Effects of Citrulline Malate Supplementation on Muscle Strength in Resistance-Trained Adults: A Systematic Review and Meta-Analysis of Randomized Controlled Trials

References

• ACSM. 2009. American College of Sports Medicine position stand. Progression models in resistance training for healthy adults. Med Sci Sports Exerc. 41(3):687–708. doi:10.1249/MSS.0b013e3181915670.
   PubMed Web of Science ®Google Scholar
• Aguiar AF, Vechetti-Júnior IJ, Souza RW, Piedade WP, Pacagnelli FL, Leopoldo AS, Casonatto J, Dal-Pai-Silva M. 2017. Nitric oxide synthase inhibition impairs muscle regrowth following immobilization. Nitric Oxide. 69:22–27. doi:10.1016/j.niox.2017.07.006.
   PubMed Web of Science ®Google Scholar
• Bailey SJ, Blackwell JR, Lord T, Vanhatalo A, Winyard PG, Jones AM. 2015. l-Citrulline supplementation improves O2 uptake kinetics and high-intensity exercise performance in humans. J Appl Physiol. 119(4):385–395. doi:10.1152/japplphysiol.00192.2014.
   PubMed Web of Science ®Google Scholar
• Bendahan D, Mattei JP, Ghattas B, Confort-Gouny S, Le Guern ME, Cozzone PJ. 2002. Citrulline/malate promotes aerobic energy production in human exercising muscle. Br J Sports Med. 36(4):282–289. doi:10.1136/bjsm.36.4.282.
   PubMed Web of Science ®Google Scholar
• Bloomer RJ. 2010. Nitric oxide supplements for sports. Strength Cond J. 32(2):14–20. doi:10.1519/SSC.0b013e3181bdaf89.
   Web of Science ®Google Scholar
• Breuillard C, Cynober L, Moinard C. 2015. Citrulline and nitrogen homeostasis: an overview. Amino Acids. 47(4):685–691. doi:10.1007/s00726-015-1932-2.
   PubMed Web of Science ®Google Scholar
• Campos GE, Luecke TJ, Wendeln HK, Toma K, Hagerman FC, Murray TF, Ragg KE, Ratamess NA, Kraemer WJ, Staron RS. 2002. Muscular adaptations in response to three different resistance-training regimens: specificity of repetition maximum training zones. Eur J Appl Physiol. 88(1-2):50–60. doi:10.1007/s00421-002-0681-6.
   PubMed Web of Science ®Google Scholar
• Chappell AJ, Allwood DM, Johns R, Brown S, Sultana K, Anand A, Simper T. 2018. Citrulline malate supplementation does not improve German Volume Training performance or reduce muscle soreness in moderately trained males and females. J Int Soc Sports Nutr. 15(1):42. doi:10.1186/s12970-018-0245-8.
   PubMedGoogle Scholar
• Ckless K, van der Vliet A, Janssen-Heininger Y. 2007. Oxidative-nitrosative stress and post-translational protein modifications: implications to lung structure-function relations. Arginase modulates NF-kappaB activity via a nitric oxide-dependent mechanism. Am J Respir Cell Mol Biol. 36(6):645–653. doi:10.1165/rcmb.2006-0329SM.
   PubMed Web of Science ®Google Scholar
• Curis E, Nicolis I, Moinard C, Osowska S, Zerrouk N, Bénazeth S, Cynober L. 2005. Almost all about citrulline in mammals. Amino Acids. 29(3):177–205. doi:10.1007/s00726-005-0235-4.
   PubMed Web of Science ®Google Scholar
• Del Vecchio A, Casolo A, Negro F, Scorcelletti M, Bazzucchi I, Enoka R, Felici F, Farina D. 2019. The increase in muscle force after 4 weeks of strength training is mediated by adaptations in motor unit recruitment and rate coding. J Physiol. 597(7):1873–1887. doi:10.1113/JP277250.
   PubMed Web of Science ®Google Scholar
• Duval S, Tweedie R. 2000. Trim and fill: a simple funnel-plot-based method of testing and adjusting for publication bias in meta-analysis. Biometrics. 56(2):455–463. doi:10.1111/j.0006-341X.2000.00455.x.
   PubMed Web of Science ®Google Scholar
• Farney TM, Bliss MV, Hearon CM, Salazar DA. 2019. The effect of citrulline malate supplementation on muscle fatigue among healthy participants. J Strength Cond Res. 33(9):2464–2470. doi:10.1519/JSC.0000000000002356.
   PubMed Web of Science ®Google Scholar
• Ferguson B. 2014. ACSM’s guidelines for exercise testing and prescription 9th Ed. J Can Chiropr Assoc. 58(3):328.
   Google Scholar
• Garber CE, Blissmer B, Deschenes MR, Franklin BA, Lamonte MJ, Lee I-M, Nieman DC, Swain DP. 2011. 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. 43(7):1334–1359. doi:10.1249/MSS.0b013e318213fefb.
   PubMed Web of Science ®Google Scholar
• Glenn JM, Gray M, Jensen A, Stone MS, Vincenzo JL. 2016. Acute citrulline-malate supplementation improves maximal strength and anaerobic power in female, masters athletes tennis players. Eur J Sport Sci. 16(8):1095–1103. doi:10.1080/17461391.2016.1158321.
   PubMed Web of Science ®Google Scholar
• Glenn JM, Gray M, Wethington LN, Stone MS, Stewart RW, Jr, Moyen NE. 2017. Acute citrulline malate supplementation improves upper- and lower-body submaximal weightlifting exercise performance in resistance-trained females. Eur J Nutr. 56(2):775–784. doi:10.1007/s00394-015-1124-6.
   PubMed Web of Science ®Google Scholar
• Grgic J, Trexler ET, Lazinica B, Pedisic Z. 2018. Effects of caffeine intake on muscle strength and power: a systematic review and meta-analysis. J Int Soc Sports Nutr. 15:11. doi:10.1186/s12970-018-0216-0.
   PubMed Web of Science ®Google Scholar
• Heunks LM, Machiels HA, Dekhuijzen PN, Prakash YS, Sieck GC. 2001. Nitric oxide affects sarcoplasmic calcium release in skeletal myotubes. J Appl Physiol. 91(5):2117–2124. doi:10.1152/jappl.2001.91.5.2117.
   PubMed Web of Science ®Google Scholar
• Higaki Y, Hirshman MF, Fujii N, Goodyear LJ. 2001. Nitric oxide increases glucose uptake through a mechanism that is distinct from the insulin and contraction pathways in rat skeletal muscle. Diabetes. 50(2):241–247. doi:10.2337/diabetes.50.2.241.
   PubMed Web of Science ®Google Scholar
• Hong YH, Betik AC, McConell GK. 2014. Role of nitric oxide in skeletal muscle glucose uptake during exercise. Exp Physiol. 99(12):1569–1573. doi:10.1113/expphysiol.2014.079202.
   PubMed Web of Science ®Google Scholar
• Hwang P, Morales Marroquin FE, Gann J, Andre T, McKinley-Barnard S, Kim C, Morita M, Willoughby DS. 2018. Eight weeks of resistance training in conjunction with glutathione and L-Citrulline supplementation increases lean mass and has no adverse effects on blood clinical safety markers in resistance-trained males. J Int Soc Sports Nutr. 15(1):30. doi:10.1186/s12970-018-0235-x.
   PubMedGoogle Scholar
• Joyner MJ, Casey DP. 2015. Regulation of increased blood flow (hyperemia) to muscles during exercise: a hierarchy of competing physiological needs. Physiol Rev. 95(2):549–601. doi:10.1152/physrev.00035.2013.
   PubMed Web of Science ®Google Scholar
• Joyner MJ, Dietz NM. 1997. Nitric oxide and vasodilation in human limbs. J Appl Physiol. 83(6):1785–1796. doi:10.1152/jappl.1997.83.6.1785.
   PubMed Web of Science ®Google Scholar
• Lanhers C, Pereira B, Naughton G, Trousselard M, Lesage FX, Dutheil F. 2015. Creatine supplementation and lower limb strength performance: a systematic review and meta-analyses. Sports Med. 45(9):1285–1294. doi:10.1007/s40279-015-0337-4.
   PubMed Web of Science ®Google Scholar
• Lanhers C, Pereira B, Naughton G, Trousselard M, Lesage FX, Dutheil F. 2017. Creatine supplementation and upper limb strength performance: a systematic review and meta-analysis. Sports Med. 47(1):163–173. doi:10.1007/s40279-016-0571-4.
   PubMed Web of Science ®Google Scholar
• Li M, Liu F. 2019. Effect of whey protein supplementation during resistance training sessions on body mass and muscular strength: a meta-analysis. Food Funct. 10(5):2766–2773. doi:10.1039/C9FO00182D.
   PubMed Web of Science ®Google Scholar
• Liberati A, Altman DG, Tetzlaff J, Mulrow C, Gotzsche PC, Ioannidis JP, Clarke M, Devereaux PJ, Kleijnen J, Moher D. 2009. The PRISMA statement for reporting systematic reviews and meta-analyses of studies that evaluate healthcare interventions: explanation and elaboration. BMJ. 339(jul21 1):b2700–b2700. doi:10.1136/bmj.b2700.
   PubMed Web of Science ®Google Scholar
• Mutch BJ, Banister EW. 1983. Ammonia metabolism in exercise and fatigue: a review. Med Sci Sports Exerc. 15(1):41–50.
   PubMed Web of Science ®Google Scholar
• Naclerio F, Larumbe-Zabala E. 2016. Effects of whey protein alone or as part of a multi-ingredient formulation on strength, fat-free mass, or lean body mass in resistance-trained individuals: a meta-analysis. Sports Med. 46(1):125–137. doi:10.1007/s40279-015-0403-y.
   PubMed Web of Science ®Google Scholar
• Percival JM, Anderson KN, Huang P, Adams ME, Froehner SC. 2010. Golgi and sarcolemmal neuronal NOS differentially regulate contraction-induced fatigue and vasoconstriction in exercising mouse skeletal muscle. J Clin Invest. 120(3):816–826. doi:10.1172/JCI40736.
   PubMed Web of Science ®Google Scholar
• Pérez-Guisado J, Jakeman PM. 2010. Citrulline malate enhances athletic anaerobic performance and relieves muscle soreness. J Strength Cond Res. 24(5):1215–1222. doi:10.1519/JSC.0b013e3181cb28e0.
   PubMed Web of Science ®Google Scholar
• Poderoso JJ, Helfenberger K, Poderoso C. 2019. The effect of nitric oxide on mitochondrial respiration. Nitric Oxide. 88:61–72. doi:10.1016/j.niox.2019.04.005.
   PubMed Web of Science ®Google Scholar
• Polito MD, Souza DB, Casonatto J, Farinatti P. 2016. Acute effect of caffeine consumption on isotonic muscular strength and endurance: a systematic review and meta-analysis. Sci Sports. 31(3):119–128. doi:10.1016/j.scispo.2016.01.006.
   Web of Science ®Google Scholar
• Rogers JM, Gills J, Gray M. 2020. Acute effects of Nitrosigine(R) and citrulline malate on vasodilation in young adults. J Int Soc Sports Nutr. 17(1):12. doi:10.1186/s12970-020-00343-y.
   PubMed Web of Science ®Google Scholar
• Rougé C, Des Robert C, Robins A, Le Bacquer O, Volteau C, De La Cochetière MF, Darmaun D. 2007. Manipulation of citrulline availability in humans. Am J Physiol Gastrointest Liver Physiol. 293(5):G1061–G1067. doi:10.1152/ajpgi.00289.2007.
   PubMed Web of Science ®Google Scholar
• Simmonds MJ, Detterich JA, Connes P. 2014. Nitric oxide, vasodilation and the red blood cell. Biorheology. 51(2-3):121–134. doi:10.3233/BIR-140653.
   PubMed Web of Science ®Google Scholar
• Smith LW, Smith JD, Criswell DS. 2002. Involvement of nitric oxide synthase in skeletal muscle adaptation to chronic overload. J Appl Physiol. 92(5):2005–2011. doi:10.1152/japplphysiol.00950.2001.
   PubMed Web of Science ®Google Scholar
• Stamler JS, Meissner G. 2001. Physiology of nitric oxide in skeletal muscle. Physiol Rev. 81(1):209–237. doi:10.1152/physrev.2001.81.1.209.
   PubMed Web of Science ®Google Scholar
• Sureda A, Córdova A, Ferrer MD, Pérez G, Tur JA, Pons A. 2010. L-citrulline-malate influence over branched chain amino acid utilization during exercise. Eur J Appl Physiol. 110(2):341–351. doi:10.1007/s00421-010-1509-4.
   PubMed Web of Science ®Google Scholar
• Thibault R, Flet L, Vavasseur F, Lemerle M, Ferchaud-Roucher V, Picot D, Darmaun D. 2011. Oral citrulline does not affect whole body protein metabolism in healthy human volunteers: results of a prospective, randomized, double-blind, cross-over study. Clin Nutr. 30(6):807–811. doi:10.1016/j.clnu.2011.06.005.
   PubMed Web of Science ®Google Scholar
• Trexler ET, Persky AM, Ryan ED, Schwartz TA, Stoner L, Smith-Ryan AE. 2019. Acute effects of citrulline supplementation on high-intensity strength and power performance: a systematic review and meta-analysis. Sports Med. 49(5):707–718. doi:10.1007/s40279-019-01091-z.
   PubMed Web of Science ®Google Scholar
• Viribay A, Burgos J, Fernandez-Landa J, Seco-Calvo J, Mielgo-Ayuso J. 2020. Effects of arginine supplementation on athletic performance based on energy metabolism: a systematic review and meta-analysis. Nutrients. 12(5):1300. doi:10.3390/nu12051300.
   PubMed Web of Science ®Google Scholar
• Wax B, Kavazis AN, Luckett W. 2016. Effects of supplemental citrulline-malate ingestion on blood lactate, cardiovascular dynamics, and resistance exercise performance in trained males. J Diet Suppl. 13(3):269–282. doi:10.3109/19390211.2015.1008615.
   PubMedGoogle Scholar
• Wax B, Kavazis AN, Weldon K, Sperlak J. 2015. Effects of supplemental citrulline malate ingestion during repeated bouts of lower-body exercise in advanced weightlifters. J Strength Cond Res. 29(3):786–792. doi:10.1519/JSC.0000000000000670.
   PubMed Web of Science ®Google Scholar
• Yamato TP, Maher C, Koes B, Moseley A. 2017. The PEDro scale had acceptably high convergent validity, construct validity, and interrater reliability in evaluating methodological quality of pharmaceutical trials. J Clin Epidemiol. 86:176–181. doi:10.1016/j.jclinepi.2017.03.002.
   PubMed Web of Science ®Google Scholar