Effects of taurine supplementation in elite swimmers performance

Abstract

AIM

Taurine is considered a semi-essential amino acid characterized by having various physiological functions in the body that modulate mechanisms of action involved in the muscle contraction process, increased energy expenditure, insulin signaling pathway, carbohydrate metabolism, and scavenging free radicals. These functions are crucial for aerobic exercise performance; thus, taurine supplementation may benefit athletes’ performance. The objective of this study was to evaluate the effects of taurine supplementation on the resting energy expenditure and physical performance of swimming athletes.

METHODS

In a double-blind study, 14 male swimmers were randomized into two groups: the taurine group (n = 7) and the placebo group (n = 7), which received 3 g per day of taurine or placebo in capsules during 8 weeks. Resting energy expenditure, plasma taurine, physical performance, anthropometry, dietary consumption were measured and an incremental test was performed to determine their maximal front crawl swimming performances before and after the 8-week period.

RESULTS

The levels of serum taurine (p < 0.0001) and lactate (p = 0.0130) showed a significant increase in the taurine group; however, the other variables were not different. No changes were observed in the resting energy expenditure, mean speed performed, and the anaerobic threshold of the swimmers post-supplementation period.

CONCLUSION

Supplementation of taurine increased plasma concentrations of this amino acid, but did not lead to significant changes in food intake, rest energy expenditure, and athletes’ performance. However, the supplemented group presented a higher lactate production, suggesting a possible positive effect of taurine on the anaerobic lactic metabolism.

Keywords
anaerobic lactic metabolism; energy expenditure; swim

Introduction

Taurine (2-aminoethanesulfonic acid) is a non-essential amino acid found in abundance in mammalian cells, which is synthesized from other sulfur-containing amino acids such as methionine and cysteine. Although taurine can be obtained by endogenous synthesis, there are reports in the literature showing the endogenous production is insufficient for attending the body requirement of taurine. This non-essential amino participates in numerous biological and physiological functions like regulation of calcium homeostasis in both skeletal muscle and cardiac tissue ¹,², increases muscle force³ and insulin sensitivity⁴, improves energy expenditure⁵ and lipid metabolism⁶ and prevents oxidative stress in athletes⁷. Therefore, taurine must be obtained by food intake and can be found mainly in fish and seafood². This amino acid does not participate in the process of protein synthesis².

Among the functions related to taurine is the regulation of intracellular calcium levels (Ca²+), membrane stabilizing²,⁸, antioxidant⁷,⁸ and anti-inflammatory processes⁹,¹⁰. Taurine can modulate glucose metabolism potentiating the hepatic and muscular insulin signaling pathways^4,11. Also, this amino acid modulates the use of lipids, stimulating the expression of genes related to the production of the following enzymes: lipoprotein lipase, acyl-CoA oxidase, acyl-CoA synthase, and acyl-CoA dehydrogenase, which are involved in the metabolism of lipid substrates⁵.

Due to the several effects attributed to the action of taurine in the body, some investigations tried to understand the relationship between this nutrient and physical exercise. According to Bakker and Berg¹², taurine can increase the transport of calcium to myofibrillar contractile proteins, optimizing skeletal muscle function, with consequent benefits to athletic performance. Acute supplementation of 6 g/day of taurine for seven days significantly increased the time to exhaustion, maximum workload, and maximal oxygen uptake (VO₂ max) on a cycle ergometer, and reduced the oxidative stress markers¹³. Yatabe, Miyakawa, Miyazaki, Matsuzaki, Ochiai¹⁴ evaluated the taurine concentrations in the skeletal muscles of rats and their time to exhaustion after endurance running. The authors found that 0.5 g/kg/day of taurine increased physical strength in the supplemented group.

In swimming, the contribution of the aerobic metabolism to a maximal effort of 400 m may range from 25 to 83% of total energy and can be influenced by maximal oxygen uptake, metabolic thresholds and peak speed performed^{15, 16}. Thus, the use of taurine supplementation may oppose the possible overproduction of reactive oxygen species (ROS). Since other investigations described nutritional inadequacies in competitive swimmers that result in losses of recovery time and performance^{17, 18}, some attention must be given to the provision of adequate energy intake of both macronutrients and micronutrients¹⁹.

Considering taurine supplementation has potential effects on energy metabolism and muscle contraction strength, we hypothesize that its use as an ergogenic resource will benefit swimmers’ performance, especially those performing efforts of 400 m. Thus, the primary aim of the present investigation was to evaluate the effects of taurine supplementation on the resting energy expenditure and physical performance of swimmers.

Methods

Participants

The volunteers participating in the present study were 14 male swimmers with 18-25 years of age, the weight of 78.6 ± 5.8 kg, the height of 180.0 ± 4 cm, and a body mass index (BMI) of 24.1 ± 0.6 kg/m². All volunteers were from the elite competitive swim team of Ribeirão Preto city. These athletes regularly trained two to three hours per day during a particular training period and were competitive swimmers with a minimum of 3 years of experience at regional and/or national competition level. Each participant gave a written consent before the start of the study. The inclusion criterion was based on their participation for at least two consecutive years in national competitions. Also, they were not using any medication at the time of the research. The present study was approved by the Human Subject Committee of the Faculty of Pharmaceutical Sciences, Food and Nutrition Department / Food and Nutrition Postgraduate Program- São Paulo State University (protocol nº 00526312.9.0000.5426).

Trial design

A double-blind and randomized study was conducted. The subjects were divided randomly into two groups: the placebo group (n = 7) and the taurine group (n = 7). The taurine group received 3g of taurine per day⁷,²⁰, while the placebo group received 3g of starch flour, which was identical in appearance to taurine capsules.

After a fasting period of 8h, each volunteer was to the University Hospital of Ribeirão Preto to measure resting energy expenditure by indirect calorimetry, plasma taurine and anthropometric measurements. Also, guidelines were given to complete the three-day food register. These evaluations were performed before and after eight weeks of placebo or taurine supplementation.

Supplementation protocol

The participants were instructed to intake 3 grams of pure taurine⁷,²⁰ or placebo, which refers to 3 capsules containing 1g of the supplement, every day in the morning before breakfast, during an eight-week period. The taurine powder was obtained from Ajinomoto (Aminoethylsulfonic Acid, Ajinomoto R, São Paulo, SP) and the capsules were manipulated by the Department of Industrial Pharmacy of the School of Medicine of Ribeirão Preto, University of São Paulo. Swimmers were instructed to avoid taurine food sources such as fish, seafood, and energy drinks during the study protocol.

Nutritional assessments

Dietary intake was assessed using three-day dietary records. The records were filled by the volunteers on 2 weekdays and 1 weekend day. The software DietPro 5.1 (A.S. Sistemas, Viçosa, MG, Brazil) was used to quantify the intake of macronutrients and total energy of athletes.

Measurement of resting energy expenditure

The resting energy expenditure (REE) was determined by indirect calorimetry. The subjects were instructed to breathe immediately into a face mask (Hans Rudolph, Kansas City, MO, USA) connected to a breath-by-breath gas analyses system Medics Calorimeter® (SensorMedics Corporation, Yorba Linda, California, USA). After a fasting period of 8h, the athletes were evaluated during the 30-minute test¹⁸. The values with variations higher than 10% were not used. Also, the average of the values of oxygen uptake (VO₂) and carbon dioxide elimination (VCO₂) was used to calculate energy expenditure according to Weir’s formula²¹.

Plasma taurine assay

The concentrations of plasma taurine were determined by high-performance liquid chromatography (Shimadzu model LC 10AD) using a Shimadzu Model RF-535 fluorescence detector. Taurine 99 % was used as standard (Sigma-Aldrich, St. Louis, MO, USA)²².

Performance test protocol

After 15 min of warm-up (i.e., 500m of low and moderate intensity), the swimmers randomly performed three 400-m front-crawl submaximal efforts with 3 min of passive recovery in between and in intensities corresponding to 85, 90, and 100% of the maximum velocity obtained by the athletes for this swimming distance²³. It is important to point out the maximal velocity for the 400-m swimming distance was measured before and after the 8-week period. The motion-analysis software KinoveaTM (version 0.8.15, available for download at http://www.kinovea.org) was used to analyze performance (time and velocity). The tests were performed in a 25-m swimming pool with a water temperature of 25 ± 1ºC.

Blood samples were obtained from the earlobes in 25 μL heparinized capillary tubes 1min after the end of each effort. Also, after the last effort of 400 m, blood samples were also taken after 3 and 5min to measure peak blood lactate concentrations²³. Blood lactate concentrations were assayed by a lactate analyzer (YSI 2300 Sport, Yellow Spring Instruments, Yellow Springs, Ohio). The swimming intensity corresponding to the 4.0 mM blood lactate concentration was considered as the anaerobic threshold²⁴ and was obtained by the exponential interpolation of the lactatemia vs. swimming intensity curve.

Statistical analyses

Shapiro-Wilk and Levene’s tests were applied to assess normality and homogeneity, respectively. Two-way repeated measures analysis of variance followed by Sidak post hoc test were conducted to compare changes within and between groups (Placebo versus Taurine). In cases of nonparametric distribution, Friedman test was applied. For data with heterogeneous variances, Welch test was conducted. The level of significance was set at p ≤ 0.05 in all analyses and data were expressed as mean ± standard deviation and as confidence intervals graphics.

Results

The plasma taurine concentrations were not different between the studied groups at baseline. After the 8-week period, the taurine group showed a significant increase in plasma taurine (Taurine group pre: 104.75 ± 88.33 nmol/L; Taurine group post: 3983.48 ± 768.87 nmol/L, p < 0.0001). Also, compared to the placebo group, the taurine group showed a significant increase of plasma taurine (Placebo group pre: 49.91 ± 8.1 nmol/L; Placebo group post: 174.00 ± 120.29 nmol/L).

Figure 1 shows the parameters assessed by the three-day dietary records. The intake of calories and macronutrients (carbohydrates, proteins, and lipids) was similar between the groups, before and after the period of taurine supplementation.

Figure 1
Evaluation of food intake before (Pre) and after (Post) 8 weeks of placebo or taurine supplementation (n = 14).

Figure 2 shows the values ​​obtained by the indirect calorimetry before and after the intervention period. No significant differences were found between the groups and periods studied.

Figure 2
Evaluation of REE, VO₂, VCO₂ and QR before (Pre) and after (Post) 8 weeks of placebo or taurine supplementation (n = 14).

Regarding blood lactate concentrations, the taurine group increased all values after the supplementation period. First effort of 400m : F _{(1 , 12)} = 8.161, p < 0.05; Second effort of 400m: F _{(1 , 12)} = 12.007, p < 0.05; Third effort of 400m: F _{(1 , 12)} = 8.423, p < 0.05; 3 min after the third effort of 400m: F _{(1 , 12)} = 49.211, p < 0.05; 5 min after the third effort of 400m: F _{(1 , 12)} = 34.669, p < 0.05) (Figure 3).

Figure 3:
Evaluation of blood lactate concentrations (mmol/L) before (Pre) and after (Post) 8 weeks of placebo or taurine supplementation (n = 14).

Figure 4 shows the mean speed achieved in each effort of 400 m and the anaerobic threshold of the swimmers. No significant changes were observed before and after the supplementation period.

Figure 4
Evaluation of mean speeds (m/s) before (Pre) and after (Post) 8 weeks of placebo or taurine supplementation (n = 14).

Discussion

In this study, we examined the effects of eight weeks of taurine supplementation on energy consumption, resting energy expenditure and swimmers’ performance. The levels of serum taurine and lactate showed a significant increase in the taurine group; however, the other variables were not statistically significant. No changes were observed in the resting energy expenditure, the mean speed achieved in each effort of 400 m, and the anaerobic threshold of the swimmers post-supplementation period.

The plasma taurine concentrations were not different between groups at baseline. However, eight weeks of supplementation of 3g of taurine increased its plasma concentration (p < 0.0001) in 22.89 times compared to the placebo group, which evidenced the effectiveness of the current supplementation protocol. Similar results were found by Galloway, Talanian, Shoveller, Heigenhauser, Spriet²⁵ that used an acute supplementation of 5g of taurine in physically active subjects and detected an increase of approximately 16 times in the plasma taurine concentration compared to the baseline condition. According to Bakker and Berg²⁶, the content of taurine in muscle cells can modulate contractile muscle activity. Therefore, the increase of plasma taurine may be beneficial for the athlete, because can promote the maintenance of muscular integrity.

Adequate energy consumption is essential to maintain the performance, body composition, and health of athletes (American College of Sports Medicine Joint Position Statement)²⁷. Herein, energy intake ranged from 3120 to 3720 Kcal/day, and we did not verify significant differences in total calories and macronutrients consumed between the groups or between the evaluated time periods. Since we did not observe significant changes in body mass, we consider that the energy intake was sufficient to deal with the energy requirements imposed by the total energy expenditure of the athletes. Furthermore, their energy intake attended the nutritional recommendations for athletes suggested by American College of Sports Nutrition²⁷, which refers to 45 kcal/kg of body weight.

Regarding the effects of taurine supplementation on athletes’ performance, Balshaw, Bampouras Barry, Sparks²⁸ observed that the acute use of 1g of taurine in runners improved their time trial performances. However, their oxygen uptake and blood lactate concentrations were not influenced by this dose. The authors considered that the probability that their performance results were associated with the action of taurine was 99.3%, although it was noted that the mechanism of taurine action has not yet been elucidated.

In the current investigation, the mean speeds of the three efforts of 400 m and the anaerobic threshold were not affected by the chronic use of 3g of taurine. However, after the eight weeks of intervention, the taurine group increased the blood lactate concentrations measured after the three efforts of 400 m as well as those measured at the third and fifth minute after the third effort of 400 m. These results suggest that taurine supplementation stimulated the use of the anaerobic lactic metabolism during the efforts of 400 m. Also, despite the increased lactate production, our results showed that the taurine supplemented athletes did not decrease the speed performed even when the lactate production was higher than the placebo group.

Also, Beyranvand, Khalafi, Roshan, Choobineh, Parsa, Piranfar²⁹ evaluated the effects of 1.5 g supplementation for two weeks in seven patients with cardiac insufficiency. The authors observed that the application of an exercise capacity test performed before and after taurine supplementation resulted in a greater ability to perform the exercise, including an increase in time and distance when compared to the control group. Their results suggest that taurine optimized the performance of the test by increasing the tolerance to the effort.

It is well established in the literature that the physiological adaptations of the athlete are highly specific to the nature of the training³⁰. In practical terms, the difference of 0.027 m/s found between the speed attained at baseline and after taurine supplementation could be crucial in athletic performance during competition. In fact, in the last Absolute Brazilian Swimming Championships - Maria Lenk Trophy-2016, the difference in mean speed between the first and second place in the 400 m competition was 0.007 m/s³¹.

Considering that all participants underwent the same training program in the current study, we can hypothesize that the statistical difference observed in the concentration of lactate and the slight alteration in average speed may be associated with taurine supplementation. However, more studies are needed to evaluate the effects of chronic supplementation of taurine on swimmer’s performance to elucidate the mechanisms associated with taurine and increased lactate production as well as the viability of its consumption for enhancing the training capacity of athletes.

Conclusions

The results of this study showed that supplementation of taurine during the eight-week period in elite swimmers did not promote significant changes in rest energy expenditure and 400 m performance; however, there were observed higher levels of blood lactate after all efforts without impairing speed performance. Thus, taurine supplementation may contribute to the anaerobic lactic metabolism. As a practical application, taurine supplementation may allow the performance of training sessions that emphasize the anaerobic lactic metabolism development.

References

• ¹
  De Luca A, Pierno S, Camerino DC. Taurine: the appeal of a safe amino acid for skeletal muscle disorders. J Transl Med. 2015;13:243.
• ²
  Huxtable RJ. Physiological actions of taurine. Physiol Rev. 1992;72(1):101-63.
• ³
  Schaffer SW, Jong CJ, Ramila KC, Azuma J. Physiological roles of taurine in heart and muscle. J Biomed Sci. 2010;17(Suppl. 1):S2.
• ⁴
  Vettorazzi JF, Ribeiro RA, Santos-Silva JC, Borck PC, Batista TM, Nardelli TR. Taurine supplementation increases K(ATP) channel protein content, improving Ca2+ handling and insulin secretion in islets from malnourished mice fed on a high-fat diet. Amino Acids. 2014;46, 2123-2136.
• ⁵
  Murakami S. Role of taurine in the pathogenesis of obesity. Mol Nutr Food Res. 2015;59:1353-1363.
• ⁶
  Kim J, Park J, Lim K. Nutrition Supplements to Stimulate Lipolysis: A Review in Relation to Endurance Exercise Capacity. J Nutr Sci Vitaminol (Tokyo). 2016;62(3):141-61.
• ⁷
  De Carvalho FG, Galan BSM, Santos PS, Pritchett K, Pfrimer K, Ferriolli E, Papoti M, Marchini JS, Freitas, EC. Taurine: A Potential Ergogenic Aid for Preventing Muscle Damage and Protein Catabolism and Decreasing Oxidative Stress Produced by Endurance Exercise. Front Physiol. 2017; 8:710.
• ⁸
  Sun M, Qian F, Shen W, Tian C, Hao J, Sun L, Liu J. Mitochondrial nutrients stimulate performance and mitochondrial biogenesis in exhaustively exercised rats. Scand J Med Sci Sports. 2012;22(6):764-75.
• ⁹
  Barua M, Liu Y, Quinn MR. Taurine chloramine inhibits inducible nitric oxide synthase and TNF-α gene expression in activated alveolar macrophages: decreased NF-kβ activation and lkβ kinase activity. J Immunol. 2002;167:2275-81.
• ¹⁰
  Schuller-Levis GB, Park E. Taurine: new implications for an old amino acid. FEMS Microbiol Lett. 2003;226:195-202.
• ¹¹
  Carneiro EM, Latorraca MQ, Araujo E, Beltrá M, Olivers MJ, Navarro M, Berná G, Bedoya FJ, Velloso LA, Soria B, Martin F. Taurine supplementation modulates glucose homeostasis and islet function. J Nutr Biochem. 2009;20:503-511.
• ¹²
  Bakker AJ, Berg HM. Effect of taurine on sarcoplasmic reticulum function and force in skinned fast-twitch skeletal muscle fibres of the rat. J Physiol. 2002;538(1):185-194.
• ¹³
  Zhang M, IzumI I, Kagamimori S, Sokejima S, Yamagami T, Liu Z, Qi B. Role of taurine supplementation to prevent exercise-induced oxidative stress in healthy young men. Amino Acids. 2004;26:203-207.
• ¹⁴
  Yatabe Y, Miyakawa S, Miyazaki T, Matsuzaki Y, Ochiai N. Effects of taurine administration in rat skeletal muscles on exercise. J Orthop Sci. 2003;8:415-419.
• ¹⁵
  Rodríguez F A, Mader A. Energy metabolism during 400 and 100-m crawl swimming: computer simulation based on free swimming measurement. In: Chatard J.C. (ed.), Biomechanics and Medicine in Swimming IX, pp. 373-378. Saint-Étienne: Publications del’Université de Saint-Étienne [ISBN 2-86272-303-7], 2003.
• ¹⁶
  Kalva-Filho CA, Campos EZ, Andrade VL, Silva ASR, Zagatto AM, Lima MCS, Papoti M. Relationship of aerobic and anaerobic parameters with 400 m front crawl swimming performance. Biol Sport. 2015;32:333-337.
• ¹⁷
  Burke LM, Cox GR, Culmmings NK, Desbrow B. Guidelines for daily carbohydrate intake: do athletes achieve them? Sports Med. 2001;31(4):267-99.
• ¹⁸
  Rodrigues F, Mader A. Energy Systems in Swimming. In: Seifert L, Chollet D, Mujika I, editors. World Book of Swimming: From Science to Performance. New York: Nova Science Publishers Inc.; 2011. pp. 224-54.
• ¹⁹
  Smith JEW, Holmes ME, McAllister MJ. Nutritional Considerations for Performance in Young Athletes. J Sports Med. 2015, Article ID 734649.
• ²⁰
  Shao A, Hathcock JN. Risk assessment for the amino acids taurine, L-glutamine and L-arginine. Regul Toxicol Pharmacol. 2008;50(3):376-99.
• ²¹
  Weir JB. New methods for calculating metabolic rate with special reference to protein metabolism. J Physiol. 1949;65(3):243-254.
• ²²
  Deyl Z, Hyanek J, Horakova M. Profiling of amino acids in body fluids and tissues by means of liquid chromatography. J Chromat. 1986;379:177-250.
• ²³
  Pereira R, Papoti M, Zagatto AM, Gobatto CA. Validation of two Protocols for Determination of Anaerobic Threshold in Swimming. Motriz: J. Phys. Ed. 2002;8:57-61.
• ²⁴
  Papoti M, Vitório R, Araújo GG, Silva ASRD, Santhiago V, Martins LEB, Cunha SA, Gobatto CA. Determination of Force Corresponding to Maximal Lactate Steady State in Tethered Swimming. Int J Exerc Sci. 2009;2(4):269-279.
• ²⁵
  Galloway SD, Talanian JL, Shoveller AK, Heigenhauser GJ, Spriet LL. Seven days of oral taurine supplementation does not increase muscle taurine content or alter substrate metabolism during prolonged exercise in humans. J Appl Physiol. 2008;105(2):643-51.
• ²⁶
  Bakker AJ, Berg HM. The effect of taurine on sarcoplasmic reticulum function and contractile properties in skinned skeletal muscle fibers of the rat. J Physiol. 2002;538:185-194.
• ²⁷
  Thomas DT, Erdman KA, Burke LM. American College of Sports Medicine Joint Position Statement. Nutrition and Athletic Performance. Med Sci Sports Exerc. 2016 Mar;48(3):543-68.
• ²⁸
  Balshaw TG, Bampouras TM, Barry TJ, Sparks SA. The effect of acute taurine ingestion on 3-km running performance in trained middle-distance runners. Amino Acids. 2013;44(2):555-61.
• ²⁹
  Beyranvand MR, Khalafi MK, Roshan VD, Choobineh S, Parsa SA, Piranfar MA. Effect of taurine supplementation on exercise capacity of patients with heart failure. J Cardiol. 2011;57,333-337.
• ³⁰
  Keskinen KL, Komi PV, Rusko H. A comparative study of blood lactate tests in swimming. Int J Sports Med. 1989;10(3):197-201.
• ³¹
  Federação Aquática Paulista. Acess:< https://www.aquaticapaulista.org.br/federacao.php>. In: https://www.aquaticapaulista.org.br/arquivos/2016/20160531105234.pdf.
  » https://www.aquaticapaulista.org.br/federacao.php

Publication Dates

• Publication in this collection
  2018

History

• Received
  23 Sept 2017
• Accepted
  07 Feb 2018