The Beneficial Effects of Lactobacillus plantarum PS128 on High-Intensity, Exercise-Induced Oxidative Stress, Inflammation, and Performance in Triathletes

Wen-Ching Huang, Chen-Chan Wei, Chi-Chang Huang, Wen-Lin Chen, Hui-Yu Huang, Wen-Ching Huang, Chen-Chan Wei, Chi-Chang Huang, Wen-Lin Chen, Hui-Yu Huang

Abstract

A triathlon, which consists of swimming, bicycling, and running, is a high-intensity and long-term form of exercise that can cause injuries such as muscular damage, inflammation, oxidative stress, and energy imbalance. Probiotics are thought to play an important role in disease incidence, health promotion, and nutrient metabolism, but only a few studies have focused on physiological adaptations to exercise in sports science. Previous studies indicated that Lactobacillus supplementation could improve oxidative stress and inflammatory responses. We investigate the effects of Lactobacillus plantarum PS128 supplementation on triathletes for possible physiological adaptation. The triathletes were assigned to one of two groups with different exercise intensity stimulations with different time-points to investigate the effects of body compositions, inflammation, oxidative stress, performance, fatigue, and injury-related biochemical indices. L. plantarum PS128 supplementation, combined with training, can significantly alleviate oxidative stress (such as creatine kinase, Thioredoxin, and Myeloperoxidase indices) after a triathlon (p < 0.05). This effect is possibly regulated by a 6⁻13% decrease of indicated pro-inflammation (TNF-α, IL-6, and IL-8) cytokines (p < 0.05) and 55% increase of anti-inflammation (IL-10) cytokines (p < 0.05) after intensive exercise stimulation. In addition, L. plantarum PS128 can also substantially increase 24⁻69% of plasma-branched amino acids (p < 0.05) and elevate exercise performance, as compared to the placebo group (p < 0.05). In conclusion, L. plantarum PS128 may be a potential ergogenic aid for better training management, physiological adaptations to exercise, and health promotion.

Keywords: L. plantarum PS128; inflammation; oxidative stress; performance; triathlon.

Conflict of interest statement

The authors declare no conflict of interest.

Figures

Figure 1
Figure 1
Experimental scheme.
Figure 2
Figure 2
Body compositions between pre- and post-supplementation in the two studies. The data are represented as mean ± SEM. Study I included subjects (A) pre- and (B) post-supplementation with muscle, fat, and bone percentages (%) in the placebo group (PG) (n = 9) and L. plantarum group (LG) (n = 9). Study II included subjects (C) pre- and (D) post-supplementation with muscle, fat, and bone percentages (%) in the PG (n = 8) and LG (n = 8). p < 0.05 was considered to be a statistically significant difference within and between the groups.
Figure 3
Figure 3
The profiles of kidney injury and inflammation-associated markers were collected and assessed from the participants in Study II who engaged in a championship triathlon intervention. (A) TRX (Thioredoxin), (B) C5a (Component 5a), and (C) MPO (Myeloperoxidase) were assessed at multiple time points included Basal, AfterEx, and 3hRest, and the data were represented as mean ± SEM. * indicates a significant difference between groups; + indicates a significant difference compared with the basal point within groups; and # indicates a significant difference compared with the AfterEx point within the groups. The significant difference within and between groups was considered when p < 0.016 (0.05/3).

References

    1. Jeukendrup A.E., Jentjens R.L., Moseley L. Nutritional considerations in triathlon. Sports Med. 2005;35:163–181. doi: 10.2165/00007256-200535020-00005.
    1. Bertola I.P., Sartori R.P., Corrêa D.G., Zotz T.G., Gomes A.R. Profile of injures prevalence in athletes who participated in SESC Triathlon Caiobá-2011. Acta. Ortop. Bras. 2014;22:191–196. doi: 10.1590/1413-78522014220400895.
    1. Brentano M.A., Martins Kruel L.F. A review on strength exercise-induced muscle damage: Applications, adaptation mechanisms and limitations. J. Sports Med. Phys. Fitness. 2011;51:1–10.
    1. Howatson G., van Someren K.A. The prevention and treatment of exercise-induced muscle damage. Sports Med. 2008;38:483–503. doi: 10.2165/00007256-200838060-00004.
    1. Rubio-Arias J.Á., Ávila-Gandía V., López-Román F.J., Soto-Méndez F., Alcaraz P.E., Ramos-Campo D.J. Muscle damage and inflammation biomarkers after two ultra-endurance mountain races of different distances: 54 km vs 111 km. Physiol. Behav. 2018;18 doi: 10.1016/j.physbeh.2018.10.002.
    1. Lynn A., Garner S., Nelson N., Simper T.N., Hall A.C., Ranchordas M.K. Effect of bilberry juice on indices of muscle damage and inflammation in runners completing a half-marathon: A randomised, placebo-controlled trial. J. Int. Soc. Sports Nutr. 2018;15:22. doi: 10.1186/s12970-018-0227-x.
    1. Hill C., Guarner F., Reid G., Gibson G.R., Merenstein D.J., Pot B., Morelli L., Canani R.B., Flint H.J., Salminen S., et al. Expert consensus document. The International Scientific Association for Probiotics and Prebiotics consensus statement on the scope and appropriate use of the term probiotic. Nat. Rev. Gastroenterol. Hepatol. 2014;11:506–514. doi: 10.1038/nrgastro.2014.66.
    1. Fijan S. Microorganisms with Claimed Probiotic Properties: An Overview of Recent Literature. Int. J. Environ. Res. Public Health. 2014;11:4745–4767. doi: 10.3390/ijerph110504745.
    1. Khalili L., Alipour B., Asghari Jafar-Abadi M., Faraji I., Hassanalilou T., Mesgari Abbasi M., Vaghef-Mehrabany E., Alizadeh Sani M. The Effects of Lactobacillus casei on Glycemic Response, Serum Sirtuin1 and Fetuin—A Levels in Patients with Type 2 Diabetes Mellitus: A Randomized Controlled Trial. Iran. Biomed. J. 2019;23:68–77. doi: 10.29252/ibj.23.1.68.
    1. Kim S., Huang E., Park S., Holzapfel W., Lim S.D. Physiological Characteristics and Anti-obesity Effect of Lactobacillus plantarum K10. Korean J. Food Sci. Anim. Resour. 2018;38:554–569. doi: 10.5851/kosfa.2018.38.3.554.
    1. Toral M., Romero M., Rodríguez-Nogales A., Jiménez R., Robles-Vera I., Algieri F., Chueca-Porcuna N., Sánchez M., de la Visitación N., Olivares M., et al. Lactobacillus fermentum Improves Tacrolimus-Induced Hypertension by Restoring Vascular Redox State and Improving eNOS Coupling. Mol. Nutr. Food Res. 2018 doi: 10.1002/mnfr.201800033.
    1. Son S.H., Yang S.J., Jeon H.L., Yu H.S., Lee N.K., Park Y.S., Paik H.D. Antioxidant and immunostimulatory effect of potential probiotic Lactobacillus paraplantarum SC61 isolated from Korean traditional fermented food, jangajji. Microb. Pathog. 2018 doi: 10.1016/j.micpath.2018.10.018.
    1. Oh N.S., Joung J.Y., Lee J.Y., Kim Y. Probiotic and anti-inflammatory potential of Lactobacillus rhamnosus 4B15 and Lactobacillus gasseri 4M13 isolated from infant feces. PLoS ONE. 2018;13:e0192021. doi: 10.1371/journal.pone.0192021.
    1. Huang W.C., Hsu Y.J., Li H., Kan N.W., Chen Y.M., Lin J.S., Hsu T.K., Tsai T.Y., Chiu Y.S., Huang C.C. Effect of Lactobacillus plantarum TWK10 on Improving Endurance Performance in Humans. Chin. J. Physiol. 2018;61:163–170. doi: 10.4077/CJP.2018.BAH587.
    1. Chen Y.M., Wei L., Chiu Y.S., Hsu Y.J., Tsai T.Y., Wang M.F., Huang C.C. Lactobacillus plantarum TWK10 Supplementation Improves Exercise Performance and Increases Muscle Mass in Mice. Nutrients. 2016;8:205. doi: 10.3390/nu8040205.
    1. Michalickova D.M., Kostic-Vucicevic M.M., Vukasinovic-Vesic M.D., Stojmenovic T.B., Dikic N.V., Andjelkovic M.S., Djordjevic B.I., Tanaskovic B.P., Minic R.D. Lactobacillus helveticus Lafti L10 Supplementation Modulates Mucosal and Humoral Immunity in Elite Athletes: A Randomized, Double-Blind, Placebo-Controlled Trial. J. Strength Cond. Res. 2017;31:62–70. doi: 10.1519/JSC.0000000000001456.
    1. Michalickova D., Minic R., Dikic N., Andjelkovic M., Kostic-Vucicevic M., Stojmenovic T., Nikolic I., Djordjevic B. Lactobacillus helveticus Lafti L10 supplementation reduces respiratory infection duration in a cohort of elite athletes: a randomized, double-blind, placebo-controlled trial. Appl. Physiol. Nutr. Metab. 2016;41:782–789. doi: 10.1139/apnm-2015-0541.
    1. Komano Y., Shimada K., Naito H., Fukao K., Ishihara Y., Fujii T., Kokubo T., Daida H. Efficacy of heat-killed Lactococcus lactis JCM 5805 on immunity and fatigue during consecutive high intensity exercise in male athletes: a randomized, placebo-controlled, double-blinded trial. J. Int. Soc. Sports Nutr. 2018;15:39. doi: 10.1186/s12970-018-0244-9.
    1. Liu W.H., Chuang H.L., Huang Y.T., Wu C.C., Chou G.T., Wang S., Tsai Y.C. Alteration of behavior and monoamine levels attributable to Lactobacillus plantarum PS128 in germ-free mice. Behav. Brain Res. 2016;298:202–209. doi: 10.1016/j.bbr.2015.10.046.
    1. Naharudin M.N., Yusof A. Fatigue index and fatigue rate during an anaerobic performance under hypohydrations. PLoS ONE. 2013;8:e77290. doi: 10.1371/journal.pone.0077290.
    1. Clifford T., Allerton D.M., Brown M.A., Harper L., Horsburgh S., Keane K.M., Stevenson E.J., Howatson G. Minimal muscle damage after a marathon and no influence of beetroot juice on inflammation and recovery. Appl. Physiol. Nutr. Metab. 2017;42:263–270. doi: 10.1139/apnm-2016-0525.
    1. Withee E.D., Tippens K.M., Dehen R., Tibbitts D., Hanes D., Zwickey H. Effects of Methylsulfonylmethane (MSM) on exercise-induced oxidative stress, muscle damage, and pain following a half-marathon: a double-blind, randomized, placebo-controlled trial. J. Int. Soc. Sports Nutr. 2017;14:24. doi: 10.1186/s12970-017-0181-z.
    1. Huang W.C., Chang Y.C., Chen Y.M., Hsu Y.J., Huang C.C., Kan N.W., Chen S.S. Whey Protein Improves Marathon-Induced Injury and Exercise Performance in Elite Track Runners. Int. J. Med. Sci. 2017;14:648–654. doi: 10.7150/ijms.19584.
    1. Bohlooli S., Barmaki S., Khoshkhahesh F., Nakhostin-Roohi B. The effect of spinach supplementation on exercise-induced oxidative stress. J. Sports Med. Phys. Fitness. 2015;55:609–614.
    1. Zając A., Chalimoniuk M., Maszczyk A., Gołaś A., Lngfort J. Central and Peripheral Fatigue During Resistance Exercise—A Critical Review. J. Hum. Kinet. 2015;49:159–169. doi: 10.1515/hukin-2015-0118.
    1. Kawamura T., Muraoka I. Exercise-Induced Oxidative Stress and the Effects of Antioxidant Intake from a Physiological Viewpoint. Antioxidants (Basel) 2018;7:E119. doi: 10.3390/antiox7090119.
    1. Bernecker C., Scherr J., Schinner S., Braun S., Scherbaum W., Halle M. Evidence for an exercise induced increase of TNF-α and IL-6 in marathon runners. Scand. J. Med. Sci. 2013;23:207–214. doi: 10.1111/j.1600-0838.2011.01372.x.
    1. Huang S.C., Wu J.F., Saovieng S., Chien W.H., Hsu M.F., Li X.F., Lee S.D., Huang C.Y., Huang C.Y., Kuo C.H. Doxorubicin inhibits muscle inflammation after eccentric exercise. J. Cachexia Sarcopenia Muscle. 2017;8:277–284. doi: 10.1002/jcsm.12148.
    1. Silva F.O.C., Macedo D.V. Physical exercise, inflammatory process and adaptive condition: An overview. Rev. Bras. Cineantropom. Desempenho Hum. 2011;13:320–328.
    1. Galan B.S., Carvalho F.G., Santos P.C., Gobbi R.B., Kalva-Filho C.A., Papoti M., da Silva A.S., Freitas E.C. Effects of taurine on markers of muscle damage, inflammatory response and physical performance in triathletes. J. Sports Med. Phys. Fitness. 2018;58:1318–1324. doi: 10.23736/S0022-4707.17.07497-7.
    1. Suzuki K., Peake J., Nosaka K., Okutsu M., Abbiss C.R., Surriano R., Bishop D., Quod M.J., Lee H., Martin D.T., et al. Changes in markers of muscle damage, inflammation and HSP70 after an Ironman Triathlon race. Eur. J. Appl. Physiol. 2006;98:525–534. doi: 10.1007/s00421-006-0296-4.
    1. Sugama K., Suzuki K., Yoshitani K., Shiraishi K., Miura S., Yoshioka H., Mori Y., Kometani T. Changes of thioredoxin, oxidative stress markers, inflammation and muscle/renal damage following intensive endurance exercise. Exerc. Immunol. Rev. 2015;21:130–142.
    1. Kasuno K., Nakamura H., Ono T., Muso E., Yodoi J. Protective roles of thioredoxin, a redox-regulating protein, in renal ischemia/reperfusion injury. Kidney Int. 2003;64:1273–1282. doi: 10.1046/j.1523-1755.2003.00224.x.
    1. Danobeitia J.S., Djamali A., Fernandez L.A. The role of complement in the pathogenesis of renal ischemia-reperfusion injury and fibrosis. Fibrogenesis Tissue Repair. 2014;7:16. doi: 10.1186/1755-1536-7-16.
    1. Marumoto M., Suzuki S., Hosono A., Arakawa K., Shibata K., Fuku M., Imaeda N. Changes in thioredoxin concentrations: an observation in an ultra-marathon race. Environ. Health Prev. Med. 2010;15:29–34. doi: 10.1007/s12199-009-0119-4.
    1. Cheng I.S., Wang Y.W., Chen I.F., Hsu G.S., Hsueh C.F., Chang C.K. The Supplementation of Branched-Chain Amino Acids, Arginine, and Citrulline Improves Endurance Exercise Performance in Two Consecutive Days. J. Sports Sci. Med. 2016;15:509–515.
    1. Lysenko E.A, Vepkhvadze T.F., Lednev E.M., Vinogradova O.L., Popov D.V. Branched-chain amino acids administration suppresses endurance exercise-related activation of ubiquitin proteasome signaling in trained human skeletal muscle. J. Physiol. Sci. 2018;68:43–53. doi: 10.1007/s12576-016-0506-8.
    1. Xu M., Kitaura Y., Ishikawa T., Kadota Y., Terai C., Shindo D., Morioka T., Ota M., Morishita Y., Ishihara K., et al. Endurance performance and energy metabolism during exercise in mice with a muscle-specific defect in the control of branched-chain amino acid catabolism. PLoS ONE. 2017;12:e0180989. doi: 10.1371/journal.pone.0180989.
    1. Bradley A.L., Ball T.E. The Wingate test: Effect of load on the power outputs of female athletes and nonathletes. J. Strength Cond. Res. 1992;6:193–199. doi: 10.1519/00124278-199211000-00001.
    1. Mueller S.M., Knechtle P., Knechtle B., Toigo M. An Ironman triathlon reduces neuromuscular performance due to impaired force transmission and reduced leg stiffness. Eur. J. Appl. Physiol. 2015;115:795–802. doi: 10.1007/s00421-014-3051-2.

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