Psychology 2013. Vol.4, No.7, 613-618 Published Online July 2013 in SciRes (http://www.scirp.org/journal/psych) http://dx.doi.org/10.4236/psych.2013.47087 Copyright © 2013 SciRes. 613 Elite Sport and Biological Age Influence of Extensive or Regular Low to Moderate Exercise on Plasma DHEA-S and Cortisol in Ice-Hockey Players Benny Johansson1, Lars-Eric Uneståhl2 1Scandinavian International University, Örebro, Sweden 2Örebro University, Örebro, Sweden Email: info@siu.nu, benny@akloma.com Received April 21st, 2013; revised May 23rd, 2013; accepted June 22nd, 2013 Copyright © 2013 Benny Johansson, Lars-Eric Uneståhl. This is an open access article distributed under the Creative Commons Attribution License, which permits unrestricted use, distribution, and reproduction in any medium, provided the original work is properly cited. Based on common comments that elite players in soccer and ice-hockey often looked “older” than non- players of the same age, the authors examined the research literature but found that very few studies had been conducted in the area of elite sport and biological age. We therefore decided to conduct a pilot study comparing professional elite ice hockey players (EP) (22 males, M = 24.7 years) with a cohort of amateur players (AP) similar in age but from a lower competitive level (17 males, M = 25.4 years). Subjective ratings of motivational, attitude and emotional factors were combined with measurements of blood con- centrations of DHEA-S, cortisol and the DHEA-S/cortisol ratio. DHEA-S and the DHEA-S/cortisol ratio were significantly higher (p < 0.01) while cortisol was unaffected in the AP compared with the EP group. Interpretation of the differences in adrenal hormones level indicated a biological age difference of around 10 years, with the EP group being older. Also, significant differences in the subjective ratings were noted with a more positive self-image, goal-image, attitude and emotions noted in the AP-group. As we have earlier demonstrated a decrease in biological age with mental training of these factors, further studies have to determine how much the higher biological age among the EP-group is due to exercise factors, ex- periential/personal factors or a combination of these and other factors. Keywords: Competitive Sport; Biological Age; Stress; Adrenal Hormones; Emotional Factors; Lifestyle Hypothesis The process of biological aging goes faster in elite athletes compared with athletes from a lower level. If so, the difference in biological age depends on a combina- tion of factors, of which two have been investigated in this study: 1) The frequency and intensity of the physical training (physical stress); 2) How differences in physical and mental stress levels effect psychological and personality dimensions with relations to bio- logical age. Introduction Many studies have been conducted to determine the health effects of physical exercise and competitive sport (Blair, Cheng, & Holder, 2001; Kriska, Saremi, Hanson, Bennett, Kobes, Wil- liams, & Knowler, 2003; Pate, Pratt, Blair, Haskell, Macera, Bouchard, Buchner, Ettinger, Heath, King, Kriska, Leon, Mar- cus, Morris, Paffenbarger, Patrick, Pollock, Rippe, Sallis, & Wilmore, 1995; Fogelholm, Kaprio, & Sarna, 1994; Haskell, Lee, Pate, Powell, Blair, Franklin, Macera, Heath, Thompson, & Bauman, 2007), but the “dose-response” as well as type, optimal intensity and duration of exercise for wellbeing and good health remains unclear (Blair, LaMonte, & Nichman, 2004; Kesaniemi, Danforth, Jensen, Kopelman, Lefebvre, & Reeder, 2001). Statistics of longevity of elite athletes from sport have been difficult to find and the few found show con- flicting results (Schnor, 1971; Schnor, 1972; Kujala, Tikkanen, Sarna, Pukkala, Kaprio, & Koskenvou, 2001; Kujala, 2005; Paffenbarger, Hyde, Wing, & Hsieh, 1986; Sanchis-Gomar, Olaso-Gonzales, Corella, Gomez-Cabrera, & Vina, 2011). Sev- eral studies confirm that physical and cardiorespiratory fitness and healthy life style factors contribute to increased average longevity even at long-term strenuous exercise (Fogelholm, Kaprio, & Sarna, 1994; Sanchis-Gomar, Olaso-Gonzales, Corella, Gomez-Cabrera, & Vina, 2011; Lee, Artero, Sui, & Blair, 2010). One explanation of the contradictory results could be that the relation between health levels and competitive sport levels may be described as an inverted U-form relation, where too little and too much may lower health levels compared with a moderate level. Physical exercise and the influence of emotional and psy- chological stress are significant stimuli of the endocrine system. The hypothalamus, pituitary and adrenal glands (HPA-axis) play a central role in the body’s adaptation to stress-related responses (Faredin, Fazekas, Toth, & Juslesz, 1969; Parker, Eugene, Farber, Lifrak, Lai, & Juler, 1985). The typical hor- mone stressors are of physical, emotional, psychological and infectious nature depending on type, intensity, and duration of the stressor and individual characteristics (Endoh, Kristiansen,
B. JOHANSSON, L.-E. UNESTÅHL Casson, Buster, & Hornsby, 1996). The hormonal response to physical exercise depends on several external factors, e.g. in- tensity, duration and mode of exercise (Galbo, Hummer, Petersen, Christensen, & Bie, 1977; Sutton, Coleman, Casey, & Lazarus, 1973; Trembaly, Copeland, & Van Helder, 2004). The regulative response of the HPA-axis towards environmental changes and challenges also involves perceptual and cognitive experiences (Endoh, Kristiansen, Casson, Buster, & Hornsby, 1996). The most important and abundant stress hormone is cortisol (Parker, Eugene, Farber, Lifrak, Lai, & Juler, 1985). The secre- tion of adrenal cortisol in response to stress activation is in a counteracted manner related to the level of dehydroepiandros- terone sulfate (DHEA-S) (Orentreich, Brind, Rizer, & Vogel- man, 1984). The blood concentration of DHEA-S and its pri- mary active analogue dehydroepiandrosterone (DHEA) (Le- owattana, 2001) reflects the biological conditions of acute and chronic stress (Kroboth, Salek, Pittenge, Fabian, & Frye, 1999; Boudarene, Legros, & Timsit-Berthier, 2002). Falling concen- trations have been observed in both mental and psychological stress and physical illness (Boudarene, Legros, & Timsit- Berthier, 2002). The adrenal secretion and blood concentration follows a biphasic time course during lifetime, peaking in the range of 20 - 30 years (Barrett-Conner, Khaw, & Yen, 1986; Baulieu, 1996; Corrigan, 2002). Thereafter, the blood concen- tration is declining by a small percentage yearly (Baulieu, 1996; Wisniewski, Hilton, Morse, & Svec, 1993). Extensive physical load during marathon in male athletes demonstrated that DHEA-S and cortisol were significantly increased (Ponjee, De Rooy, & Vader, 1994). During endurance training, DHEA-S increased in a dose-dependent manner at repeated running sessions for two hours. Cortisol was declined at all running sessions except at two hours, where the response was increased. The ratio of DHEA-S to cortisol was greater at rest and shorter running than at longer runs (Tremblay, Cope- land, & Van Helder, 2005). Plasma DHEA was reported to increase with exercise, depending on the level of performance and intensity of the exercise (Cumming & Rebar, 1985; Valaido, Pantaleoni, & Valeiro, 1991). During 24 h running in men, DHEA-S, was increased over the course of 24 h, while falling level in DHEA-S may be possible using continuous aerobic exercise (Shimizu, Imanishi, Sugimoto, Takeda, Hirata, Andou, Morikawa, Suzuki, Watanabe, Okuta, Kawana, Namikawa, Suzuki, Watanabe, Okada, & Oht, 2011). Even though, cortisol was increased, changes in reactive oxygen spices were within normal range and the adaptation for antioxidation was good, indicating low or moderate stress to the body. In marathon run- ners, lowered cortisol and higher DHEA-S/cortisol ratio corre- lated with lowered leptin and thus more efficient energy expen- diture for the best runners (Bobbert, Mai, Brechtel, Schult, Weger, Pfeiffer, Spranger, & Diederich, 2012). Evaluated from two separate independent studies, the plasma DHEA-S differs by approximately 14% when compared between endurance trained (Tremblay, Copeland, & Van Helder, 2005) and un- trained (Nafziger, Bowlin, Jenkins, & Pearson, 1998) men at comparable age (31 years), the extensively trained men being lower at rest. The exercise in the trained men increased the DHEA-S in a dose-response manner with the greatest increase observed during 2 h run, comparable to the normal plasma level in untrained men. In sportswomen, the ratio of DHEA to cortisol in saliva was increased by more than 30% during a 16 week training pro- gram with no difference between highly trained national and moderately trained regional groups. The athletes with the high- est performance levels and greatest amount of training showed a less increase in the DHEA/cortisol ratio In contrast, the cor- responding ratio was significantly lower in sedentary women (Filaire, Duch, & Lac, 1998). Cortisol did not change with the training over the season and was higher in the elite than in re- gional women. The training program increased significantly DHEA in all sportswomen. In non-athletes, increased plasma DHEA-S has been con- nected with alleviated chronic stress-load (Glaser, Brind, Vo- gelma, Eisner, Dillbeck, Walace, Chopra, Orentreich, 1992; Arlt, Callies, van Vlijmen, Koehler, Reinecke, Bidlingmaier, Huebler, Oettel, Ernst, Schulte, & Allolio, 1999), positive measures of well-being (Cawodd, & Bancroft, 1996), continued moderate physical activity (Keiser, Kuipers, de Haan, Beckers, & Habets, 1987; Caciarri, Mazzanti, Tassinar, Bergamaschi, Magnani, Zappulla, Nanni, Cobianchi, Ghini, Pini, & Tani, 1990) and repetitive application of stress-reducing and relaxa- tion activities (Glaser, Brind, Vogelma, Eisner, Dillbeck, Wal- ace, Chopra, & Orentreich, 1992; Johansson, & Uneståhl, 2005). The aim of this study was to compare elite with amateur ice- hockey players on cognitive and emotional issues and on the integrity of the HPA-axis by assessing the level of the adrenal hormones DHEA and cortisol in order to relate this to biologi- cal age. Subjects and Methods Design The purpose of this study was to monitor the effect of exten- sive or low to moderate training for two teams of male ice- hockey players, on blood concentrations of DHEA-S and corti- sol, the DHEA-S/cortisol ratio and on experiential areas. Sub- jective data were collected from the SMAE factor questionnaire (Unestahl & Bundzen, 1996), which measures self-image, goal-Images, attitude and emotions. One team consisted of highly-trained elite players, playing on national level, while the second team was a low to moderate trained regional ice hockey team. In accordance with previous presented research findings, the blood concentration ratio of DHEA-S/cortisol could serve as a biochemical marker and model for the anabolic/catabolic balance in sportsmen (Adler- creuts, Hakonen, Kuoopasalami, Naveri, Huhtanemi, Tikkanen, Remes, Dessypris, & Karvonen, 1986) with relation to biologi- cal age and to physiological and psychological well-being (Johansson & Uneståhl, 2005). Subjects A group of 39 healthy male volunteers took part in the study; 22 national and 17 regional ice-hockey players. The Elite Play- ers (EP) had an average age of 24.7 years (19 - 33) and the amateur players (AP) averaged at 25.4 years (17 - 35). The EP group consisted of professional ice-hockey players, whereas the players in the AP group were amateur players with ordinary labour work during daytime. None of the participants were taking medication. Both groups were lead by professional coaches. The study was done during the second part of the winter season. All subjects in the EP group were on daily scheduled individual and team-based extensive training pro- Copyright © 2013 SciRes. 614
B. JOHANSSON, L.-E. UNESTÅHL gram except on match days and remained unchanged during the study. The training program during non-match days, comprised of two daily sessions of two hours each. Long-distance and exhausting continental bus transfers provided the transportation of the professional team players away from home competitions. Two competition games were performed on regular weekly basis during the season. The players in the AP group followed a low or moderate training and competition program. Scheduled training was per- formed twice weekly for two hours and a competition game only once a week. Due to the local character and short-distance of transportation at competitions, co-transportation of team players was done by car. The content of the study protocol fol- lowed the recommendations of the local committee of human ethics. Each subject was informed of the test procedures and a written consent was obtained before study start. Subjective Measures Subjective self-reported measurements were made with the Swedish “SMAK” test, measuring the dimension: Self-image (S), Goal-images and Motivation (M), Attitudes (A) and Emo- tions (K). The Test was developed by Unestahl in the 1970’s in cooperation with a number of national teams and the Swedish Olympic Teams 1976 and 1980. It has been used in a number of studies since then, among other in our last study about biologi- cal age (Johansson & Uneståhl, 2005). The test has good reli- ability and validity. The S-factor (Self-Image) has statements related to Self-con- fidence as well as Self-esteem. The Goal-Images covers both Goal-level and Motivation. The Attitude scale has statements related to the Optimist—Not Optimist dimension, and also statements about Mental toughness and Resilience. The “E” factor is intended to measure “Internal Success” (transitory feelings of satisfaction, enjoyment, wellbeing and happiness). Changes in the SMAE factors through Mental Training have earlier been related to a number of psychophysiological and neuroimmunological factors (Johansson & Uneståhl, 2005; Unestahl & Bundzen, 1996; Bundzen, Leissner, Malinin, & Unestahl, 1996; Unestahl, Bundzen, Gavrilova, & Isakov, 2004; Bundzen, Gavrilova, Isakov, & Unestahl, 1998). Collection of B lood and Analysis of Stero i d Hor mo nes Venous blood samples were collected in the morning in Vacutainer® tubes and 5 ml of blood were drawn for each sam- ple. Blood samples were centrifuged immediately and stored frozen at –20˚C until assayed. All plasma samples were ana- lysed in duplicate at an accredited local hospital department of clinical chemistry, according to standard laboratory methods for DHEA-S and cortisol (Beishuizen, Thijs, & Vermes, 2002; Normile, 1998; Labrie, Bélanger, Cusan , Gomez, & Candaz, 1997). Statistical Analysis All descriptive quantitative data were reported as mean ± SD. Comparisons between groups were made by unpaired student’s t-test, while a two-tailed p value < 0.05 was considered as sta- tistical significant. Results Mean plasma DHEA-S, cortisol and the ratio of DHEA-S/ cortisol for the EP and AP groups are given in Figures 1-3, respectively. The plasma concentration of DHEA-S in the EP group was significantly lower (<0.01) compared to the AP- group (Figure 1). The level of plasma cortisol was the same in both groups (Figure 2). The ratio of DHEA-S to cortisol was significantly higher in the EP-group compared with the AP group (p < 0.01), indicating elevated catabolism in professional players with sustained anabolism in amateurs (Figure 3). In the SMAE factor test all personal subjective factors were found to have significantly more positive ratings in the amateurs (AP); 0 2 4 6 8 10 12 14 EP LP Plasma concentration of DHEA-S (μmol/l) Figure 1. Plasma concentration of DHEA-S (Mean ± SD) in the EP and LP groups (**p < 0.01). 0 50 100 150 200 250 300 350 400 450 500 EP LP Plasma concentration of Cortisol (nmol/l) Figure 2. Plasma concentration of cortisol (Mean ± SD) in EP and LP groups. 0 5 10 15 20 25 30 35 40 45 50 EP LP Ratio of plasma concentration of DHEA-S and Cortisol ** Figure 3. Plasma concentration of the DHEA-S/cortisol ratio (Mean ± SD) in the EP and LP groups (**p < 0.01). Copyright © 2013 SciRes. 615
B. JOHANSSON, L.-E. UNESTÅHL Self-image (p = 0.008), Goal images (p = 0.023), Attitudes (p = 0.032), and Emotions (p < 0.001) (Table 1). Thus, in profes- sionals the response of the HPA-axis followed the level of physical exercise reflected in a concomitant emotional and cognitive stress load. Discussion The 33% higher plasma DHEA-S in the AP group corre- sponds to a difference in biological age that according to nor- mal reference observations is approximately 10 years below the average age range in the EP-group. The subjective ratings showed that the amateur ice-hockey players (AP) had signifi- cantly better self-images, were more goal-oriented and moti- vated, were interpreting life in a more positive way and had more of positive emotions. Whether, the difference in biologi- cal age was mainly due to exercise levels or cognitive and emo- tional factors or a combination of these cannot be directly de- termined based on this study. We know from an earlier study (Johansson & Uneståhl, 2005) that mental training of cognitive and emotional factors can raise the DHEA-S/Cortisol ratio (thus suggesting a lowering of the biological age). We also know from a previous study (Unestahl, Bundzen, Gavrilova, & Isakov, 2004) that systematic mental training can increase the tolerance for hard training and prevent the negative effects of “overtrain- ing”, partly due to improved rest and recovery skills. Thus, one contributing explanation of the results of our study could be that the lower intensity of training and matches in the amateur players gave them more time for rest and recover. The plasma DHEA-S and DHEA-S to cortisol ratio were concomitantly higher in the AP group, in spite of no difference in the plasma cortisol between groups. Thus, the lower DHEA-S and the lower DHEA-S to cortisol ratio together with less positive subjective emotional experi- ences among the elite players, agrees with the negative influ- ence of lowered levels of these hormones on both psychological and physiological, physical performance and health outcome (Endoh, Kristiansen, Casson, Buster, & Hornsby, 1996). Since the HPA axis is influenced by psychological, emo- tional or physical stress (Faredin, Fazekas, Toth, & Juslesz, 1969; Parker, Eugene, Farber, Lifrak, Lai, & Juler, 1985; Duran-Bush, Faubert, & Newburg, 2004); Singh, Petrides, Gold, Chrousos, & Deuster, 1999), DHEA-S has been identified as an anti-stress hormone related to the antagonistic action towards cortisol (Boudarene, Legros, & Timsit-Berthier, 2002). The counteracting inter-balanced secretion towards stress and anxi- ety of the most numerous androgen DHEA-S has been a sug- gested force on experience of the positive feeling of wellbeing (Orentreich, Brind, Rizer, & Vogelman, 1984, Boudarene, Legros, & Timsit-Berthier, 2002; Normile, 1998). Tentatively, DHEA-S is involved in conditioning of an emotional state based not only on improved wellbeing and external suc- cess(Glaser, Brind, Vogelma, Eisner, Dillbeck, Walace, Chopra, Orentreich, 1992; Cawodd & Bancroft, 1996; Johansson & Table 1. SMAE personal trait factors in ice-hockey players. Goal-image* Self-image’** Attitude*** Emotion# Amateurs Professionals 2.9 ± 0.5 2.4 ± 0.5 2.2 ± 0.4 1.9 ± 0.35 2.1 ± 0.4 1.7 ± 0.4 1.9 ± 0.4 1.6 ± 0.5 Note: *p = 0.008; **p = 0.024; ***p = 0.032; #p = 0.001. Uneståhl, 2005), but a shift in personal traits aligned with a comfortable attitude towards life-experiences and events built on high emotional internal self-residence. The results indicate that the amateurs are more adapted to a resonance state in a process that allows the individuals to feel the way they want to feel. Such a state of self-development underlies how to make meaning of daily experiences, and is reflected in the success of planning, thinking, and acting (Lo- evinger, 1976; Loevinge, Cohn, Bonneville, Redmore, Streich, Bonneville, Redmore, Streich, & Sargent, 1985; Cook-Greuter, 1999). The process is typically experienced as a seamless fit or harmony between the individual and the environment (Duran- Bush, Faubert, & Newburg, 2004). The unchanged plasma cortisol between groups at restful conditions in the morning before the daily physical exercise begun accompanied with the decrease in the DHEA-S/cortisol ratio in professionals, agrees with findings after moderate physical exercise, which even lead to an increase in plasma cortisol when the exercise was intensified (Adlercreuts, Hakonen, Kuoopasalami, Naveri, Huhtanemi, Tikkanen, Remes, Dessypris, & Karvonen, 1986; Trembaly, Copeland, & Van Helder, 2004). Prolonged over-intense training may lead to an over-strained condition, which may involve mental exhaustion, emotional discomfort and hormonal disturbance in the balance between anabolic and catabolic hormones. Continuing the phy- sical training with unchanged intensity will in such a case have negative effects on physical performance (Adlercreuts, Hakonen, Kuoopasalami, Naveri, Huhtanemi, Tikkanen, Remes, Dessy- pris, & Karvonen, 1986). A study monitoring over-strain in two groups of long-distance runners, identified physiological over- strain from the plasma testosterone/cortisol ratio when it was exceeding 30% (Adlercreuts, Hakonen, Kuoopasalami, Naveri, Huhtanemi, Tikkanen, Remes, Dessypris, & Karvonen, 1986). Besides testosterone, other anabolic hormones have been tested monitoring physical overstrain (Adlercreuts, Hakonen, Kuoopa- salami, Naveri, Huhtanemi, Tikkanen, Remes, Dessypris, & Karvonen, 1986). In this regime, DHEA-S is a precursor hormone of more po- tent androgens involved to restore the consequences of cata- bolic activity and processes (Nafziger, Bowlin, Jenkins, & Pearson, 1998). Since DHEA-S is also a balancing hormone counteracting on the alleviated secretion of cortisol, e.g. after induction of an physiological state impressed by emotional comfort and well-being (Glaser, Brind, Vogelma, Eisner, Dill- beck, Walace, Chopra, & Orentreich, 1992; Johansson & Uneståhl, 2005), the DHEA-S/cortisol ratio has been used fol- lowing the physical load in athletes (Ponjee, De Rooy, & Vader, 1994; Trembaly, Copeland, & Van Helder, 2005; Filaire, Duch, & Lac, 1998). The significant difference in DHEA-S/cortisol ratio (32.7%) between the two groups in our study was strongly aliened with the lower rating in especially the subjective emo- tional measurement in professional ice-hockey players, that may highlight not only the negative influence of professional and elite sports on performance, but the risk of future ill-health (Endoh, Kristiansen, Casson, Buster, & Hornsby, 1996). The age-dependence of plasma DHEA-S and its precursor DHEA, and the proposed preventive and anti-aging effects including their role as biomarkers of physiological aging has been debated and questioned (Kroboth, Salek, Pittenge, Fabian, & Frye, 1999; Shimizu, Imanishi, Sugimoto, Takeda, Hirata, Andou, Morikawa, Suzuki, Watanabe, Okuta, Kawana, Nami- kawa, Suzuki, Watanabe, Okada, & Oht, 2011). Studies have Copyright © 2013 SciRes. 616
B. JOHANSSON, L.-E. UNESTÅHL shown that stress and serious disease are associated with a shift from secretion of androgens towards glucocorticoids (Cook- Greuter, 2000). This can mainly be seen as increased plasma cortisol and lower DHEA-S (Corrigan, 2002). Additionally, a decrease in the DHEA/cortisol ratio and low DHEA-S has been correlated with the suppression of cellular immunity and the severity of disease (Parker & Odell, 1980). The average age-dependent decline in plasma DHEA-S con- centrations differed significantly by a few % per year by sex and age group (Baulieu, 1996; Wisniewski, Hilton, Morse, & Svec, 1993; Nafziger, Bowlin, Jenkins, & Pearson, 1998). The falling concentration in DHEA-S related to level of mental and physiological stress and physical illness (Boudarene, Legros, & Timsit-Berthier, 2002) support the hypothesis that those sub- jects with lower DHEA-S has a shorter life-span (Baulieu, 1996). A common belief with so far limited support by research, is that elite athletes especially elite players in team sports, have a shorter life span than other human beings (Ruiz, Moran, Arenas, & Lucia, 2010). The thrifty of longevity research show con- flicting results, where long-distance runners and cross-country skiers (Kujala, Tikkanen, Sarna, Pukkala, Kaprio, & Kosken- vou, 2001; Kujala, 2005) and Tour de France cyclists (Sanchis- Gomar, Olaso-Gonzales, Corella, Gomez-Cabrera, & Vina, 2011) had increased longevity, while individuals with weekly energy expenditure in the range of 3500 kcal show a mortality rate higher than the sedentary population (Paffenbarger, Hyde, Wing, & Hsieh, 1986). A less effective energy expenditure gains a stress induced anabolic hormonal response with in- creased leptin values in over-strain athletes (Bobbert, Mai, Brechtel, Schult, Weger, Pfeiffer, Spranger, & Diederich, 2012r), a plausible longevity risk factor. 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