Elsevier

Psychoneuroendocrinology

Volume 38, Issue 7, July 2013, Pages 1122-1132
Psychoneuroendocrinology

Diurnal patterns of salivary alpha-amylase and cortisol secretion in female adolescent tennis players after 16 weeks of training

https://doi.org/10.1016/j.psyneuen.2012.11.001Get rights and content

Summary

We examined the effects of 16 weeks of training on diurnal pattern of salivary alpha-amylase (sAA), cortisol, and the ratio of sAA over cortisol (AOC) in 12 national adolescent female tennis players. Stress and recovery were also evaluated using the Recovery-Stress-Questionnaire for Athletes-RESTQ-Sport. Data were collected after a 2-week rest (January, W0), and 4 months after W0 (W16). Subjects collected five saliva samples throughout a day. While all participants displayed the previously shown decrease after awakening in adolescents at W0, they showed a rise in the alpha-amylase awakening response and a higher alpha-amylase activity output (p < 0.01) at W16 compared to W0. For the daily rhythm of cortisol we found subjects having a low overall output of salivary cortisol (p < 0.01) and a blunted response to awakening at W16. Furthermore, an increase in the ratio AOC at W16, and a negative correlation between this ratio and Sport-specific recovery score. Our findings offer support for the hypothesis that increase of training load during the study period induced asymmetry activation between the two stress systems, in relation to psychological alterations and performance decrease. These results provide encouragement to continue exploring the impact of training program using a psychobiological approach among young athletes in order to prevent fatigue and preserve the health of these athletes.

Introduction

Young athletes, wishing to reach the highest level of performance, engage in intensive training program that requires several hours of training per day (Georgopoulos et al., 2011). This pressured schedule often induces little opportunity for recovery (Matos et al., 2011). A sustained mismatch between the load of training and recovery can lead to overreaching (OR). OR is characterized by a short-term decrement in sport specific performance and is often coupled with psychological symptoms (Brink et al., 2012). OR can be further classified as either functional overreaching (FOR) or non-functional overreaching (NFOR) with the criteria for each based on the duration of performance decrement and severity of symptoms (Meeusen et al., 2006, Matos et al., 2011). FOR refers to a short-term performance decrement (i.e., days to weeks) with a planned recovery period, while NFOR is the more severe condition where performance decrement lasts longer (weeks or months) and usually presents with more severe symptoms. The overtraining syndrome (OTS) is the final stage of the continuum with recovery periods lasting from months to years (Meeusen et al., 2006). The avoidance of OR and the achievement of optimal performance can be only realized when athletes are able to recover and optimally balance training stress and subsequent recovery (Kellmann and Kallus, 2001). These complex effects of stress and recovery may be evaluated through the Recovery-Stress Questionnaire for Athletes (RESTQ-Sport), which assesses the frequency of experienced stressors and regeneration related activities (Nederhof et al., 2008).

In comparison to adults, our knowledge of the OTS in elite young athletes is lacking, and knowledge regarding health outcomes related to youth sport specialization is limited (Capranica and Millard-Stafford, 2011). Some studies indicate an incidence of 30%, with relatively higher occurrence seen in individual sport, females and those competing at the highest representative levels (Raglin, 1993, Matos et al., 2011). Recently, the International Olympic Committee has recommended international federations to monitor the volume and intensity of training and competition, considering that young athletes could be exposed to an excessive psychophysiological stress (Mountjoy et al., 2008). The availability of noninvasive lightweight equipment (i.e., portable lactate analyzers, saliva collectors) and the cooperation with sport federations allowed a multidisciplinary approach to examine physiological and psychological contributors to stress in individual athletes (Capranica and Millard-Stafford, 2011), and to evaluate the balance in allostasis (meaning literally “maintaining stability or homeostasis”), defined in terms of ability to achieve stability through change (Minetto et al., 2008).

The most common allostatic responses involve the sympathetic adrenomedullary system (SAM) with the secretion of catecholamines and the hypothalamic-pituitary-adrenal (HPA) axis with the secretion of cortisol (Urhausen et al., 1998). In a general manner, allostatic load is a framework, which asserts that the cumulative burden of stress manifests as physiological dysregulation across multiple, interrelated systems involved in restoring allostasis and maintaining healthy functioning in the presence of internal or environmental demands (McEwen, 1998). This “load” is typically indicated by elevated (or reduced) levels across neuroendocrine markers of the sympathetic-adrenal-medullary (SAM; i.e., adrenaline and noradrenaline) and hypothalamic-pituitary-adrenal (HPA) axis (i.e., cortisol) (Gallo et al., 2011). It has also been shown that the degree of dysregulation associated with chronic stress could depend markedly on subjective distress, personality and coping resources, and the social context in which stress occurs (Chun et al., 2006). Acute intense exercise activates the HPA axis, while intense physical training, by acting as a chronic repeated stress, leads to a reduced HPA axis reactivity (Urhausen et al., 1998). Salivary cortisol sampling has been used as a measure for HPA axis activity for quite some time (Kirschbaum and Hellhammer, 1994). One method to analyze cortisol secretory activity is the assessment of saliva cortisol levels after awakening when hormone concentrations strongly increase until 30 min after awakening and decrease thereafter (Pruessner et al., 1997). The cortisol awakening response (CAR; the difference in cortisol from awakening to some period after awakening) has been introduced as a measure of cortisol reactivity and appears to be a distinct phenomenon superimposing the circadian rhythm of cortisol (Wilhelm et al., 2007). CAR also allows repeated assessment and has been shown to have a high intra-individual stability (Clow et al., 2004). As alterations of the CAR may reveal subtle changes in the HPA axis activity, this parameter has been investigated in several patient groups. In many disorders including chronic fatigue syndrome, posttraumatic stress disorder, or sleep disorder, a blunted CAR has been observed when comparing patients with healthy controls (Fries et al., 2009). To our knowledge, limited information is available concerning the CAR and diurnal variations of cortisol concentrations in athletes, Georgopoulos et al. (2011) showing an abolished diurnal rhythm of salivary cortisol in elite artistic gymnasts. A blunted diurnal rhythmicity of cortisol in young male dancers was also reported by Strahler et al. (2010a). These researchers also observed a markedly reduced HPA activity in male martial artists (Strahler et al., 2010b). However, the reason for the reduced basal HPA activity in trained athletes is still unclear. On the contrary, Rohleder et al. (2007) showed that competitive dancing produces substantial increases in cortisol compared to a control day. These increases were not due to the physical load of dancing and responses did not habituate across competitions and were mostly elevated under highly focused conditions of threat, supporting the notion of a social self-preservation system that is physiologically responsive to threats to the social self.

Direct measurements of salivary adrenaline and noradrenaline do not seem to reflect SAM activity (Schwab et al., 1992). The search for a similar non-invasive and easily obtainable marker of the SAM activity has raised salivary alpha-amylase (sAA) as a promising candidate (Filaire et al., 2010, Granger et al., 2007). Pharmacological study in the human also provides direct evidence for the sensitivity of sAA to changes in adrenergic activity and specifically as a marker in reaction to psychological stress (Van Stegeren et al., 2006). sAA is the most important and abundant protein in saliva, and is mostly synthesized by the parotid gland. AA is an enzyme that breaks down starch into maltose and is also important in host defenses, inhibiting the adherence and growth of certain bacteria. Its secretion is under strong neurohormonal control (released upon sympathetic stimulation). Nater et al. (2007) reported a diurnal rhythm of salivary alpha-amylase secretion in humans with a decrease immediately after awakening and a subsequent steadily rise toward the afternoon and the evening. The same diurnal profile was shown in children and adolescents (Wolf et al., 2008). Since the early work of Chatterton et al. (1996), several studies have also underscored the usefulness of variations in sAA in reflecting changes in autonomic activity in sports and exercise (Kivlighan and Granger, 2006, Nater and Rohleder, 2009, Bocanegra et al., 2012, Diaz et al., 2012). In studies using different kinds of physical stimulation, a sympathetic-like response was shown for sAA with rapid increases immediately after the stressor and rapidly declining values afterwards, either in morning or afternoon exercise sessions (Allgrove et al., 2008, Chiodo et al., 2011, Capranica et al., 2012). Recent results collected in controlled laboratory conditions also showed that a short-duration incremental exercise to exhaustion determines a temporary increase in sAA (Gallina et al. (2011). Studies investigating the cumulative effects of repeated or chronic stress on sAA rhythmicity are rare. Nater et al. (2007) reported an association between chronic stress and increases in daytime sAA concentrations. Strahler et al. (2010a), who have worked on the sAA in relation to awakening responses and the diurnal profile in the athletes, found a flattened diurnal profile of sAA in young male dancers which might be an effect of repeated stressful experiences. Recently, Ali and Pruessner (2012) have suggested that HPA axis and SAM work in coordination to mediate the physiologic response to perceived stressor, whereby a blunting of the HPA axis activity is associated with an augmented SAM response to stress. They proposed that the ratio of sAA over cortisol (AOC) might be a better marker of chronic stress than sAA or cortisol alone, and can be used in studies investigating chronic dysregulations of the two stress systems as seen in allostatic load.

Results from competitions or training (Kivlighan and Granger, 2006, Filaire et al., 2009, Bresciani et al., 2012) indicate that the concomitant measurement of psychological and hormonal parameters offers a unique possibility to achieve a more comprehensive evaluation of the stress responses of an athlete. Relatively little evidence exists regarding the long-term effects of training on children in specific sports (Filaire et al., 2003, Chiodo et al., 2011, Capranica and Millard-Stafford, 2011), and to our knowledge, no study has evaluated the physiological and psychological responses in junior tennis players in relation to practice volumes and annual months competing. Tennis requires physical, mental, and emotional skills, and is characterized by a high degree of physical and psychological stress due to intensive training based on repetition of strokes and to sequences of training and matches each week, without recuperation (Therminarias et al., 1990, Hornery et al., 2007, Jayanthi et al., 2011). In youth, competitive players usually compete in between 15 and 25 tournaments per year, which results in 50–120 competitive single matches (Filaire et al., 2009). Recovery is often overlooked or worse taken for granted (Jayanthi et al., 2011). However, to date, the effect of chronic physical and psychological stress induced by tennis training is not well understood, especially among young people, even if some recommendations are beginning to be issued (Jayanthi et al., 2011).

Therefore, the aim of this study was to evaluate the effects of 16 weeks of tennis training and matches on psychological and physiological stress indicators in adolescent female tennis players and to examine possible dysregulation of HPA and SAM axis during this period. Based on the most recent study of Ali and Pruessner (2012), it was hypothesized that this 16-week training creates a high load for the tennis players and would induce a blunting of the HPA axis activity, an elevated SAM response to stress, and higher AOC values compared to low load period. Based on our previous study (Bouget et al., 2006), it was also hypothesized that alterations in cortisol concentrations as a result of heavy training stress would be positively related to the change for somatic component of stress evaluated through the RESTQ-Sport.

Section snippets

Participants

Twelve female tennis players, mean age 14.8 ± 0.6 years (SD), range 13.5–15.3 years, participated in this study which lasted 4 months from January until April. They had been involved in this sport for 7.3 ± 0.3 (SD) years and trained tennis five days a week (15.6 ± 1.8 h week−1) in addition to two physical training session (3 h week−1), and matches and their usual correspondence school activities. They participated in national and international level competitions. All tennis players followed a similar

Results

The characteristics of the group are shown in Table 1.

Weight/height2 ratio (kg/m2) assigned the women to the 50% percentile of the national French data. Four months of training did not result in any changes in anthropometric variables (Table 1).

Training load (AU for arbitrary units) increased in W16 (p < 0.001) compared to this noted at W0. Between W0 and W16, the tennis players participated in both national and international tournaments and won 48% of their matches. For comparison, they won 72%

Discussion

To our knowledge, this is the first study to focus on the psychobiological response to tennis training, and to investigate the effects of chronic/repetitive stress on HPA/SAM axis regulation in adolescent female tennis players. As noted by Capranica and Millard-Stafford (2011), the examination of stress-related psychobiological responses of young athletes is particularly relevant to establish the recovery of these athletes.

For the daily rhythm of cortisol we found subjects having a low overall

Limitations and conclusion

There are a number of limitations to our study. First, it is not possible to generalize findings from elite athletes to populations of different sports or fitness levels. Secondly, we used a small sample size that cannot generalize our findings, even if a small sample size is strongly encouraged to maximize homogeneity of the sample. Third, the absence of a control group makes us unable to filter out threats to experimental validity. Finally, another limitation is that when investigating elite

Role of the funding source

This research was supported by the Laboratoire CIAMS, EA4532 and the Orleans University.

Conflicts of interest

None declared.

Acknowledgement

We have no acknowledgements.

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