily energy intake 31 , while the intake of essential and monounsaturated fatty acids should be encouraged 44 (Table  I).

Hydration requirements
Although dehydration during water activities is lower than in other outdoor sports 45 , due to thermoregulation improvement of different mechanisms from sweat as convection and conduction 46 , the hydration needs of swimmers is higher than of the sedentary population 47 . The higher the water temperature is, the higher the water loss in sweat will be 46 .
The first goal with regard to hydration is starting both training sessions and competitions in a euhydration state, which requires the athlete to hydrate in a rate of 5-7 ml/kg 4 hours prior to training, in addition to 3-5 ml/kg in case the athlete does not urinate during that time, or if the color of the urine is dark 48 . The beverage should be cold, because cold beverage intake favors thermoregulation during swimming, especially when the temperature is high 49 .
When the losses of sweat are higher than 2% of body weight, and the amount of time in between training is less than 6-8 hours, it is necessary to establish a specific post training rehydration program 3, 16 . With the goal of optimizing hydration, and water retention (considering that some part will be excreted via diuresis), the amount of water should be equivalent to around 150% of fluid lost during training. Adding sodium to the beverage 3,16 could favor hydric retention, even if the co-ingested with carbohydrates.

Ergogenic Aids
In addition to adhering to an adequate nutrition plan, the intake of some nutritional supplements could favor both the athletes' health status, as well as performance 13 .
Owing to the effect of supplement changes depending on the type of effort and sport modality 50 , some supplements could have an ergogenic effect or show an improvement in performance for water sports. Swimmers are regularly reported to have high rates of supplement use. Even when there is an evidence base for the use of such products, the swimmer is advised to be aware of the appropriate situations and protocols of use, and to take into account the "cost" of products in terms of financial outlay and the small but real risk of an inadvertent doping outcome 51 . The supplements and their effects are presented in Table 2.

Caffeine
Caffeine (1,3,7, trimethylxanthine) is an alkaloid from the family of the methylated xanthines, antagonist of the adenosine receptor 52 . Caffeine intake in the athlete's diet is common, as it is found in a wide variety of foods, such as coffee, tea, chocolate, energy drinks, and gels. Caffeine is quickly absorbed at the intestinal levels 53 , detecting high concentration levels 15-45 minutes post intake, and maximum levels in the blood an hour post intake 54 .
Although studies, like the one published by Costill et al. show how supplementing with caffeine stimulates the rise of fatty acids in the blood, and thereby delaying period within which glycogen storage depletion occurs 55 , there is no sufficient evidence to justify this hypothesis at the moment 56 . Nevertheless, caffeine consumption can cause other side effects that could improve sport performance, as it stimulates the central nervous system due to the adenosine antagonistic effect 53 , increases catecholamine levels 57 , improves muscle contractility 58 , improves action potential 59 , as well as decreases the perceived exertion 60 . Nowadays, caffeine is actually considered a supplement with ergogenic effects both in cardiorespiratory endurance, as well as in strength 61 .
Although there are few studies found on the consumption of caffeine in swimmers, there is evidence that prerace caffeine supplementation may enhance swimming performance 62, 63 , but further studies into swimming sports are required to know the dose and timing of prerace caffeine intake that are effective for swimming events, since recent studies suggest that the ergogenic benefit of taking caffeine alone for repeated 200-m swimming performance appears limited 64 .
There is some evidence from endurance sports protocols that small to moderate doses of caffeine (1-3 mg/kg) are as effective as larger doses (5-6 mg/kg) in achieving benefits and may reduce risk of side effects 51 . Recently, Goods et al. had concluded that, a moderate dose of caffeine (3 mg/kg) ingested 1 h before a repeat sprint freestyle set significantly improves mean sprint time in elite swimmers, and the combination of at least a moderate dose of caffeine (>3 mg/kg) with trained athletes appears the most likely to result in ergogenic benefit to anaerobic exercise performance 65 .
Caffeine may be consumed in drinks or as an ingredient in some sport products (e.g., some gels). In this way, a recent study had concluded that a caffeinated energy drink increased some aspects of swimming performance in competitive sprinters, whereas the side effects derived from the intake of this beverage were marginal at this dosage (3 mg/kg) 66 .
Further research is required to determine the precise mechanism(s) responsible for caffeine's ergogenic potential for anaerobic exercise performance.

Creatine
The purpose of supplementing with phosphocreatine is to increase the concentrations of muscular creatine, with the goal of maximizing the resynthesis of ATP through the phosphagen system 8 . This process depends on the availability of muscular creatine 67 . The metabolic pathway will have a great impact on performance, like high-intensity training carried out in most sports. During high-intensity training, creatine supplementation allows for higher training loads, which leads to higher training adaptations 8 .
Studies conducted specifically with the swimming population, showed that the supplementation of 20 g/day over 6 days, did not achieve any improvement in a group of trained swimmers, in a test of 6 x 50 m 68 , or with a 25 g/kg supplementation during 4 days in a test of 10 x 50 m 69 . A literature review therefore concluded that there was not enough evidence to recommend supplementing with creatine to improve performance in swimming tests, although it could improve performance during interval session in the swimming pool 70 . The most likely benefits for swimmers come from using creatine in the training phase to enhance training adaptations to interval and resistance training. However, while there are studies that report an enhancement of the performance of such sessions in highly trained swimmers 71 , there is some controversy about it at the moment 72 .
Nevertheless, because a higher quality in training means higher adaptation, creatine could be useful for water sports, especially during periods of high intensity training. The recommended dosage is 3 g/day, since it showed the same effects in 4 weeks with a load protocol of 5 days (20-30 g/day), followed by maintenance dosage of 3 g/ day, compared to continued intake of 3 g/day 73 , although this should be studied in swimmers.

Sodium bicarbonate
The increase in H+ derived from lactic acid dissociation, leads to a decrease in blood and muscle pH 74 , disturbing the glycolytic rate 75 , the uptake and reuptake of calcium in the sarcoplasmic reticulum 76 , decreasing the contractile speed, while at the same time, causing perceived exertion to increase 77 . These mechanisms aim to decrease the glycolytic contribution to metabolism, most likely as a defense mechanism facing a hypothetic extreme acidosis situation. Supplementing with sodium bicarbonate allows the release of H+ ions into the bloodstream, avoiding a situation of extreme acidosis in the intracellular compartment, which could inhibit muscular contractions 78 , thus considering it as the main regulating agent of the acid-base balance at the extracellular level 51 . It has been shown that supplementing swimmers with sodium bicarbonate, increases levels of sodium bicarbonate and pH in the blood, increases performance in 50-m swim tests 79 , 200 m 80 , successive sets of freestyle 100 m 81 , and increases the average time in a 4-repetition set of freestyle 50-m swim 79 . Since supplementing with sodium bicarbonate can increase performance of repeated sprints 81,82 , it could also improve the quality of trainings, allowing the body to adapt 3. The acute use of bicarbonate to increase extracellular buffering capacity (300 mg/kg 1-2 hour prerace) might enhance the performance of 200-800 m swimming events via increased tolerance to the production of H+ ions via anaerobic glycolysis 51 . Further field studies are needed with high-level swimmers since the few available studies show controversies 64, 83, 84 .

β-alanine
The main purpose of supplementing with b-alanine is to increase muscular carnosine levels. The synthesis of carnosine depends on the bioavailability of the dietary intake of b-alanine 85 . Carnosine, just like sodium bicarbonate, plays an important role with pH regulation, but acts differently than sodium bicarbonate, in that it acts at an

NUTRITIONAL NEEDS IN THE PROFESSIONAL PRACTICE OF SWIMMING
Journal of Exercise Nutrition & Biochemistry intracellular level 86 . In addition to its acid base regulation effect, carnosine has also shown to improve performance, through improving the Myosin ATPase activation 87 , as well as improve calcium sensibility on muscular fibers 88 because of its antioxidant function 89 .
In swimmers, chronic supplementation with B-alanine to increase muscle carnosine, an intracellular buffer, may provide an alternative or additive strategy to support training adaptations and race performance 51 . In a 4-week study performed on swimmers, the effect of 300 mg/kg of sodium bicarbonate, and 4.8 g/day of b-alanine in two tests of 100-m freestyle showed, that b-alanine alone did not affect performance, while the supplementation of b-alanine with sodium bicarbonate did improve performance on the second set of 100 m 81 . It should be noted that even though b-alanine did not show an increase in performance, the recommended dosage is 6.4 g/day, for a period of 4-6 weeks 90 , which is higher than what was used during the study. In relation to this, another study with highly trained swimmers who were supplemented with 6.4 g/day of b-alanine for 5 weeks, showed positive effects on performance in 100 m, and a tendency to improve in 200 m freestyle 91 .
It is, therefore, recommended to supplement 6.4 g/day of b-alanine for 4 or 6 weeks taken in 4-8 dosages of 0/8-1/6 g, with the aim of avoiding the main secondary effect from the supplement (paresthesia) 90 .

Nitrate
The intake of 300-400 mg/day of nitrate, in the form of sodium nitrate 92,93 , or beetroot juice (6-8 mmol of nitrate) 94 , has demonstrated a doubling or tripling of nitrate plasma levels. The increase in nitrate plasma levels can lead to a simultaneous increase of nitric oxide levels, which regulates the muscle blood flow, as well as regulates the mitochondrial respiration 82 . Supplementing with nitrate has shown to decrease VO2, for the same intensity effort 92 . Supplementing with nitrate decreases the magnitude of the slow component of the VO2 95,96 , increasing the time until exhaustion at submaximal intensities 97 .
Although no studies on nitrates on aquatic spot modalities exist, it is feasible to assume that for these athletes who require a lower VO2 when employing a specific power output level, this supplement could have an ergogenic effect. This can especially be of importance in aquatic sports where a higher time in apnea (synchronized swimming) or swimming tests of longer distances in swimming pools or open waters is required. It is, therefore, recommended to supplement with nitrate salts, or beetroot juice (6-8 mmol of nitrate) in the 150-180 minutes prior to training sessions 98 .

Vitamin D
Vitamin D has multiple functions related to sports performance, bone remodeling being one of them 99 , improving muscle contractions, synthesizing new muscle proteins, as well as enhancing immune function 100 .
A study found that one third of a group of high perfor-mance swimmers had low serum levels of this vitamin, placing aquatic sports athletes at risk of developing hypovitaminosis 100 . It may be caused due to limited sun light exposure, as most of the training takes place in indoor facilities, and high-level athletes usually dedicate the rest of the day to sedentary activities to aid recovery. This may explain the lower levels of serum vitamin D particularly found in swimmers, compared other sport modalities that train outdoors 101 .
Owing to the fact that optimal levels of vitamin D are linked with higher bone mineral density 102 , it is assumed that this vitamin is important for optimal bone mineral density 99 ; therefore, lower levels of this vitamin could place the athlete at risk of injuries 39 . To avoid the negative effects on performance that are associated with a deficit of this vitamin 10 , swimmers should periodically check their serum levels in case supplementation is necessary if presented with suboptimal levels, and consume doses 10 µg/ day approximately 100-103 .

Bovine colostrum
Bovine colostrum is the milk produced by cows after they give birth to their calves, and it is known as a substance rich in immunoglobulins and growth factors 104 . Because aquatic sports athletes frequently suffer from respiratory tract infections, it has been proposed that supplementing with bovine colostrum could improve the immune system, decreasing the risk of immunosuppression, and respiratory tract infections 39 .
In some studies, supplementation with bovine colostrum has demonstrated improvements in performance in cardiorespiratory endurance tests 105,106 , as well as speed and strength 107 . On the contrary, other research could not prove positive effects supplementing with bovine colostrum on strength or speed performances 108 .
Improvements in performance study were observed in a 12-minute cycloergometer test after ingesting 20 g/day of bovine colostrum compared to 60 g/day 106 , and thus, it is feasible to suggest supplementing with 20 g/day of bovine colostrum, with the goal being to improve the immune function, and possibly improving performance.

β-hydroxy-βmethylbutyrate
β-hydroxy-βmethylbutyrate (HMB), is a bioactive metabolite formed from the decomposition of leucine, an essential branched-chain amino acid 109 . Although the body has the ability to synthesize HMB, the amount of leucine necessary to synthesize 3 g of HMB is 60 g of leucine, which would amount to 600 g of high biological value protein 110 . The most important function of HMB for athletes is its anti-catabolic effect, improving protein synthesis, and inhibiting proteolysis 111 . Research has demonstrated that supplementing with 3 g/day of HMB during high-intensity training sessions and/or during short periods of recovery in between training sessions, as could be in some aquatic sports modalities, can improve performance. The supplement has shown to improve health, performance, as well as increasing muscle strength 111-113 .

Conclusions
High-level performance swimmers have a high energy expenditure, due to high training volume that they must try to balance with adequate energy intake. Dietary intake of carbohydrates should range between 6 g/kg/ day on days of low-intensity training, and 10-12 g/kg/ day on the days prior to high-intensity training sessions. Dietary protein intake should be at 2 g/kg/day for swimmers, while fat should be consumed at 20-25% of daily energy intake on days of high-intensity training, and 30-35% on days of high volume and low-intensity training. In addition to having an adequate hydration plan in place before, during, and after training to help improve performance, and aid in recovery, the implementation of supplements at the right dosage, can enhance the athlete's health, performance, and recovery. These include, caffeine, creatine, sodium bicarbonate, B-alanine, beetroot juice, vitamin D, bovine colostrum, and HMB.

Limitations
Although most of the nutritional guidelines recommended in this article have been extracted from swimmer articles, some of these recommendations are not from swimming studies and are from a limited case in swimming. These limitations result from an inadequate sample in sex, age, training status, and sports modalities.