Biomarkers in Sports and Exercise: Tracking Health, Performance, and Recovery in Athletes

Elaine C Lee, Maren S Fragala, Stavros A Kavouras, Robin M Queen, John Luke Pryor, Douglas J Casa, Elaine C Lee, Maren S Fragala, Stavros A Kavouras, Robin M Queen, John Luke Pryor, Douglas J Casa

Abstract

Biomarker discovery and validation is a critical aim of the medical and scientific community. Research into exercise and diet-related biomarkers aims to improve health, performance, and recovery in military personnel, athletes, and lay persons. Exercise physiology research has identified individual biomarkers for assessing health, performance, and recovery during exercise training. However, there are few recommendations for biomarker panels for tracking changes in individuals participating in physical activity and exercise training programs. Our approach was to review the current literature and recommend a collection of validated biomarkers in key categories of health, performance, and recovery that could be used for this purpose. We determined that a comprehensive performance set of biomarkers should include key markers of (a) nutrition and metabolic health, (b) hydration status, (c) muscle status, (d) endurance performance, (e) injury status and risk, and (f) inflammation. Our review will help coaches, clinical sport professionals, researchers, and athletes better understand how to comprehensively monitor physiologic changes, as they design training cycles that elicit maximal improvements in performance while minimizing overtraining and injury risk.

Figures

Figure 1.
Figure 1.
Comprehensive approach to biomarker analysis. Assessing multiple aspects of biological function allows coaches and athletes to track performance, recovery, and health in an individualized, practical manner. Relying on multiple validated biomarkers increases sensitivity, allowing athletes to detect potential impacts of training, recovery, diet, etc., long term. Data from long-term biomarker analysis will enhance preventative detection of injury or negative effects on performance. Examples of options for well-studied biomarkers in each category are provided as suggested components of a customized panel.
Figure 2.
Figure 2.
Suggested biomarker testing time points. ● represents suggested biomarker panel testing at diagnostic opportunities throughout off-season and during-season training. * represents competitive season during which both training and competition occur. ** represents peak competition season during which championship matches might occur. Suggested time points for biomarker testing include before and after each major shift in training. Frequent (2–3 tests) testing during rested, healthy periods in the off-season will provide baseline values for many biomarkers and will be important for providing individualized biomarker data. Testing is also recommended before and after at least 1 acute exercise bout or performance test in the middle of a training season to acquire data around optimal performance. Testing before and after an acute bout of exercise will also allow athletes to analyze variables that might be more meaningful as responsive to an acute bout rather than as a single value at rest. It is also recommended that flexibility be built in to test biomarkers around a major championship competition or acute injury event. Testing not just before and after such an event, but also at additional time points after the competition or injury will allow the athlete to assess a recovery response. Data from biomarkers should be analyzed with physiological and physical data to contextualize results. This approach will optimize sensitivity, precision, and accuracy.
Figure 3.
Figure 3.
Exercise-induced muscle damage and inflammation are physiologically integrated. Biomarkers of skeletal muscle damage and inflammation often increase concurrently during exercise-induced muscle damage or injury that will negatively affect performance. Inflammation is a process that will follow initial tissue damage and lag during recovery.

References

    1. Adlercreutz H. Western diet and Western diseases: Some hormonal and biochemical mechanisms and associations. Scand J Clin Lab Invest Suppl 201: 3–23, 1990.
    1. Aldred S, Love JA, Tonks LA, Stephens E, Jones DS, Blannin AK. The effect of steady state exercise on circulating human IgE and IgG in young healthy volunteers with known allergy. J Sci Med Sport 13: 16–19, 2010.
    1. Anderson RA, Bryden NA, Polansky MM, Deuster PA. Exercise effects on chromium excretion of trained and untrained men consuming a constant diet. J Appl Physiol (1985) 64: 249–252, 1988.
    1. Apro W, Blomstrand E. Influence of supplementation with branched-chain amino acids in combination with resistance exercise on p70S6 kinase phosphorylation in resting and exercising human skeletal muscle. Acta Physiol (Oxf) 200: 237–248, 2010.
    1. Armstrong LE, Maresh CM, Castellani JW, Bergeron MF, Kenefick RW, LaGasse KE, Riebe D. Urinary indices of hydration status. Int J Sport Nutr 4: 265–279, 1994.
    1. Armstrong LE, Maughan RJ, Senay LC, Shirreffs SM. Limitations to the use of plasma osmolality as a hydration biomarker. Am J Clin Nutr 98: 503–504, 2013.
    1. Bacharach DW, Petit M, Rundell KW. Relationship of blood urea nitrogen to training intensity of elite female biathlon skiers. J Strength Cond Res 10: 105–108, 1996.
    1. Banfi G, Marinelli M, Roi GS, Agape V. Usefulness of free testosterone/cortisol ratio during a season of elite speed skating athletes. Int J Sports Med 14: 373–379, 1993.
    1. Beard JL, Murray-Kolb LE, Rosales FJ, Solomons NW, Angelilli ML. Interpretation of serum ferritin concentrations as indicators of total-body iron stores in survey populations: The role of biomarkers for the acute phase response. Am J Clin Nutr 84: 1498–1505, 2006.
    1. Beck TJ, Ruff CB, Shaffer RA, Betsinger K, Trone DW, Brodine SK. Stress fracture in military recruits: Gender differences in muscle and bone susceptibility factors. Bone 27: 437–444, 2000.
    1. Berglund B. High-altitude training. Aspects of haematological adaptation. Sports Med 14: 289–303, 1992.
    1. Bermejo F, Garcia-Lopez S. A guide to diagnosis of iron deficiency and iron deficiency anemia in digestive diseases. World J Gastroenterol 15: 4638–4643, 2009.
    1. Blomstrand E, Eliasson J, Karlsson HK, Köhnke R. Branched-chain amino acids activate key enzymes in protein synthesis after physical exercise. J Nutr 136(1 Suppl): 269S–73S, 2006.
    1. Bloomer RJ, Larson DE, Fisher-Wellman KH, Galpin AJ, Schilling BK. Effect of eicosapentaenoic and docosahexaenoic acid on resting and exercise-induced inflammatory and oxidative stress biomarkers: A randomized, placebo controlled, cross-over study. Lipids Health Dis 8: 36, 2009.
    1. Borel MJ, Smith SM, Derr J, Beard JL. Day-to-day variation in iron-status indices in healthy men and women. Am J Clin Nutr 54: 729–735, 1991.
    1. Bouget M, Rouveix M, Michaux O, Pequignot JM, Filaire E. Relationships among training stress, mood and dehydroepiandrosterone sulphate/cortisol ratio in female cyclists. J Sports Sci 24: 1297–1302, 2006.
    1. Brancaccio P, Lippi G, Maffulli N. Biochemical markers of muscular damage. Clin Chem Lab Med 48: 757–767, 2010.
    1. Brownlie T, IV, Utermohlen V, Hinton PS, Haas JD. Tissue iron deficiency without anemia impairs adaptation in endurance capacity after aerobic training in previously untrained women. Am J Clin Nutr 79: 437–443, 2004.
    1. Brownlie T, IV, Utermohlen V, Hinton PS, Giordano C, Haas JD. Marginal iron deficiency without anemia impairs aerobic adaptation among previously untrained women. Am J Clin Nutr 75: 734–742, 2002.
    1. Buresh R, Berg K, French J. The effect of resistive exercise rest interval on hormonal response, strength, and hypertrophy with training. J Strength Cond Res 23: 62–71, 2009.
    1. Calvisi V, Lupparelli S. C-reactive protein changes in the uncomplicated course of arthroscopic anterior cruciate ligament reconstruction. Int J Immunopathol Pharmacol 21: 603–607, 2008.
    1. Casa DJ, Armstrong LE, Hillman SK, Montain SJ, Reiff RV, Rich BS, Roberts WO, Stone JA. National athletic trainers' association position statement: Fluid replacement for athletes. J Athl Train 35: 212–224, 2000.
    1. Castell LM, Yamamoto T, Phoenix J, Newsholme EA. The role of tryptophan in fatigue in different conditions of stress. Adv Exp Med Biol 467: 697–704, 1999.
    1. Cevada T, Vasques PE, Moraes H, Deslandes A. Salivary cortisol levels in athletes and nonathletes: A systematic review. Horm Metab Res 46: 905–910, 2014.
    1. Cheuvront SN, Kenefick RW, Charkoudian N, Sawka MN. Physiologic basis for understanding quantitative dehydration assessment. Am J Clin Nutr 97: 455–462, 2013.
    1. Chicharro JL, López-Mojares LM, Lucía A, Pérez M, Alvarez J, Labanda P, Calvo F, Vaquero AF. Overtraining parameters in special military units. Aviat Space Environ Med 69: 562–568, 1998.
    1. Constantini NW, Arieli R, Chodick G, Dubnov-Raz G. High prevalence of vitamin D insufficiency in athletes and dancers. Clin J Sport Med 20: 368–371, 2010.
    1. Corsetti R, Barassi A, Perego S, Sansoni V, Rossi A, Damele CA, Melzi D'Eril G, Banfi G, Lombardi G. Changes in urinary amino acids excretion in relationship with muscle activity markers over a professional cycling stage race: In search of fatigue markers. Amino Acids 48: 183–192, 2016.
    1. Cuisinier C, Ward RJ, Francaux M, Sturbois X, de Witte P. Changes in plasma and urinary taurine and amino acids in runners immediately and 24h after a marathon. Amino Acids 20: 13–23, 2001.
    1. Cummins P, Young A, Auckland ML, Michie CA, Stone PC, Shepstone BJ. Comparison of serum cardiac specific troponin-I with creatine kinase, creatine kinase-MB isoenzyme, tropomyosin, myoglobin and C-reactive protein release in marathon runners: Cardiac or skeletal muscle trauma? Eur J Clin Invest 17: 317–324, 1987.
    1. Dahlquist DT, Dieter BP, Koehle MS. Plausible ergogenic effects of vitamin D on athletic performance and recovery. J Int Soc Sports Nutr 12: 33, 2015.
    1. DellaValle DM. Iron supplementation for female athletes: Effects on iron status and performance outcomes. Curr Sports Med Rep 12: 234–239, 2013.
    1. 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 21: 501–506, 2011.
    1. DellaValle DM, Haas JD. Iron supplementation improves energetic efficiency in iron-depleted female rowers. Med Sci Sports Exerc 46: 1204–1215, 2014.
    1. Deuster PA, Day BA, Singh A, Douglass L, Moser-Veillon PB. Zinc status of highly trained women runners and untrained women. Am J Clin Nutr 49: 1295–1301, 1989.
    1. Dietrich MO, Tort AB, Schaf DV, Farina M, Gonçalves CA, Souza DO, Portela LV. Increase in serum S100B protein level after a swimming race. Can J Appl Physiol 28: 710–716, 2003.
    1. Dubnov G, Constantini NW. Prevalence of iron depletion and anemia in top-level basketball players. Int J Sport Nutr Exerc Metab 14: 30–37, 2004.
    1. Ebo DG, Stevens WJ. IgE-mediated food allergy–extensive review of the literature. Acta Clin Belg 56: 234–247, 2001.
    1. Einspahr KJ, Tharp G. Influence of endurance training on plasma amino acid concentrations in humans at rest and after intense exercise. Int J Sports Med 10: 233–236, 1989.
    1. Fahrner CL, Hackney AC. Effects of endurance exercise on free testosterone concentration and the binding affinity of sex hormone binding globulin (SHBG). Int J Sports Med 19: 12–15, 1998.
    1. Feingold D, Hame SL. Female athlete triad and stress fractures. Orthop Clin North Am 37: 575–583, 2006.
    1. Filaire E, Duche P, Lac G. Effects of amount of training on the saliva concentrations of cortisol, dehydroepiandrosterone and on the dehydroepiandrosterone: Cortisol concentration ratio in women over 16 weeks of training. Eur J Appl Physiol Occup Physiol 78: 466–471, 1998.
    1. Flink EB. Magnesium deficiency. Etiology and clinical spectrum. Acta Med Scand Suppl 647: 125–137, 1981.
    1. Fortes MB, Diment BC, Di Felice U, Gunn AE, Kendall JL, Esmaeelpour M, Walsh NP. Tear fluid osmolarity as a potential marker of hydration status. Med Sci Sports Exerc 43: 1590–1597, 2011.
    1. Fortes MB, Owen JA, Raymond-Barker P, Bishop C, Elghenzai S, Oliver SJ, Walsh NP. Is this elderly patient dehydrated? Diagnostic accuracy of hydration assessment using physical signs, urine, and saliva markers. J Am Med Dir Assoc 16: 221–228, 2015.
    1. Friedmann B, Weller E, Mairbaurl H, Bärtsch P. Effects of iron repletion on blood volume and performance capacity in young athletes. Med Sci Sports Exerc 33: 741–746, 2001.
    1. Gillespie CA, Edgerton VR. The role of testosterone in exercise-induced glycogen supercompensation. Horm Metab Res 2: 364–366, 1970.
    1. Gleeson M. Biochemical and immunological markers of over-training. J Sports Sci Med 1: 31–41, 2002.
    1. Golf SW, Bender S, Gruttner J. On the significance of magnesium in extreme physical stress. Cardiovasc Drugs Ther 12(Suppl 2): 197–202, 1998.
    1. Graham MR, et al. Direct hits to the head during amateur boxing is associated with a rise in serum biomarkers for brain injury. Int J Immunopathol Pharmacol 24: 119–125, 2011.
    1. Haas JD, Brownlie T. Iron deficiency and reduced work capacity: A critical review of the research to determine a causal relationship. J Nutr 131: 676S–688S, 2001; discussion 688S–690S.
    1. Häkkinen K, Pakarinen A. Acute hormonal responses to two different fatiguing heavy-resistance protocols in male athletes. J Appl Physiol (1985) 74: 882–887, 1993.
    1. Häkkinen K, Pakarinen A, Alén M, Kauhanen H, Komi PV. Neuromuscular and hormonal adaptations in athletes to strength training in two years. J Appl Physiol (1985) 65: 2406–2412, 1988.
    1. Häkkinen K, Pakarinen A, Alén M, Kauhanen H, Komi PV. Relationships between training volume, physical performance capacity, and serum hormone concentrations during prolonged training in elite weight lifters. Int J Sports Med 8(Suppl 1): 61–65, 1987.
    1. Haslauer CM, Proffen BL, Johnson VM, Hill A, Murray MM. Gene expression of catabolic inflammatory cytokines peak before anabolic inflammatory cytokines after ACL injury in a preclinical model. J Inflamm (Lond) 11: 34, 2014.
    1. Hernandez-Morante JJ, Pérez-de-Heredia F, Luján JA, Zamora S, Garaulet M. Role of DHEA-S on body fat distribution: Gender- and depot-specific stimulation of adipose tissue lipolysis. Steroids 73: 209–215, 2008.
    1. Hinton PS, Giordano C, Brownlie T, Haas JD. Iron supplementation improves endurance after training in iron-depleted, nonanemic women. J Appl Physiol (1985) 88: 1103–1111, 2000.
    1. Hinton PS, Sinclair LM. Iron supplementation maintains ventilatory threshold and improves energetic efficiency in iron-deficient nonanemic athletes. Eur J Clin Nutr 61: 30–39, 2007.
    1. Hong CZ, Lien IN. Metabolic effects of exhaustive training of athletes. Arch Phys Med Rehabil 65: 362–365, 1984.
    1. Hood DA, Kelton R, Nishio ML. Mitochondrial adaptations to chronic muscle use: Effect of iron deficiency. Comp Biochem Physiol Comp Physiol 101: 597–605, 1992.
    1. James WP, Hay AM. Albumin metabolism: Effect of the nutritional state and the dietary protein intake. J Clin Invest 47: 1958–1972, 1968.
    1. Jastrezebski Z. Effect of vitamin D supplementation on the level of physical fitness and blood parameters of rowers during the 8-week high intensity training. Facicula Educ Fiz Si Sport 2: 57–67, 2014.
    1. Jouris KB, McDaniel JL, Weiss EP. The effect of Omega-3 fatty acid supplementation on the inflammatory response to eccentric strength exercise. J Sports Sci Med 10: 432–438, 2011.
    1. Kanazawa I, Yamaguchi T, Sugimoto T. Serum insulin-like growth factor-I is a marker for assessing the severity of vertebral fractures in postmenopausal women with type 2 diabetes mellitus. Osteoporos Int 22: 1191–1198, 2011.
    1. Kanter MM. Free radicals, exercise, and antioxidant supplementation. Int J Sport Nutr 4: 205–220, 1994.
    1. Kavouras SA, Johnson EC, Bougatsas D, Arnaoutis G, Panagiotakos DB, Perrier E, Klein A. Validation of a urine color scale for assessment of urine osmolality in healthy children. Eur J Nutr 55: 907–915, 2016.
    1. Kingsbury KJ, Kay L, Hjelm M. Contrasting plasma free amino acid patterns in elite athletes: Association with fatigue and infection. Br J Sports Med 32: 25–32, 1998; discussion 32–3.
    1. Kleiner G, Marcuzzi A, Zanin V, Monasta L, Zauli G. Cytokine levels in the serum of healthy subjects. Mediators Inflamm 2013: 434010, 2013.
    1. Koch AJ, Pereira R, Machado M. The creatine kinase response to resistance exercise. J Musculoskelet Neuronal Interact 14: 68–77, 2014.
    1. Kraemer WJ, French DN, Paxton NJ, Häkkinen K, Volek JS, Sebastianelli WJ, Putukian M, Newton RU, Rubin MR, Gómez AL, Vescovi JD, Ratamess NA, Fleck SJ, Lynch JM, Knuttgen HG. Changes in exercise performance and hormonal concentrations over a big ten soccer season in starters and nonstarters. J Strength Cond Res 18: 121–128, 2004.
    1. Kraemer WJ, Häkkinen K, Newton RU, Nindl BC, Volek JS, McCormick M, Gotshalk LA, Gordon SE, Fleck SJ, Campbell WW, Putukian M, Evans WJ. Effects of heavy-resistance training on hormonal response patterns in younger vs. older men. J Appl Physiol (1985) 87: 982–992, 1999.
    1. Kraemer WJ, Ratamess NA. Hormonal responses and adaptations to resistance exercise and training. Sports Med 35: 339–361, 2005.
    1. LaManca JJ, Haymes EM. Effects of iron repletion on VO2max, endurance, and blood lactate in women. Med Sci Sports Exerc 25: 1386–1392, 1993.
    1. Li Y, Oosting M, Deelen P, Ricaño-Ponce I, Smeekens S, Jaeger M, Matzaraki V, Swertz MA, Xavier RJ, Franke L, Wijmenga C, Joosten LA, Kumar V, Netea MG. Inter-individual variability and genetic influences on cytokine responses to bacteria and fungi. Nat Med 22: 952–960, 2016.
    1. Lindholm C, Hirschberg AL, Carlström K, von Schoultz B. Hormone anabolic/catabolic balance in female endurance athletes. Gynecol Obstet Invest 36: 176–180, 1993.
    1. Lippi G, Montagnana M, Salvagno GL, Franchini M, Guidi GC. Glycaemic control in athletes. Int J Sports Med 29: 7–10, 2008.
    1. Lohmander LS, Englund PM, Dahl LL, Roos EM. The long-term consequence of anterior cruciate ligament and meniscus injuries: Osteoarthritis. Am J Sports Med 35: 1756–1769, 2007.
    1. Lohmander LS, Ostenberg A, Englund M, Roos H. High prevalence of knee osteoarthritis, pain, and functional limitations in female soccer players twelve years after anterior cruciate ligament injury. Arthritis Rheum 50: 3145–3152, 2004.
    1. Lukaski HC. Vitamin and mineral status: Effects on physical performance. Nutrition 20: 632–644, 2004.
    1. MacKinnon LT. Special feature for the Olympics: Effects of exercise on the immune system: Overtraining effects on immunity and performance in athletes. Immunol Cell Biol 78: 502–509, 2000.
    1. McClung JP, Gaffney-Stomberg E, Lee JJ. Female athletes: A population at risk of vitamin and mineral deficiencies affecting health and performance. J Trace Elem Med Biol 28: 388–392, 2014.
    1. McClung JP, Karl JP, Cable SJ, Williams KW, Nindl BC, Young AJ, Lieberman HR. Randomized, double-blind, placebo-controlled trial of iron supplementation in female soldiers during military training: Effects on iron status, physical performance, and mood. Am J Clin Nutr 90: 124–131, 2009.
    1. McKenzie AL, Munoz CX, Armstrong LE. Accuracy of urine color to detect equal to or greater than 2% body mass loss in men. J Athl Train 50: 1306–1309, 2015.
    1. Mendias CL, Lynch EB, Davis ME, Sibilsky Enselman ER, Harning JA, Dewolf PD, Makki TA, Bedi A. Changes in circulating biomarkers of muscle atrophy, inflammation, and cartilage turnover in patients undergoing anterior cruciate ligament reconstruction and rehabilitation. Am J Sports Med 41: 1819–1826, 2013.
    1. Morita E, Kunie K, Matsuo H. Food-dependent exercise-induced anaphylaxis. J Dermatol Sci 47: 109–117, 2007.
    1. Mougios V. Reference intervals for serum creatine kinase in athletes. Br J Sports Med 41: 674–678, 2007.
    1. Munoz-Torres M, Mezquita-Raya P, Lopez-Rodriguez F, Torres-Vela E, de Dios Luna J, Escobar-Jimenez F. The contribution of IGF-I to skeletal integrity in postmenopausal women. Clin Endocrinol (Oxf) 55: 759–766, 2001.
    1. Muñoz C, Rios E, Olivos J, Brunser O, Olivares M. Iron, copper and immunocompetence. Br J Nutr 98(Suppl 1): S24–S28, 2007.
    1. Muñoz CX, Johnson EC, Demartini JK, Huggins RA, McKenzie AL, Casa DJ, Maresh CM, Armstrong LE. Assessment of hydration biomarkers including salivary osmolality during passive and active dehydration. Eur J Clin Nutr 67: 1257–1263, 2013.
    1. Mussack T, Dvorak J, Graf-Baumann T, Jochum M. Serum S-100B protein levels in young amateur soccer players after controlled heading and normal exercise. Eur J Med Res 8: 457–464, 2003.
    1. Nattiv A, Loucks AB, Manore MM, Sanborn CF, Sundgot-Borgen J, Warren MP; American College of Sports Medicine. American College of Sports Medicine position stand. The female athlete triad. Med Sci Sports Exerc 39: 1867–1882, 2007.
    1. Neselius S, Brisby H, Theodorsson A, Blennow K, Zetterberg H, Marcusson J. CSF-biomarkers in Olympic boxing: Diagnosis and effects of repetitive head trauma. PLoS One 7: e33606, 2012.
    1. Nielsen BW, Bjerke T, Damsgaard TM, Herlin T, Thestrup-Pedersen K, Schiøtz PO. Hyperosmolarity selectively enhances IgE-receptor-mediated histamine release from human basophils. Agents Actions 35: 170–178, 1992.
    1. Nindl BC, Alemany JA, Tuckow AP, Kellogg MD, Sharp MA, Patton JF. Effects of exercise mode and duration on 24-h IGF-I system recovery responses. Med Sci Sports Exerc 41: 1261–1270, 2009.
    1. Otto M, Holthusen S, Bahn E, Söhnchen N, Wiltfang J, Geese R, Fischer A, Reimers CD. Boxing and running lead to a rise in serum levels of S-100B protein. Int J Sports Med 21: 551–555, 2000.
    1. Peeling P, Blee T, Goodman C, Dawson B, Claydon G, Beilby J, Prins A. Effect of iron injections on aerobic-exercise performance of iron-depleted female athletes. Int J Sport Nutr Exerc Metab 17: 221–231, 2007.
    1. Peeling P, Dawson B, Goodman C, Landers G, Trinder D. Athletic induced iron deficiency: New insights into the role of inflammation, cytokines and hormones. Eur J Appl Physiol 103: 381–391, 2008.
    1. Peeling P, Dawson B, Goodman C, Landers G, Wiegerinck ET, Swinkels DW, Trinder D. Training surface and intensity: Inflammation, hemolysis, and hepcidin expression. Med Sci Sports Exerc 41: 1138–1145, 2009.
    1. Papa L, Ramia MM, Edwards D, Johnson BD, Slobounov SM. Systematic review of clinical studies examining biomarkers of brain injury in athletes after sports-related concussion. J Neurotrauma 32: 661–673, 2015.
    1. Phillips PA, Rolls BJ, Ledingham JG, Forsling ML, Morton JJ. Osmotic thirst and vasopressin release in humans: A double-blind crossover study. Am J Physiol 248: R645–R650, 1985.
    1. Pimstone BL, Barbezat G, Hansen JD, Murray P. Studies on growth hormone secretion in protein-calorie malnutrition. Am J Clin Nutr 21: 482–487, 1968.
    1. Pollock N, Grogan C, Perry M, Pedlar C, Cooke K, Morrissey D, Dimitriou L. Bone-mineral density and other features of the female athlete triad in elite endurance runners: A longitudinal and cross-sectional observational study. Int J Sport Nutr Exerc Metab 20: 418–426, 2010.
    1. Refsum HE, Gjessing LR, Stromme SB. Changes in plasma amino acid distribution and urine amino acids excretion during prolonged heavy exercise. Scand J Clin Lab Invest 39: 407–413, 1979.
    1. Risser WL, Lee EJ, Poindexter HB, West MS, Pivarnik JM, Risser JM, Hickson JF. Iron deficiency in female athletes: Its prevalence and impact on performance. Med Sci Sports Exerc 20: 116–121, 1988.
    1. Roecker L, Meier-Buttermilch R, Brechtel L, Nemeth E, Ganz T. Iron-regulatory protein hepcidin is increased in female athletes after a marathon. Eur J Appl Physiol 95: 569–571, 2005.
    1. Rowland TW, Deisroth MB, Green GM, Kelleher JF. The effect of iron therapy on the exercise capacity of nonanemic iron-deficient adolescent runners. Am J Dis Child 142: 165–169, 1988.
    1. Sawka MN, Cheuvront SN, Kenefick RW. Hypohydration and human performance: Impact of environment and physiological mechanisms. Sports Med 45(Suppl 1): S51–S60, 2015.
    1. Sawka MN, Burke LM, Eichner ER, Maughan RJ, Montain SJ, Stachenfeld NS; American College of Sports Medicine. American College of Sports Medicine position stand. Exercise and fluid replacement. Med Sci Sports Exerc 39: 377–390, 2007.
    1. Schoene RB, Escourrou P, Robertson HT, Nilson KL, Parsons JR, Smith NJ. Iron repletion decreases maximal exercise lactate concentrations in female athletes with minimal iron-deficiency anemia. J Lab Clin Med 102: 306–312, 1983.
    1. Selby GB, Eichner ER. Endurance swimming, intravascular hemolysis, anemia, and iron depletion. New perspective on athlete's anemia. Am J Med 81: 791–794, 1986.
    1. Shahim P, Tegner Y, Wilson DH, Randall J, Skillbäck T, Pazooki D, Kallberg B, Blennow K, Zetterberg H. Blood biomarkers for brain injury in concussed professional ice hockey players. JAMA Neurol 71: 684–692, 2014.
    1. Siles RI, Hsieh FH. Allergy blood testing: A practical guide for clinicians. Cleve Clin J Med 78: 585–592, 2011.
    1. Sinclair LM, Hinton PS. Prevalence of iron deficiency with and without anemia in recreationally active men and women. J Am Diet Assoc 105: 975–978, 2005.
    1. Smith LL. Cytokine hypothesis of overtraining: A physiological adaptation to excessive stress? Med Sci Sports Exerc 32: 317–331, 2000.
    1. Smith DJ, Norris SR. Changes in glutamine and glutamate concentrations for tracking training tolerance. Med Sci Sports Exerc 32: 684–689, 2000.
    1. Snow CM, Rosen CJ, Robinson TL. Serum IGF-I is higher in gymnasts than runners and predicts bone and lean mass. Med Sci Sports Exerc 32: 1902–1907, 2000.
    1. Sorichter S, Puschendorf B, Mair J. Skeletal muscle injury induced by eccentric muscle action: Muscle proteins as markers of muscle fiber injury. Exerc Immunol Rev 5: 5–21, 1999.
    1. Spriet LL, Whitfield J. Taurine and skeletal muscle function. Curr Opin Clin Nutr Metab Care 18: 96–101, 2015.
    1. Stalnacke BM, Ohlsson A, Tegner Y, Sojka P. Serum concentrations of two biochemical markers of brain tissue damage S-100B and neurone specific enolase are increased in elite female soccer players after a competitive game. Br J Sports Med 40: 313–316, 2006.
    1. Stalnacke BM, Sojka P. Repeatedly heading a soccer ball does not increase serum levels of S-100B, a biochemical marker of brain tissue damage: An experimental study. Biomark Insights 3: 87–91, 2008.
    1. Stalnacke BM, Tegner Y, Sojka P. Playing ice hockey and basketball increases serum levels of S-100B in elite players: A pilot study. Clin J Sport Med 13: 292–302, 2003.
    1. Stalnacke BM, Tegner Y, Sojka P. Playing soccer increases serum concentrations of the biochemical markers of brain damage S-100B and neuron-specific enolase in elite players: A pilot study. Brain Inj 18: 899–909, 2004.
    1. Stiefel P, Ruiz-Gutierrez V, Gajón E, Acosta D, García-Donas MA, Madrazo J, Villar J, Carneado J. Sodium transport kinetics, cell membrane lipid composition, neural conduction and metabolic control in type 1 diabetic patients. Changes after a low-dose n-3 fatty acid dietary intervention. Ann Nutr Metab 43: 113–120, 1999.
    1. Strohbach CA, Scofield DE, Nindl BC, Centi AJ, Yanovich R, Evans RK, Moran DS. Female recruits sustaining stress fractures during military basic training demonstrate differential concentrations of circulating IGF-I system components: A preliminary study. Growth Horm IGF Res 22: 151–157, 2012.
    1. Sugimoto T, Nishiyama K, Kuribayashi F, Chihara K. Serum levels of insulin-like growth factor (IGF) I, IGF-binding protein (IGFBP)-2, and IGFBP-3 in osteoporotic patients with and without spinal fractures. J Bone Miner Res 12: 1272–1279, 1997.
    1. Suzuki K, Nakaji S, Yamada M, Totsuka M, Sato K, Sugawara K. Systemic inflammatory response to exhaustive exercise. Cytokine kinetics. Exerc Immunol Rev 8: 6–48, 2002.
    1. Svoboda SJ, Harvey TM, Owens BD, Brechue WF, Tarwater PM, Cameron KL. Changes in serum biomarkers of cartilage turnover after anterior cruciate ligament injury. Am J Sports Med 41: 2108–2116, 2013.
    1. Tanskanen MM, Kyröläinen H, Uusitalo AL, Huovinen J, Nissilä J, Kinnunen H, Atalay M, Häkkinen K. Serum sex hormone-binding globulin and cortisol concentrations are associated with overreaching during strenuous military training. J Strength Cond Res 25: 787–797, 2011.
    1. Tartibian B, Maleki BH, Abbasi A. The effects of ingestion of omega-3 fatty acids on perceived pain and external symptoms of delayed onset muscle soreness in untrained men. Clin J Sport Med 19: 115–119, 2009.
    1. Todd J, Simpson P, Estis J, Torres V, Wub AH. Reference range and short- and long-term biological variation of interleukin (IL)-6, IL-17A and tissue necrosis factor-alpha using high sensitivity assays. Cytokine 64: 660–665, 2013.
    1. Tom A, Nair KS. Assessment of branched-chain amino Acid status and potential for biomarkers. J Nutr 136(1 Suppl): 324S–330S, 2006.
    1. Tourville TW, Johnson RJ, Slauterbeck JR, Naud S, Beynnon BD. Relationship between markers of type II collagen metabolism and tibiofemoral joint space width changes after ACL injury and reconstruction. Am J Sports Med 41: 779–787, 2013.
    1. Urhausen A, Gabriel H, Kindermann W. Blood hormones as markers of training stress and overtraining. Sports Med 20: 251–276, 1995.
    1. Urhausen A, Kindermann W. Diagnosis of overtraining: What tools do we have? Sports Med 32: 95–102, 2002.
    1. Vallee BL, Falchuk KH. The biochemical basis of zinc physiology. Physiol Rev 73: 79–118, 1993.
    1. Vandenbogaerde TJ, Hopkins WG. Effects of acute carbohydrate supplementation on endurance performance: A meta-analysis. Sports Med 41: 773–792, 2011.
    1. Velloso CP. Regulation of muscle mass by growth hormone and IGF-I. Br J Pharmacol 154: 557–568, 2008.
    1. Vervoorn C, Quist AM, Vermulst LJ, Erich WB, de Vries WR, Thijssen JH. The behaviour of the plasma free testosterone/cortisol ratio during a season of elite rowing training. Int J Sports Med 12: 257–263, 1991.
    1. Volek JS, Freidenreich DJ, Saenz C, Kunces LJ, Creighton BC, Bartley JM, Davitt PM, Munoz CX, Anderson JM, Maresh CM, Lee EC, Schuenke MD, Aerni G, Kraemer WJ, Phinney SD. Metabolic characteristics of keto-adapted ultra-endurance runners. Metabolism 65: 100–110, 2016.
    1. Volfinger L, Lassourd V, Michaux JM, Braun JP, Toutain PL. Kinetic evaluation of muscle damage during exercise by calculation of amount of creatine kinase released. Am J Physiol 266: R434–R441, 1994.
    1. von Porat A, Roos EM, Roos H. High prevalence of osteoarthritis 14 years after an anterior cruciate ligament tear in male soccer players: A study of radiographic and patient relevant outcomes. Ann Rheum Dis 63: 269–273, 2004.
    1. Walsh NP, Laing SJ, Oliver SJ, Montague JC, Walters R, Bilzon JL. Saliva parameters as potential indices of hydration status during acute dehydration. Med Sci Sports Exerc 36: 1535–1542, 2004.
    1. Wang W, Wu Z, Dai Z, Yang Y, Wang J, Wu G. Glycine metabolism in animals and humans: Implications for nutrition and health. Amino Acids 45: 463–477, 2013.
    1. Ward RJ, Francaux M, Cuisinier C, Sturbois X, De Witte P. Changes in plasma taurine levels after different endurance events. Amino Acids 16: 71–77, 1999.
    1. Warren MP, Perlroth NE. The effects of intense exercise on the female reproductive system. J Endocrinol 170: 3–11, 2001.
    1. Webster CC, Noakes TD, Chacko SK, Swart J, Kohn TA, Smith JA. Gluconeogenesis during endurance exercise in cyclists habituated to a long-term low carbohydrate high fat diet. J Physiol 594: 4389–4405, 2016.
    1. Yanovich R, Evans RK, Friedman E, Moran DS. Bone turnover markers do not predict stress fracture in elite combat recruits. Clin Orthop Relat Res 471: 1365–1372, 2013.
    1. Young VR, El-Khoury AE, Raguso CA, Forslund AH, Hambraeus L. Rates of urea production and hydrolysis and leucine oxidation change linearly over widely varying protein intakes in healthy adults. J Nutr 130: 761–766, 2000.
    1. Zetterberg H, Hietala MA, Jonsson M, Andreasen N, Styrud E, Karlsson I, Edman A, Popa C, Rasulzada A, Wahlund LO, Mehta PD, Rosengren L, Blennow K, Wallin A. Neurochemical aftermath of amateur boxing. Arch Neurol 63: 1277–1280, 2006.
    1. Zetterberg H, Tanriverdi F, Unluhizarci K, Selcuklu A, Kelestimur F, Blennow K. Sustained release of neuron-specific enolase to serum in amateur boxers. Brain Inj 23: 723–726, 2009.
    1. Zhu YI, Haas JD. Altered metabolic response of iron-depleted nonanemic women during a 15-km time trial. J Appl Physiol (1985) 84: 1768–1775, 1998.
    1. Zoller H, Vogel W. Iron supplementation in athletes–first do no harm. Nutrition 20: 615–619, 2004.

Source: PubMed

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