Downloaded from bjsm.bmj.com on April 5, 2012 - Published by group.bmj.com BJSM Online First, published on December 14, 2011 as 10.1136/bjsports-2011-090492 Original article Monitoring performance, pituitary–adrenal hormones and mood profiles: how to diagnose non-functional over-reaching in male elite junior soccer players Sándor L Schmikli,1 Wouter R de Vries,1 Michel S Brink,2 Frank JG Backx1 1Rudolf Magnus Institute of Neuroscience, Department of Rehabilitation, Nursing Science and Sport, University Medical Center Utrecht, Utrecht, The Netherlands 2Center for Human Movement Sciences, University Medical Center Groningen, Groningen, The Netherlands Correspondence to Sandor Schmikli, Department of Rehabilitation, Nursing Science and Sport, University Medical Center Utrecht, Research coordinator Sports Medicine, Heidelberglaan 100, 3508 GA, The Netherlands; [email protected] Received 12 August 2011 Accepted 12 November 2011 ABSTRACT Objective To verify if in male elite junior soccer players a minimum 1-month performance decrease is accompanied by a mood profile and hormone levels typical of non-functional over-reaching (NFOR). Design A prospective case-control study using a monthly performance monitor with a standardised field test to detect the performance changes. Players with a performance decrease lasting at least 1 month were compared with control players without a performance decrease on mood scores and pre-exercise and postexercise levels of stress hormones. Setting Sporting field and sports medical laboratory. Participants Ninety-four young elite soccer players were monitored during the 2006–2008 seasons. Twenty-one players were invited to the laboratory, seven of whom showed a significant performance decrease. Main outcome measures Performance change over time, scores on the profile of mood states and premaximal and postmaximal exercise serum levels of adrenocorticotropic hormone (ACTH), growth hormone (GH) and cortisol. Results Players with a performance decrease showed psychological and hormonal changes typical of the nonfunctional state of over-reaching. Scores were higher on depression and anger, whereas the resting GH levels and ACTH levels after maximal exercise were reduced. ACTH and GH were capable of classifying all but one player correctly as either NFOR or control. Conclusions Performance-related criteria in field tests are capable of identifying players with worsened mood and adaptations of the endocrine system that fit the definition of NFOR. Performance, mood and hormone levels may therefore be considered as valid instruments to diagnose NFOR in young elite soccer players. INTRODUCTION Over the past 30 years, much attention has been given to the hormones of the hypothalamus-pituitary axis in studies examining the markers of the overtraining process. In 1998, Lehman et al1 suggested that the overtraining syndrome (OTS) was the result of a malfunctioning of the regulatory processes in the hypothalamus and the pituitary. However, in 1991, Fry et al2 already mentioned that in addition to a reduced pituitary response due to a reduced pituitary sensitivity to hypothalamic stimulation, a decreased sensitivity to adrenocorticotropic hormone (ACTH) at the adrenal gland could also explain why overtrained athletes showed reduced levels of cortisol (C) in response to stress. In fact, in 1985, Barron et al 3 reported that a pharmacological stress test (insulin-induced Copyright (or theirMed employer) 2011. Produced by Schmikli SL, de VriesArticle WR, Brinkauthor MS, et al. Br J Sports (2011). doi:10.1136/bjsports-2011-090492 hypoglycaemia) showed reduced growth hormone (GH), prolactin and ACTH responses in overtrained athletes. Many other hormones produced by the pituitary gland have been studied (eg, luteinising hormone, follicle stimulating hormone) in the subsequent years, but the current consensus is that no single objective marker can reliably identify the OTS.4–8 The lack of any scientific evidence for diagnostic parameters in OTS is associated with various methodological issues, the lack of uniform definitions, and as a result an inconsistent use of the terms over-reaching (OR), overtraining (OT) or the OTS.4 5 7 9–12 Evidently, this makes any interpretation of the results from previous studies with subjects anywhere between a compensated and a decompensated state of adaptation13 to stress extremely difficult. A lack of uniformity must have been one of the arguments to rephrase defi nitions, terms and the timeframe in the process of overtraining in a position statement8 in 2006, in which the process of overtraining was divided into three phases. It was suggested that functional OR (FOR) would last only days to weeks, the latter being similar with general OR according to Kreider.10 An underperformance persisting for weeks or months was associated to a transitional state called ‘non-functional OR’ (NFOR). Longer periods of underperformance were then linked to the OTS. Until now, only a small number of studies reported the hormone levels in NFOR athletes.14–17 Unfortunately, none of the studies on NFOR provided characteristics typical to the transition of FOR to NFOR. Either the studies failed to induce NFOR14 15 or NFOR was diagnosed retrospectively several months after the transition took place.16 17 According to Uusitalo,18 prevention is still the best treatment in OTS. However, if an unknown process causes any disease or syndrome, the opportunity to intervene and prevent such a process should be sought in its earliest stages: when the fi rst signs and symptoms (SAS) appear. According to the latest model in OTS,8 such SAS should be associated to the point that FOR evolves into NFOR. Therefore, in a prospective case-control study, the aim was to detect the early markers of NFOR in a group of young elite soccer players. In accordance with the Steinacker model,13 it was hypothesised that ACTH, C and GH responses to (physical) stress should be reduced in NFOR players, and particularly that reduced C levels would be related to a reduced adrenal sensitivity to ACTH. Premaximal and postmaximal exercise levels of these hormones in blood were compared between players BMJ Publishing Group Ltd under licence. 1 of 6 Downloaded from bjsm.bmj.com on April 5, 2012 - Published by group.bmj.com Original article showing a persistent reduction in the performance lasting more than 4 weeks and control players without a performance reduction. To confi rm the diagnosis of NFOR further, differences in mood (profi le of mood states (POMS)) were also tested for. Finally, we evaluated the diagnostic qualities of NFOR. Table 1 Average mood scores* of seven NFOR players and 12 controls prior to maximal exercise testing NFOR Control Depression† Anger† Fatigue Vigour Tension 6.9 (2.8) 1.3 (0.7) 11.3 (1.1) 3.8 (1.1) 6.6 (1.2) 5.1 (0.8) 12.1 (1.1) 11.5 (0.8) 6.0 (1.8) 3.0 (0.8) *N=19, 2 control cases missing, SEM in brackets. †Significant group difference (p<0.05). NFOR, non-functional over-reaching. METHODS Subjects Of the 94 young elite soccer players (mean age 16.5 years, range 15–18 years), 21 players were included for laboratory testing during the 2006/2007 and 2007/2008 season (seven players with a performance decrease and 14 controls). Selection for laboratory testing during a competitive season took place on a monthly basis using performance changes measured in sportspecific field tests. Young elite soccer players with a persistent performance decrease lasting at least 1 month, that is, measured at two consecutive field tests, were suspected of NFOR (hereafter NFOR players). Controls were randomly selected from the same age group only if they did not show a performance decrease for at least 1 month. Controls were invited and tested at the laboratory within 7 days after the last performance test. The study was approved by the Dutch Central Committee on Research Ethics involving Human Subjects (study no: NL12864.000.06). All participants provided written informed consent, including both parents if participants were younger than 18 years of age. Interval shuttle run test for soccer players To determine the performance capacity in soccer players, a submaximal interval shuttle run test (ISRT) was used.19 20 During the entire season, the submaximal intensity was set at 70% of the maximal number of runs achieved at the start of the season. An elevated heart rate response indicated a state of over-reaching.21 22 During the outdoor ISRTs, players alternately ran for 30 s and walked for 15 s. The running speed increased from 10 km/h every 90 s up to 15 km/h depending on the baseline maximal running performance. Heart rate (in beats/min) was recorded at 5-s intervals (Polar, Kempele, Finland; Suunto, Vantaa, Finland). The tests were performed every month at the start of a training session as a substitute for the warm-up. A reduced physical fitness and a decreased sports-specific performance over a period of time are the most prominent indicators of NFOR.8 Therefore, players with an elevated heart rate response exceeding the day-to-day variance of ≥5 beats/min 23, and a relative heart rate increase of at least 5% persisting for at least 1 month (and measured at consecutive field tests) were included as NFOR players. Laboratory tests Profile of mood states A validated short version of the POMS24 25 was used containing 32 items in five subscales: ‘tension’, ‘depression’, ‘anger’, ‘fatigue’ and ‘vigour’. Participants responded on a five-point Likert scale ranging from 0 (not at all) to 4 (extremely). Mood profi les were obtained prior to a standardised lunch (about 71% CHO, 19% protein and 10% fat). at 10 km/h until voluntary exhaustion. The test ended after 1-min recovery running. The heart rate was monitored at 5-s intervals (Suunto, Vaanta, Finland; Polar, Kempele, Finland). All exercise tests were supervised by a sports physician. Hormones At least 2 h after the standardised lunch, and within 5 min of the start of the treadmill test (between 13:00 and 15:00 p.m), blood samples were taken under resting conditions in supine position from an antecubital vein in Dickinson vacutainer tubes (Becton Dickinson, Franklin Lakes, New Jersey, USA). Samples were taken again in supine position 1 min after recovery walking had ended, mostly within 20 min after the start of the test. SSTII tubes were used for cortisol and GH and K2E EDTA tubes for ACTH. Samples were immediately stored on ice and transported to the laboratory for subsequent analysis. Serum cortisol was determined by radio immunoassay, whereas serum GH and ACTH levels were determined using chemiluminescence immunoassay. Statistical analyses Statistical analyses were performed with SPSS 17 (SPSS, Chicago, Illinois, USA). Baseline characteristics were described as the means and standard errors of the mean in brackets. Group differences in mood scores, and in pre-exercise and postexercise levels of hormones were tested using analysis of variance. Logistic regression with a forward conditional procedure was used to distinguish NFOR players from controls. A sample size of 21 players allowed us to use a maximum of two hormones as predictors. Goodness of fit for logistic regression models was tested using the Hosmer–Lemeshow test. Collinearity statistics (variance inflation factor (VIF) and tolerance) were provided as a test for the independence of the predictors in the logistic regression model. Sensitivity, specificity and area under the curve (AUC) were provided as indicators of the quality of the classifications. The significance level was set at p<0.05. RESULTS Subjects Seven NFOR players were invited to the laboratory: age (years) 17.1 (0.3), height (cm) 173.3 (2.0) and body weight (kg) 69.9 (2.7). The control group consisted of 14 players: age (years) 17.1 (0.2), height (cm) 179.6 (1.8) and body weight (kg) 69.2 (1.5). Only height showed a borderline group difference (p=0.05). NFOR players with an average submaximal heart rate of 172 beats/min showed an average 6% increase of their submaximal heart rate response (10 beats/min±5) during the ISRT. Exercise test Mood profile A graded maximal exercise test until exhaustion was performed on a treadmill to induce acute fatigue. Players were encouraged to run to exhaustion. The tests were performed between 13:00 and 15:00 p.m. All subjects started with a 3-min warm-up at 8 km/h. Every 2 min, the speed increased by 1 km/h starting The group of NFOR players scored significantly higher on anger (p=0.00) and depression (p=0.03), whereas a trend towards a higher score was found on tension (table 1). Although depression scores were 5.3 times higher in NFOR compared with controls, the smaller significance compared with anger was 2 of 6 Schmikli SL, de Vries WR, Brink MS, et al. Br J Sports Med (2011). doi:10.1136/bjsports-2011-090492 Downloaded from bjsm.bmj.com on April 5, 2012 - Published by group.bmj.com Original article Table 2 Average pre-exercise and postexercise serum hormone levels* in seven NFOR players and 14 controls Pre-exercise NFOR Control Postexercise GH† ACTH 0.17 (0.02) 6.64 (1.89) 21.14 (4.05) 22.57 (2.05) C 0.22 (0.02) 0.28 (0.02) GH‡ ACTH†‡ C 35.80 (10.23) 44.20 (6.44) 51.00 (10.80) 91.50 (8.81) 0.25 (0.04) 0.31 (0.03) *ACTH in ng/l, C in µmol/l, GH in µg/l; SEM in brackets. †Significant group difference (p<0.05). ‡Significant pre-postexercise difference in NFOR and controls (p<0.05). ACTH, adrenocorticotropic hormone; C, cortisol; GH, growth hormone; NFOR, non-functional over-reaching. Figure 1 Pre-exercise growth hormone levels in non-functional over-reaching players and controls. caused by the large variation in the depression scores in the NFOR group. Age, height and body weight were not associated with scores on any of the POMS scales. Hormones Pre-exercise levels Only pre-exercise GH levels showed a statistically significant difference between groups (p=0.03, table 2). Figure 1 shows the individual data of pre-exercise levels of GH, the soccer players, explaining the difference between both groups. Pre-exercise C levels showed a tendency to be higher in controls (p=0.09, table 2). However, as shown in figure 2, these C levels did not increase with increasing levels of ACTH in the NFOR players. This is in contrast with the control players who showed a clear relationship between ACTH and C (r=0.75, p=0.00). Age, height and body weight did not correlate with pre-exercise hormone levels. Postexercise levels Postexercise, all three hormones were higher in controls, but only ACTH showed large enough group differences to reach statistical significance (p=0.01, table 2). Age, height and body weight were not correlated with hormone levels, except for the height on postexercise C (r=0.46, p=0.04). Compared with preexercise levels, ACTH and GH levels increased significantly after the exercise test in both groups (NFOR: ACTH p=0.04, GH p=0.01; controls: ACTH p=0.00, GH p=0.00). Only the postexercise increase of ACTH levels showed a significant group effect (p=0.02, see table 2). Prediction of NFOR with pre-exercise and postexercise hormone levels In a logistic regression model, the pre-exercise GH levels and postexercise ACTH levels classified all but a single control soccer player correctly (overall 95% correct, sensitivity 100%, specificity 93%). With both hormones in the regression equation, the two regression coefficients showed a negative relation with the NFOR status. The AUC in the receiver operating characteristic graph was 99% and the model goodness of fit was high (χ2 =23.0 at p=0.00). Tolerance and VIF were close to one. The only control soccer player who was erroneously classified as an NFOR did show a high level of postexercise ACTH typical for control players. However, he also showed a low level of pre-exercise GH, which is typical for NFOR players. Schmikli SL, de Vries WR, Brink MS, et al. Br J Sports Med (2011). doi:10.1136/bjsports-2011-090492 3 of 6 Downloaded from bjsm.bmj.com on April 5, 2012 - Published by group.bmj.com Original article Figure 2 Pre-exercise C as the function of pre-exercise adrenocorticotropic hormone in non-functional over-reaching players and controls. DISCUSSION Apart from a performance decrease as a primary criterion, NFOR soccer players in this study also showed a deteriorated mood with increased anger and depression score. The results on mood differences parallel the earliest reports about mood changes in overtraining by Morgan et al, 26 for example, describing female swimmers after 4 weeks overload with significantly increased anger and depression scores. However, in the Morgan article, 26 studies with similar short-term overload periods also showed that mood rapidly responded to the periods of increased training load, as well as to tapering during macrocycles. To prevent overestimation of the severity of this type of overload, one could choose to monitor mood on a frequent basis and for longer period of time, including taper periods. Alternatively, the interpretation of mood changes could be paired with a performance assessment, given that a more severe imbalance between load and recovery will likely increase the risk of a deteriorated mood and performance. 7 The latter method is integrated in our study design, supporting the conclusion of an imbalance between (physical and mental) load and recovery in NFOR soccer players. It is assumed that the resting levels of C do not change in short-term overtraining/over-reaching. 7 According to the defi nition, as discussed in the introduction, a short-term overtraining/over-reaching does no last more than 4 weeks. However, our NFOR players were included with a performance decrease lasting at least 1 month (but with a maximum of 2 months), indicating that they had passed the state of short-term overtraining/over-reaching. In overtrained athletes, reduced resting C levels have been confi rmed.6 27 28 Compared with controls, the pre-exercise levels of C in the NFOR players were close to significantly reduced, and 4 of 6 differed only marginally from what was found in our previous study with a mixed sample of subjects. 29 A significant interaction of the resting ACTH with C levels was found only in controls, suggesting that a decoupling of C to ACTH may exist in NFOR players. However, the interaction in the controls did not significantly differentiate the NFOR players from controls. Until now, no studies confi rmed the changes in resting GH levels in the over-reached or overtrained athletes. In our controls, GH levels of six control players exceeded 5 μg/l. In contrast, none of the NFOR players showed GH levels above 0.5 μg/l (see fi gure 1), explaining the significant difference between both groups (see table 2). As the results of the field performance tests in NFOR players indicate a reduced physical fitness, the observed significant difference for the preexercise levels of GH may be related to differences in physical fitness between both groups. 30 This is in line with the observations that improving physical fitness by training enhances GH secretion. 31 In addition, these data indicate that control players may profit from more anabolic action of GH than NFOR players. In a training experiment with horses, 32 the authors induced a form of FOR at the end of the training period as no clear drop of performance was found. The intensively trained (IT) horses, however, showed acute compensating anabolic effects: more frequent and amplified nocturnal peaks in GH, reflecting an adaptational process to restore homeostasis. Possibly, our control players also displayed active recovery similar to the IT horses, with our NFOR players lacking the ability to produce this compensatory effect. It is often stated that reduced pituitary and adrenal activity after physical or mental stress may be a hallmark in overreached and overtrained athletes. 3 13 32–34 In this study, a reduced pituitary activity was only confi rmed with the Schmikli SL, de Vries WR, Brink MS, et al. Br J Sports Med (2011). doi:10.1136/bjsports-2011-090492 Downloaded from bjsm.bmj.com on April 5, 2012 - Published by group.bmj.com Original article Competing interests None. What is already known on this topic Ethics approval CCMO The Hague and local Medical Ethics Committee, Utrecht, The Netherlands. In contrast to the functionally over-reached athletes, nonfunctionally over-reached (NFOR) athletes share prolonged periods of reduced performance, mood problems and neuroendocrine disturbances. Early recognition of NFOR may be the key to the timing in a successful prevention of the overtraining syndrome. Until now, there is no valid instrument to diagnose NFOR in athletes. Provenance and peer review Not commissioned; externally peer reviewed. REFERENCES 1. 2. 3. 4. What this study adds A prolonged reduction of the performance with worsened mood, a reduced anabolic activity at rest and a reduced pituitary activation after maximal exercise are characteristic for NFOR in elite junior soccer players. Pre-exercise growth hormone and postexercise adrenocorticotropic hormone levels have shown a strong potential to define a diagnostic criteria for NFOR. 5. 6. 7. 8. 9. 10. 11. postexercise ACTH response in NFOR players, which was only 43% of the response in controls. The postexercise GH and C levels in both groups indicate that the pituitary–adrenal responses were similar. Therefore, the hypothesis that ACTH, C and GH responses to physical stress should be reduced could only partially be confi rmed. However, a reduced adrenal activity cannot be excluded, because lower postexercise C levels in NFOR players may have been obscured by our laboratory protocol. Our protocol is compatible with the laboratory protocol used in previous studies,11 16 17 35 which means that blood was taken to measure the C levels within minutes after maximal performance. However, it is well known that maximal C responses to exercise are delayed by as much as 30 min, 36 indicating that true maximal C levels may still be reduced in NFOR players. In future studies, we will apply a modified protocol allowing for an added C test 30 min after maximal exercise to further explore pituitaryadrenal responses in NFOR. Despite the fact that the number of cases only allowed for two diagnostic parameters in the logistic regression procedure, the distinguishing qualities of a model with preexercise GH and postexercise ACTH are very good. Low preexercise GH levels indicate that NFOR players are compensating for an imbalance between load and recovery with reduced anabolic activity at rest, whereas under stress low ACTH levels reveal a partial collapse of the pituitary-adrenal axis. This illustrates the neuroendocrine signals of an initial, overtrained (NFOR) state, associated with a reduced performance and worsened mood in young elite soccer players. However, more research is necessary to prove that this model is valid and reliable before it can be put into practice. Furthermore, the development of a similar diagnostic model in male and female athletes from different types of sports will demand additional and specific data. Acknowledgement The authors wish to thank Dr Adam Weir for his assistance in writing this manuscript. Funding Funding has been received by ZonMw, the Hague (project number 75020006). 12. 13. 14. 15. 16. 17. 18. 19. 20. 21. 22. 23. 24. 25. 26. 27. 28. 29. 30. Lehmann M, Foster C, Dickhuth HH, et al. Autonomic imbalance hypothesis and overtraining syndrome. Med Sci Sports Exerc 1998;30:1140–5. Fry RW, Morton AR, Keast D. Overtraining in athletes. An update. Sports Med 1991;12:32–65. Barron JL, Noakes TD, Levy W, et al. Hypothalamic dysfunction in overtrained athletes. J Clin Endocrinol Metab 1985;60:803–6. Gleeson M. Biochemical and immunological markers of overtraining. J Sports Sc Med 2002;2:31–41. Armstrong LE, VanHeest JL. The unknown mechanism of the overtraining syndrome: clues from depression and psychoneuroimmunology. Sports Med 2002;32:185–209. Urhausen A, Kindermann W. Diagnosis of overtraining: what tools do we have? Sports Med 2002;32:95–102. Halson SL, Jeukendrup AE. Does overtraining exist? An analysis of over-reaching and overtraining research. Sports Med 2004;34:967–81. Meeusen R, Duclos M, Gleeson M, et al. Prevention, diagnosis and treatment of the overtraining syndrome. Eur J Sport Sci 2006;6:1–14. Hawley CJ, Schoene RB. Overtraining syndrome: a guide to diagnosis, treatment, and prevention. Phys Sportsmed 2003;31:25–31. Kreider RB, Fry AC, O’TooleML. Overtraining in sport: terms, definitions, and prevalence. In: Kreider RB, Fry AC, O’Toole ML, eds. Overtraining In Sport. Champaign, Illinois: Human Kinetics 1998. Meeusen R, Piacentini MF, Busschaert B, et al. Hormonal responses in athletes: the use of a two bout exercise protocol to detect subtle differences in (over) training status. Eur J Appl Physiol 2004;91:140–6. Slivka DR, Hailes WS, Cuddy JS, et al. Effects of 21 days of intensified training on markers of overtraining. J Strength Cond Res 2010;24:2604–12. Steinacker JM, Lormes W, Reissnecker S, et al. New aspects of the hormone and cytokine response to training. Eur J Appl Physiol 2004;91:382–91. Moore CA, Fry AC. Nonfunctional over-reaching during off-season training for skill position players in collegiate American football. J Strength Cond Res 2007;21:793–800. Coutts AJ, Wallace LK, Slattery KM. Monitoring changes in performance, physiology, biochemistry, and psychology during over-reaching and recovery in triathletes. Int J Sports Med 2007;28:125–34. Nederhof E, Zwerver J, Brink M, et al. Different diagnostic tools in nonfunctional over-reaching. Int J Sports Med 2008;29:590–7. Meeusen R, Nederhof E, Buyse L, et al. Diagnosing overtraining in athletes using the two-bout exercise protocol. Br J Sports Med 2010;44:642–8. Uusitalo AL. Overtraining: making a difficult diagnosis and implementing targeted treatment. Phys Sportsmed 2001;29:35–50. Lemmink KAPM, Visscher C. The relationship between the interval shuttle run test and maximal oxygen uptake in soccer players. J Hum Movement Stud 2003;45:219–32. Lemmink KA, Visscher C, Lambert MI, et al. The interval shuttle run test for intermittent sport players: evaluation of reliability. J Strength Cond Res 2004;18:821–7. Kuipers H, Keizer HA. Overtraining in elite athletes. Review and directions for the future. Sports Med 1988;6:79–92. Kindermann W. Expression of a disturbed autonomic regulation. Dtsch Z Sportmed 1986;37:238–45. Lamberts RP, Lambert MI. Day-to-day variation in heart rate at different levels of submaximal exertion: implications for monitoring training. J Strength Cond Res 2009;23:1005–10. Wald FDM, Mellenbergh GJ. The short Dutch version of the Profile of Moods States (POMS) questionnaire. Ned Tijdschr Psychol 1990;45:86–90. Wicherts JM, Vorst HCM. Model adaptation of the short version of the profile of moods states and variance between males and females. Nederl Tijdschr Psychol 2004;59:2–21. Morgan WP, Brown DR, Raglin JS, et al. Psychological monitoring of overtraining and staleness. Br J Sports Med 1987;21:107–14. Urhausen A, Gabriel H, Kindermann W. Blood hormones as markers of training stress and overtraining. Sports Med 1995;20:251–76. Uusitalo AL, Huttunen P, Hanin Y, et al. Hormonal responses to endurance training and overtraining in female athletes. Clin J Sport Med 1998;8:178–86. Schmikli SL, Brink MS, de Vries WR, et al. Can we detect non-functional overreaching in young elite soccer players and middle-long distance runners using field performance tests? Br J Sports Med 2011;45:631–6. Weltman A, Weltman JY, Hartman ML, et al. Relationship between age, percentage body fat, fitness, and 24-hour growth hormone release in healthy young adults: effects of gender. J Clin Endocrinol Metab 1994;78:543–8. Schmikli SL, de Vries WR, Brink MS, et al. Br J Sports Med (2011). doi:10.1136/bjsports-2011-090492 5 of 6 Downloaded from bjsm.bmj.com on April 5, 2012 - Published by group.bmj.com Original article 31. 32. 33. 6 of 6 Weltman A, Weltman JY, Schurrer R, et al. Endurance training amplifies the pulsatile release of growth hormone: effects of training intensity. J Appl Physiol 1992;72:2188–96. de Graaf-Roelfsema E, Veldhuis PP, Keizer HA, et al. Overtrained horses alter their resting pulsatile growth hormone secretion. Am J Physiol Regul Integr Comp Physiol 2009;297:R403–11. Snyder AC, Kuipers H, Cheng B, et al. Overtraining following intensified training with normal muscle glycogen. Med Sci Sports Exerc 1995;27:1063–70. 34. 35. 36. Urhausen A, Gabriel HH, Kindermann W. Impaired pituitary hormonal response to exhaustive exercise in overtrained endurance athletes. Med Sci Sports Exerc 1998;30:407–14. Ronsen O, Haug E, Pedersen BK, et al. Increased neuroendocrine response to a repeated bout of endurance exercise. Med Sci Sports Exerc 2001;33:568–75. de Vries WR, Bernards NT, de Rooij MH, et al. Dynamic exercise discloses different time-related responses in stress hormones. Psychosom Med 2000;62:866–72. Schmikli SL, de Vries WR, Brink MS, et al. Br J Sports Med (2011). doi:10.1136/bjsports-2011-090492 Downloaded from bjsm.bmj.com on April 5, 2012 - Published by group.bmj.com Monitoring performance, pituitary−adrenal hormones and mood profiles: how to diagnose non-functional over-reaching in male elite junior soccer players Sándor L Schmikli, Wouter R de Vries, Michel S Brink, et al. Br J Sports Med published online December 14, 2011 doi: 10.1136/bjsports-2011-090492 Updated information and services can be found at: http://bjsm.bmj.com/content/early/2011/12/14/bjsports-2011-090492.full.html These include: References This article cites 35 articles, 8 of which can be accessed free at: http://bjsm.bmj.com/content/early/2011/12/14/bjsports-2011-090492.full.html#ref-list-1 P<P Email alerting service Topic Collections Published online December 14, 2011 in advance of the print journal. Receive free email alerts when new articles cite this article. Sign up in the box at the top right corner of the online article. Articles on similar topics can be found in the following collections Football (soccer) (164 articles) Notes Advance online articles have been peer reviewed, accepted for publication, edited and typeset, but have not not yet appeared in the paper journal. 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