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eCAM Advance Access published online on October 29, 2009
eCAM, doi:10.1093/ecam/nep169
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© The Author(s) 2009. Published by Oxford University Press.
This is an Open Access article distributed under the terms of the Creative Commons Attribution Non-Commercial License (http://creativecommons.org/licenses/by-nc/2.5/uk/) which permits unrestricted non-commercial use, distribution, and reproduction in any medium, provided the original work is properly cited.

Diaphragmatic Breathing Reduces Exercise-induced Oxidative Stress

Daniele Martarelli, Mario Cocchioni, Stefania Scuri and Pierluigi Pompei

Department of Experimental Medicine and Public Health, University of Camerino, 62032 Camerino, Macerata, Italy


   Abstract
Top
 Abstract
Introduction
 Methods
 Results
 Discussion
 Funding
 References
 
Diaphragmatic breathing is relaxing and therapeutic, reduces stress, and is a fundamental procedure of Pranayama Yoga, Zen, transcendental meditation and other meditation practices. Analysis of oxidative stress levels in people who meditate indicated that meditation correlates with lower oxidative stress levels, lower cortisol levels and higher melatonin levels. It is known that cortisol inhibits enzymes responsible for the antioxidant activity of cells and that melatonin is a strong antioxidant; therefore, in this study, we investigated the effects of diaphragmatic breathing on exercise-induced oxidative stress and the putative role of cortisol and melatonin hormones in this stress pathway. We monitored 16 athletes during an exhaustive training session. After the exercise, athletes were divided in two equivalent groups of eight subjects. Subjects of the studied group spent 1 h relaxing performing diaphragmatic breathing and concentrating on their breath in a quiet place. The other eight subjects, representing the control group, spent the same time sitting in an equivalent quite place. Results demonstrate that relaxation induced by diaphragmatic breathing increases the antioxidant defense status in athletes after exhaustive exercise. These effects correlate with the concomitant decrease in cortisol and the increase in melatonin. The consequence is a lower level of oxidative stress, which suggests that an appropriate diaphragmatic breathing could protect athletes from long-term adverse effects of free radicals.

Keywords: antioxidants – cortisol – free radicals – meditation – melatonin – physical activity


   Introduction
Top
 Abstract
 Introduction
Methods
 Results
 Discussion
 Funding
 References
 
Stress is defined as a physiological reaction to undesired emotional or physical situations. Initially, stress induces an acute response (fight or flight) that is mediated by catecholamines. When stress becomes chronic and lasts for a long time, the stressed organism reacts with physiological alterations to adapt to the unfavorable conditions. This ACTH-mediated reaction affects the immune and neuroendocrine systems, and it is responsible for several diseases (1). Numerous data support the hypothesis that the pathophysiology of chronic stress can be due, at least partially, to an increase in oxidative stress (2–4), which may also contributes to heart disease (5,6), rheumatoid arthritis (7,8), hypertension (9,10), Alzheimer's disease (11,12), Parkinson's disease (13), atherosclerosis (14) and, finally, aging (15).

Some authors have attributed stress-induced oxidative stress to an increase in glucocorticoids. In fact, there is evidence to suggest that glucocorticoids induce oxidative stress mainly by altering the expression and activity of antioxidant enzymes, thus impairing the antioxidant defense of the body (16–19). High levels of glucocorticoids are known to decrease blood reduced glutathione (GSH) and erythrocyte superoxide dismutase (SOD) activity in rats (20). Other enzymes are also involved, and NADPH oxidase, xanthine oxidase and uncoupled endothelial nitric oxide synthase are important sources of reactive oxygen species (ROS) in glucocorticoid-induced oxidative stress [see ref. (9) for a review on this argument].

A number of studies support the fact that meditation, through the modulation of the neuroendocrine response, combats stress and its related diseases. In fact, beyond its psychological and social effects, clinical studies have documented that meditation improves the immune system (21) and decreases cardiovascular risk factors such as hyperlipidemia, hypertension and atherosclerosis (22–30). A reduction in both glucocorticoids and oxidative stress has been documented in people who practice meditation regularly. Hormonal reactions to stressors, in particular plasma cortisol levels, are lower in people who meditate than in people who do not (31–36), suggesting that it is possible to modulate the neuroendocrine system through neurological pathways. Analysis of oxidative stress levels in people who meditate indicated that transcendental meditation, Zen meditation and Yoga correlate with lower oxidative stress levels (37–43).

Melatonin could also be involved in the reduction of oxidative stress because increased levels of this hormone have been reported after meditation (44–46). This neurohormone is considered a strong antioxidant and is used as a treatment for aging. Melatonin in fact, increases several intracellular enzymatic antioxidant enzymes, such as SOD and glutathione peroxidase (GSH-Px) (47,48), and induces the activity of {gamma}-glutamylcysteine synthetase, thereby stimulating the production of the intracellular antioxidant GSH (49). A number of studies have shown that melatonin is significantly better than the classic antioxidants in resisting free-radical-based molecular destruction. In these in vivo studies, melatonin was more effective than vitamin E, β-carotene (50–52) and vitamin C (53–55). In addition to mental stress, physical stress also increases the production of ROS. In exhaustive and prolonged exercise, ROS production is elevated, and changes in exercise intensity (aerobic–anaerobic) have been associated with a higher degree of oxidative stress (56–59). Although it has been established that a continuous and moderate physical activity reduces stress, intense and prolonged exercise is deleterious and needs a proper recovery procedure. The link between physical and psychological stress is apparent because they have equivalent hormonal responses. Actually, both types of stress are characterized by activation of the neuroendocrine axis, which leads to the production of ACTH and cortisol. The beneficial or detrimental role of cortisol in athletes has been debated, as some believe that its catabolic actions are detrimental to muscle recovery, whereas others believe that its anti-inflammatory actions are beneficial to muscle recovery. Plasma cortisol levels increase in response to intense and prolonged exercise (60,61). Ponjee et al. (62) demonstrated that cortisol increased significantly in male athletes after they ran a marathon. In another study, plasma ACTH and cortisol were found elevated in highly trained runners and in sedentary subjects after intense treadmill exercise (63).

Additionally, melatonin levels are affected by physical activity. There are some conflicting reports regarding the effects of exercise on melatonin levels, with some studies reporting an increase, some a decrease and some reporting no change in melatonin concentrations after exercise (64–70). However, these contradictory results could be due to light conditions and the timing or intensity of exercise. Moreover, sex, age and training of the monitored athletes may contribute to the different results reported in these studies. It has been speculated that intense sport increases melatonin secretion due to the necessity of combating the free radical production that occurs during exercise, and melatonin could be responsible for amenorrhea in female athletes as an effect of overtraining (71).

Most, if not all, meditation procedures involve diaphragmatic breathing (DB), which is the act of breathing deeply into the lungs by flexing the diaphragm rather than the rib cage. DB is relaxing and therapeutic, reduces stress and is a fundamental procedure of Pranayama Yoga, Zen, transcendental meditation and other meditation practices.

Although exercise-induced ROS production can be produced via different pathways (56), we speculated that by combating the exercise-induced increase in cortisol levels and by stimulating melatonin levels, DB could improve antioxidant defenses and, therefore, decrease oxidative stress. We have recently demonstrated that in master athletes, oxidative stress induced by intense exercise reaches dangerous levels (72). Therefore, in this study, we investigated the effects of DB on exercise-induced oxidative stress and the putative role of cortisol and melatonin hormones in this stress pathway.


   Methods
Top
 Abstract
 Introduction
 Methods
Results
 Discussion
 Funding
 References
 
Subjects and Exercise

Athletes were monitored during a training session for a 24-h long contest. This type of race lasts for 24 h, generally starting at 10:00 am and ending at 10:00 am the following day. Bikers ride as many kilometers as possible on a specific circuit trail in the 24-h period. Athletes are allowed to stop, to sleep, to rest and to eat as much food as they want to eat.

The session analyzed in this study was a reproduction of the first 8 h of the race, which is generally the most intense. Athletes started to ride at 10:00 am and stopped at 6:00 pm. They consumed the same food and rested the same time.

Since the parameters measured can differ for each individual, we performed preliminary analyses to select subjects with comparable cortisol, melatonin, antioxidant and oxidative stress values.

We selected 16 amateur male cyclists, aged 44.4 ± 2 years (±SD). Their mean height and weight were 175.4 ± 7.5 cm and 68.8 ± 5.7 kg, respectively (Table 1). Subjects were informed of the purpose of the study, and all of them gave their informed consent prior to their inclusion. This study has been performed in accordance with the ethical standards laid down in the 1964 declaration of Helsinki.


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  		Table 1. Characteristics of the sample studied

 
None of the subjects had taken medication or supplements within the past 30 days that might alter the study outcome, and none of them had a history of medical or surgical events that could affect the study outcome, including cardiovascular disease or metabolic, renal, hepatic or musculoskeletal disorders.

Experimental Procedure

After exercising, athletes took a shower and drank water to rehydrate. They were then divided in two equivalent groups of eight subjects (Table 1). Subjects of the studied group were previously trained to relax by performing DB and concentrating on their breath. These athletes spent 1 h (6:30–7:30 pm) relaxing performing DB in a quiet place. The other eight subjects, representing the control group, spent the same time sitting in an equivalent quite place. The only activity allowed was reading magazines. Lighting levels were monitored throughout the experiment and did not exceed 15 lux, a level well below that known to influence melatonin secretion (73,74).

After the resting and DB periods, athletes consumed the same food and retired for sleeping at 10:00 pm. At 11:00 pm, all of them were sleeping.

We referred to the DB applied here as a relaxation technique. Instead of training the athletes with some form of meditation, we preferred DB because it is easy to learn and to perform and because it does not require any moral conviction that could generate psychologically adverse reactions. However, DB associated with a focused mind (in this case, awareness on the breath as specified in the methods section) can be considered a form of meditation such as focused meditation or others (75).

Oxidative Stress Determination

Oxidative stress was measured by performing the d reactive oxygen metabolites (d-ROMs) test (76,77), which determines the plasma ROMs produced by ROS. The d-ROMs test is based on the concept that plasmahydroperoxides react with the transition metal ions liberated from the proteins in the acidic medium and are converted to alkoxy and peroxy radicals. These newly formed radicals are able to oxidize N,N-diethyl-para-phenylendiamine to the corresponding radical cation, and its concentration can be determined through spectrophotometric procedures (absorption at 505 nm). The d-ROMs test is expressed in U CARR (Carratelli units), where 1 U CARR = 0.08 mg H2O2 dl–1. Values higher than 300 U CARR indicate oxidative stress. ROMs were determined before starting the exercise (9:30 am), at the end of the exercise (6:00 pm), immediately after the DB periods (7:30 pm), at 2:00 am, and 24 h after the exercise (10:00 am of the following day).

Biological Antioxidant Potential Determination

The antioxidant defense status was assessed by determining the biological antioxidant potential (BAP test), which depends on the plasma levels of antioxidants. The BAP test is based on the ability of a coloured solution, containing a source of ferric (Fe3+) ions adequately bound to a special chromogenic substrate, to lose colour when Fe3+ ions are reduced to ferrous ions (Fe2+), which occurs when a reducing/antioxidant system is added. The ferric chloride reagent (50 µl) is transferred into a cuvette containing the thiocyanate derivative reagent. The resulting colored solution is gently mixed by inversion and its absorbance is measured at 550 nm. Then, 10 µl of plasma is added to the same cuvette, the solution is gently mixed, incubated in a thermostatic block for 5 min at 37°C, and its absorbance at 550 nm is remeasured (78,79). The BAP test results are expressed in µmol Fe2+/liter of sample. Values higher than 2200 µmol Fe2+/liter are considered a normal BAP. d-ROMs and BAP tests were performed using apposite kits and dedicated instrumentation Free Radical Analytical System 4 (FRAS4, Health & Diagnostics Limited Co., Parma, Italy). Since the BAP test must be performed at least 3 h after food was last consumed, the BAP was determined before breakfast at 8:00 am, during the night at 2:00 am, and 24 h post-exercise (8:00 am).

Saliva Collection

The subjects abstained from alcoholic and caffeinated beverages from the beginning of the training session and were only allowed to drink water. Subjects washed their mouths with distilled water before salivary samples were obtained using the Bühlmann saliva collection device (Bühlmann Laboratories AG, Switzerland). Immediately after collection, the saliva samples were frozen and stored at –80°C until they were assayed for cortisol and melatonin concentrations.

Cortisol Assay

Salivary cortisol was determined before the exercise began (10:00 am), at the end of the exercise (6:00 pm), immediately after the DB period (7:30 pm), at 2:00 am, and 24 h after the exercise (10:00 am of the next day) using a commercially available EIA kit (Cortisol Express, Cayman Chemical Ann Arbor, MI, USA). Absorbance values were determined at 415 nm using a plate reader. Samples were assayed in triplicate.

Melatonin Assay

Salivary nocturnal melatonin was determined at 2:00 am using the Bühlmann Direct Saliva Melatonin Elisa (Bühlmann Laboratories AG, Switzerland). This assay is based on a melatonin biotin conjugate antibody, streptavidin conjugated to horseradish peroxidase and a tetramethyl benzidine (TMB) substrate. The product of the substrate was measured spectrophotometrically at 450 nm. The assay sensitivity range was 1–60.6 pg ml–1.

Statistical Analysis

The characteristics of the studied sample and the effects of DB were analyzed by two-way ANOVA with repeated measurements. A two-sided t-test (post-hoc comparisons) and the non parametric Wilcoxon–Mann–Whitney test were used for the comparison of numerical data across groups for each time point. A P-value <0.05 was considered statistically significant. Statistics were compiled using Microsoft Excel and Winstat software. Changes in melatonin levels were analyzed by the two-sided t-test and the non-parametric Wilcoxon–Mann–Whitney test.


   Results
Top
 Abstract
 Introduction
 Methods
 Results
Discussion
 Funding
 References
 
Characteristics of the Studied Sample

Subjects were divided into two similar groups, as shown in Table 1. There were no statistical differences for age, height, weight, or km covered between the groups [F(1,62) = 0.023; P > 0.5].

Oxidative Stress Changes

As expected, the exercise induced a strong oxidative stress in athletes (Fig. 1).


Figure 1
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  		Figure 1 ROMs levels were determined at different times, before and after exercise. Athletes were divided in two equivalent groups of eight subjects. Subjects of the studied group spent 1 h (6:30–7:30 pm) relaxing performing DB and concentrating on their breath in a quiet place. The other eight subjects, representing the control group, spent the same time sitting in an equivalent quite place. Values shown are mean ± SD. **P < 0.01 DB versus control group.

 
The ROMs levels were significantly increased after exercise compared to pre-exercise levels. All athletes had an elevation in ROMs in response to the training exercise, reaching particularly high levels of oxidative stress. The overall ANOVA revealed a significant DB effect [F(1,78) = 11.184; P < 0.01] and time effect [F(4,75) = 130.481; P < 0.01]. After completing the training exercise, there was a significant amount of variability between the ROMs levels of individual athletes, suggesting that each athlete has an individual response to oxidative stress. However, post-hoc comparisons confirmed that the mean level of ROMs in athletes of the DB group was significantly lower than the control-group athletes both at 2:00 am (P < 0.01 DB versus control group) and 24 h post-exercise (P < 0.01 DB versus control group). For the DB group, the increase in ROMs levels post-exercise compared to pre-exercise levels was 161.7% at 6:00 pm, 150.9% at 7:30 pm, 141.6% at 2:00 am and 126.8% 24 h post-exercise. For the control group, the increase in ROMs levels post-exercise compared to pre-exercise levels was 160.9% at 6:00 pm, 157.1% at 7:30 pm, 159.9% at 2:00 am and 154% 24 h post-exercise.

Biological Antioxidant Potential Changes

Figure 2 shows the BAP which significantly increased in both groups.


Figure 2
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  		Figure 2 BAP levels were determined at different times, before and after exercise. Athletes were divided in two equivalent groups of eight subjects. Subjects of the studied group spent 1 h relaxing performing DB and concentrating on their breath in a quiet place. The other eight subjects, representing the control group, spent the same time sitting in an equivalent quite place. Since this test must be performed several hours after food ingestion, BAP levels were determined pre-exercise at 8:00 am before breakfast, at 2:00 am, and at 8:00 am 24 h post-exercise. Values shown are mean ± SD. *P < 0.05 DB versus control group. **P < 0.01 DB versus control group.

 
Again, a significant variation among the subjects was observed, but athletes of the DB group presented BAP levels significantly higher than the control group [F(1,46) = 21.001; P < 0.01]. This difference was more evident at 2:00 am (P < 0.01 DB versus control group, post-hoc comparisons) than 24 h post-exercise (P < 0.05 DB versus control group, post-hoc comparisons), where BAP began to return to basal levels. With respect to the pre-exercise values, for the DB group, the increase in BAP levels was 129.1% at 2:00 am and 111.1% at 24 h post-exercise.

For the control group, the increase was 114.2% at 2:00 am and 106.2% at 24 h post-exercise with respect to the pre-exercise values. ANOVA also revealed a significant time effect [F(2,45) = 91.587; P < 0.01].

Changes in Cortisol Levels

ANOVA revealed a significant DB effect [F (1,78) = 4.028; P < 0.05]. As shown in Fig. 3, significant differences between the groups were observed only at 7:30 pm, after the DB (P < 0.05 DB versus control group, post-hoc comparisons). At 2:00 am and 24 h post-exercise, cortisol levels were lower in athletes of the DB group, but differences were not statistically significant. In athletes of the DB group, the decrease in cortisol levels (07:30 p.m.) temporarily precedes the decrease in ROMs levels (2:00 am). It was not possible to determine the effects of exercise on cortisol levels, as hormone concentrations were determined at different times during its circadian rhythm. With respect to the pre-exercise values, for the DB group, cortisol values were 82.2% by 06:00 pm, 61.1% by 7:30 pm, 47.7% by 02:00 am and 74.7% 24 h post-exercise. For the control group, with respect to the pre-exercise values, values were 83.4% by 06:00 pm, 79.1% by 7:30 pm, 54.6% by 02:00 am and 86.9% 24 h post-exercise respect to the pre-exercise values. ANOVA also revealed a significant time effect [F(4,75) = 17.459; P < 0.01].


Figure 3
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  		Figure 3 Salivary cortisol levels were determined at different times, before and after exercise. Athletes were divided in two equivalent groups of eight subjects. Subjects of the studied group spent 1 h (6:30–7:30 pm) relaxing performing DB and concentrating on their breath in a quiet place. The other eight subjects, representing the control group, spent the same time sitting in an equivalent quite place. Values shown are mean ± SD. *P < 0.05 DB versus control group.

 
Changes in Melatonin Levels

Figure 4 shows the differences in nocturnal melatonin levels between the two groups of athletes. Melatonin levels were significantly higher in athletes of the DB group (P < 0.05 DB versus control group). These data are congruent with the lower ROMs levels, with the higher BAP levels and with the lower cortisol levels at 7:30 pm.


Figure 4
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  		Figure 4 Salivary nocturnal melatonin levels variation after exercise. Values shown are mean ± SD. *P < 0.05 DB versus control group.

 

   Discussion
Top
 Abstract
 Introduction
 Methods
 Results
 Discussion
Funding
 References
 
This study demonstrates that DB reduces the oxidative stress induced by exhaustive exercise. To our knowledge, this is the first study which explores the effect of DB on the stress caused by exhaustive physical activity.

It is known that cortisol inhibits enzymes responsible for the antioxidant activity of cells and that melatonin is a strong antioxidant. After the training exercise, athletes who underwent DB presented higher levels of BAP, which are congruous with the reduced levels of cortisol and ROMs and with the increased levels of nocturnal melatonin. As in our previous study (72), after exercise, we found an increase in BAP levels in both of the groups analyzed. However, the elevated levels of plasma antioxidant markers after exercise can be explained considering three processes: (i) the suspension of exercise decreases oxidant production, so antioxidant defense can return to normal levels; (ii) up-regulation of antioxidants and (iii) the mobilization of antioxidants from tissues to blood (80). Beyond these mechanisms, these results also suggest that cortisol and melatonin levels could affect the modulation of antioxidant defenses and are relevant in determining the final level of oxidative stress. The decrease of ROS concentrations in subjects performing DB could be attributed to the reduced neuroendocrine response induced by relaxation.

The rationale is as follows (Fig. 5):

  1. intense exercise increases cortisol production;
  2. a high plasmatic level of cortisol decreases body antioxidant defenses;
  3. a high plasmatic level of cortisol correlates with a high level of oxidative stress;
  4. DB reduces the production of cortisol;
  5. DB increases melatonin levels;
  6. melatonin is a strong antioxidant;
  7. DB increases the BAP and
  8. DB reduces oxidative stress.


Figure 5
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  		Figure 5 Modulation of oxidative stress by exercise and DB.

 
If these results are confirmed in other intense physical activity programs, relaxation could be considered an effective practice to significantly contrast the free radical-mediated oxidative damage induced by intense exercise. Therefore, similar to the way that antioxidant supplementation has been integrated into athletic training programs, DB or other meditation techniques should be integrated into many sports as a method to improve performance and to accelerate recovery. However, wider health implications can be accounted for the use of DB, as it can find applications in several pathologies. For example, the oxidative stress that occurs in the hyperventilation syndrome can be cured by learning DB. Hyperventilation, in fact, induces hyperoxia which is known to be related with oxidative stress (81,82). The hyperventilation syndrome affects 15% of the population and occurs when breathing rates elevate to 21–23 bpm as a result of constricted non-DB. DB can treat hyperoxia and its consequences acting by two synergic ways: restoring the normal breath rhythm and reducing oxidative stress mainly through the increase in melatonin production which is known for its ability to reduce oxidative stress induced by exposure to hyperbaric hyperoxia (83). Moreover, Orme-Johnson observed greatly reduced pathology levels in regular meditation practitioners (84,85). A 5 years statistic of approximately 2000 regular participants demonstrated that Transcendental Meditation reduced benign and malignant tumors, heart disease, infectious diseases, mental disorders and diseases of the nervous system. Mourya et al. evidenced that slow-breathing exercises may influence autonomic functions reducing blood pressure in patients with essential hypertension (86). Finally, there are also evidences that procedures which involve the control of the breathing can positively affect type 2 Diabetes (87), depression, pain (88), high glucose level and high cholesterol (89).

Our results contribute to explain these effects as oxidative stress may also play a role in the development of these pathologies (2–15). The role of melatonin must also be emphasized. Beyond its antioxidant properties, melatonin is involved in the regulation of the circadian sleep–wake rhythm and in the modulation of hormones and the immune system. Due to its wide medical implications, the increase in melatonin levels induced by DB suggests that this breath procedure deserves to be included in public health improvement programs.

In this work, we explored the acute effects of DB, but these outcomes should also be investigated for longer periods, for which we would expect a more intense and beneficial response. For example, it is likely that expert practitioners who frequently utilize of DB could obtain a more significant reduction in oxidative stress and, perhaps, an improvement in exercise performance. Moreover, relaxation could also be improved by adding another relaxation method to the formula, for example music. In fact, Khalfa et al. (90) demonstrated that relaxing music facilitates recovery from a psychologically stressful task, decreasing the salivary cortisol.

Our results must also be discussed in light of the fact that cortisol has an ACTH-dependent circadian rhythm with peak levels in the early morning and a nadir at night. Athletes start to ride at 10:00 am and stop at 6:00 pm. The DB session started at 6:30 pm and stopped at 7:30 pm. It is probable that these results would be different if the time of physical activity and the DB session were changed. The same is true for melatonin. In fact, significant differences have been reported in melatonin secretion when exercises were performed at different times and under different light conditions (64–70). We collected the saliva at 2:00 am, when a peak in melatonin must be expected. DB increased the levels of melatonin in athletes, and this correlates with lower oxidative stress (ROMs), with lower cortisol levels and with the higher antioxidant status (BAP) in these athletes.

The mechanism by which relaxation might induce an increase in melatonin levels is uncertain, and whether the melatonin increase is simply due to the cortisol decrease remains to be elucidated. Different mechanisms could be involved. Tooley et al. (46) speculated that meditation-reduced hepatic blood flow (91) could raise the plasma levels of melatonin. Alternatively, since meditation increases plasma levels of noradrenaline (92) and urine levels of the metabolite 5HIAA (93), a possible direct action on the pineal gland could be hypothesized, as melatonin is synthesized in the pineal by serotonin under a noradrenaline stimulus (94). More likely, we suspect that the increase in melatonin levels determined in our experiment can be mainly attributed to the reduced cortisol levels. Actually, a relationship between cortisol and melatonin rhythms has been observed (95), indicating that melatonin onset typically occurs during low cortisol secretion. In addition, Monteleone et al. (96) found that exercise-induced increases in plasma cortisol preceded the lower night-time melatonin secretion, thus suggesting a connection between the metabolisms of these two hormones.

More studies are needed to clarify the link between cortisol and melatonin; however, due to the complexity of the pathways involved in maintaining homeostasis and in initiating the stress response, it is plausible that the relationship between the two hormones could be mediated by several mechanisms.

Overall, these data demonstrate that relaxation induced by DB increases the antioxidant defense status in athletes after exhaustive exercise. These effects correlate with the concomitant decrease in cortisol, which is known to negatively affect antioxidant defenses, and the increase in melatonin, a strong antioxidant. The consequence is a lower level of oxidative stress, which suggests that an appropriate recovery could protect athletes from long-term adverse effects of free radicals.


   Funding
Top
 Abstract
 Introduction
 Methods
 Results
 Discussion
 Funding
References
 
Department of Experimental Medicine and Public Health, University of Camerino, Macerata, Italy.


  Footnotes
 
For reprints and all correspondence: Dr Daniele Martarelli, Department of Experimental Medicine and Public Health, University of Camerino, Via Madonna delle carceri, 62032 Camerino, Macerata, Italy. Tel: +39-737-403314; Fax: +39-737-403325; E-mail: daniele.martarelli{at}unicam.it


   References
Top
 Abstract
 Introduction
 Methods
 Results
 Discussion
 Funding
 References
 

  1. Cohen S, Janicki-Deverts D, Miller GE. Psychological stress and disease. JAMA ( 2007;) 298:: 1685–87.[Free Full Text]
  2. Itoh T, Saito T, Fujimura M, Watanabe S, Saito K. Restraint stress induced changes in endogenous zinc release from the rat hippocampus. Brain Res ( 1993;) 618:: 318–22.[CrossRef][Web of Science][Medline]
  3. Scarpellini F, Sbracia M, Scarpellini L. Psychological stress and lipoperoxidation in miscarriage. Ann NY Acad Sci ( 1994;) 709:: 210–13.[Web of Science][Medline]
  4. Adachi S, Kawamura K, Takemoto K. Oxidative damage of nuclear DNA in liver of rats exposed to psychological stress. Cancer Res ( 1993;) 53:: 4153–55.[Abstract/Free Full Text]
  5. Molavi B, Mehta JL. Oxidative stress in cardiovascular disease: molecular basis of its deleterious effects, its detection, and therapeutic considerations. Curr Opin Cardiol ( 2004;) 19:: 488–93.[CrossRef][Web of Science][Medline]
  6. Dhalla NS, Temsah RM, Netticadan T. Role of oxidative stress in cardiovascular diseases. J Hypertens ( 2000;) 18:: 655–73.[CrossRef][Web of Science][Medline]
  7. Hitchon CA, El-Gabalawy HS. Oxidation in rheumatoid arthritis. Arthritis Res Ther ( 2004;) 6:: 265–78.[CrossRef][Web of Science][Medline]
  8. Filippin LI, Vercelino R, Marroni NP, Xavier RM. Redox signalling and the inflammatory response in rheumatoid arthritis. Clin Exp Immunol ( 2008;) 152:: 415–22.[Web of Science][Medline]
  9. Ong Sl, Zhang Y, Whitworth JA. Reactive oxygen species and glucocorticoid-induced hypertension. Clinical and Experimental Pharmacology and Physiology ( 2008;) 35:: 477–82.[CrossRef][Web of Science][Medline]
  10. Kumar KV, Das UN. Are free radicals involved in the pathobiology of human essential hypertension? Free Radic. Res. Commun ( 1993;) 19:: 59–66.[Web of Science][Medline]
  11. Yves Christen. Oxidative stress and Alzheimer disease. American Journal of Clinical Nutrition ( 2000;) 71:: 621S–29S.[Web of Science][Medline]
  12. Markesbery WR. Oxidative stress hypothesis in Alzheimer's disease. Free Radic Biol Med ( 1997;) 23:: 134–47.[CrossRef][Web of Science][Medline]
  13. Jenner P, Olanow CW. Oxidative stress and the pathogenesis of Parkinson's disease. Neurology ( 1996;) 47:: S161–170.[Web of Science][Medline]
  14. Bonomini F, Tengattini S, Fabiano A, Bianchi R, Rezzani R. Atherosclerosis and oxidative stress. Histol Histopathol ( 2008;) 23:: 381–90.[Web of Science][Medline]
  15. Kregel KC, Zhang HJ. An integrated view of oxidative stress in aging: basic mechanisms, functional effects, and pathological considerations. Am J Physiol Regul Integr Comp Physiol ( 2007;) 292:: R18–36.[Abstract/Free Full Text]
  16. McIntosh LJ, Sapolsky RM. Glucocorticoids increase the accumulation of reactive oxygen species and enhance adriamycin induced toxicity in neuronal culture. Exp Neurol ( 1996;) 141:: 201–6.[CrossRef][Web of Science][Medline]
  17. Eid YZ, Ohtsuka A, Hayashi K. Tea polyphenols reduce glucocorticoidinduced growth inhibition and oxidative stress in broiler chickens. Br Poult Sci ( 2003;) 44:: 127–32.[CrossRef][Web of Science][Medline]
  18. Ohtsuka A, Kojima H, Ohtani T, Hayashi K. Vitamin E reduces glucocorticoid-induced oxidative stress in rat skeletal muscle. J Nutr Sci Vitaminol (Tokyo) ( 1998;) 44:: 779–86.[Medline]
  19. Epel ES, Blackburn EH, Lin J, Dhabhar FS, Adler NE, Morrow JD, et al. Accelerated telomere shortening in response to life stress. Proc Natl Acad Sci USA ( 2004;) 101:: 17312–15.[Abstract/Free Full Text]
  20. Orzechowski A, Ostaszewski P, Brodnicka A, Wilczak J, Jank M, Balasinska B, et al. Excess of glucocorticoids impairs whole-body antioxidant status in young rats. relation to the effect of dexamethasone in soleus muscle and spleen. Horm Metab Res ( 2000;) 32:: 174–80.[Web of Science][Medline]
  21. Davidson RJ, Kabat-Zinn J, Schumacher J, Rosenkranz M, Muller D, Santorelli SF, et al. Alterations in brain and immune function produced by mindfulness meditation. Psychosom. Med ( 2003;) 65:: 564–70.[Abstract/Free Full Text]
  22. Barnes VA, Treiber FA, Turner JR, Davis H, Strong WB. Acute effects of transcendental meditation on hemodynamic functioning in middle-aged adults. Psychosom. Med ( 1999;) 61:: 525–31.[Abstract/Free Full Text]
  23. Barnes VA, Treiber FA, Davis H. Impact of Transcendental Meditation on cardiovascular function at rest and during acute stress in adolescents with high normal blood pressure. J Psychosom Res ( 2001;) 51:: 597–605.[CrossRef][Web of Science][Medline]
  24. Wenneberg SR, Schneider RH, Walton KG, Maclean CR, Levitsky DK, Salerno JW, et al. A controlled study of the effects of the Transcendental Meditation program on cardiovascular reactivity and ambulatory blood pressure. Int J Neurosci ( 1997;) 89:: 15–28.[Web of Science][Medline]
  25. Calderon R, Schneider RH, Alexander CN, Myers HF, Nidich SI, Haney C. Stress, stress reduction and hypercholesterolemia in African Americans: a review. Ethn. Dis ( 1999;) 9:: 451–62.[Medline]
  26. Cooper MJ, Aygen MM. A relaxation technique in the management of hypercholesterolemia. J Hum Stress ( 1979;) 5:: 24–7.
  27. Castillo-Richmond A, Schneider RH, Alexander CN, Cook R, Myers H, Nidich S, et al. Effects of stress reduction on carotid atherosclerosis in hypertensive African Americans. Stroke ( 2000;) 31:: 568–73.[Abstract/Free Full Text]
  28. King MS, Carr T, D’Cruz C. Transcendental meditation, hypertension and heart disease. Aust Fam Physician ( 2002;) 31:: 164–8.[Medline]
  29. Lehrer P, Sasaki Y, Saito Y. Zazen and cardiac variability. Psychosom Med ( 1999;) 61:: 812–21.[Abstract/Free Full Text]
  30. Takeo K, Minamisawa H, Kanda K, Hasegawa S. Heart rates during the daily activity of bZenQ priests. J Hum Ergol (Tokyo) ( 1984;) 13:: 83–7.[Medline]
  31. Alexander CN, Robinson P, Orme-Johnson DW, Schneider RH, Walton KG. Effects of Transcendental Meditation compared to other methods of relaxation and meditation in reducing risk factors, morbidity and mortality. Homeostasis ( 1994;) 35:: 243–64.
  32. Sudsuang R, Chentanez V, Veluvan K. Effect of Buddhist meditation on serum cortisol and total protein levels, blood pressure, pulse rate, lung volume and reaction time. Physiol Behav ( 1991;) 50:: 543–8.[CrossRef][Medline]
  33. Jevning R, Wilson AF, Smith WR. The transcendental meditation technique, adrenocortical activity, and implications for stress. Experientia ( 1978;) 34:: 618–19.[CrossRef][Web of Science][Medline]
  34. Jevning R, Wilson AF, Davidson JM. Adrenocortical activity during meditation. Horm Behav ( 1978;) 10:: 54–60.[CrossRef][Medline]
  35. MacLean CR, Walton KG, Wenneberg SR, Levitsky DK, Mandarino JP, Waziri R, et al. Effects of the Transcendental Meditation program on adaptive mechanisms: changes in hormone levels and responses to stress after 4 months of practice. Psychoneuroendocrinology ( 1997;) 22:: 277–95.[CrossRef][Web of Science][Medline]
  36. Michaels RR, Parra J, McCann DS, Vander AJ. Renin, cortisol, and aldosterone during transcendental meditation. Psychosom Med ( 1979;) 41:: 50–4.[Abstract/Free Full Text]
  37. Kim DH, Moon YS, Kim HS, Jung JS, Park HM, Suh HW, et al. Effect of Zen Meditation on serum nitric oxide activity and lipid peroxidation. Prog Neuropsychopharmacol Biol Psychiatry ( 2005;) 29:: 327–31.[CrossRef][Medline]
  38. Schneider RH, Nidich SI, Salerno JW, Sharma HM, Robinson CE, Nidich RJ, et al. Lower lipid peroxide levels in practitioners of the Transcendental Meditation program. Psychosom Med ( 1998;) 60:: 38–41.[Abstract/Free Full Text]
  39. Sinha S, Singh SN, Monga YP, Ray US. Improvement of glutathione and total antioxidant status with yoga. J Altern Complement Med ( 2007;) 13:: 1085–90.[CrossRef][Web of Science][Medline]
  40. Yadav RK, Ray RB, Vempati R, Bijlani RL. Effect of a comprehensive yoga-based lifestyle modification program on lipid peroxidation. Indian J Physiol Pharmacol ( 2005;) 49:: 358–62.[Medline]
  41. Van Wijk EP, Koch H, Bosman S, Van Wijk R. Anatomical characterization of human ultraweak photon emission in practitioners of transcendental meditation and control subjects. J Altern Complement Med ( 1998;) 12:: 31–8.[CrossRef]
  42. Van Wijk EP, Lüdtke R, Van Wijk R. Differential effects of relaxation techniques on ultraweak photon emission. J Altern Complement Med ( 2008;) 14:: 241–50.[CrossRef][Web of Science][Medline]
  43. Kita T, Yokode M, Kume N, Ishii K, Nagano Y, Mikami A, et al. The concentration of serum lipids in Zen monks and control males in Japan. Japan Jpn Circ J ( 1988;) 52:: 99–104.
  44. Harinath K, Malhotra AS, Pal K, Prasad R, Kumar R, Kain TC, et al. Effects of Hatha Yoga and Omkar Meditation on Cardiorespiratory Performance, Psychologic Profile, and Melatonin Secretion. The Journal of Alternative and Complementary Medicine ( 2004;) 10:: 261–68.[CrossRef]
  45. Solberg EE, Holen A, Ekeberg Ø, Østerud B, Halvorsen R, Sandvik L. The effects of long meditation on plasma melatonin and blood serotonin. Med Sci Monit ( 2004;) 10:: CR96–101.[Web of Science][Medline]
  46. Tooley GA, Armstrong SM, Norman TR, Sali A. Acute increases in night-time plasma melatonin levels following a period of meditation. Biol Psychol ( 2000;) 53:: 69–78.[CrossRef][Web of Science][Medline]
  47. Rodriguez C, Mayo JC, Sainz RM, Antolín I, Herrera F, Martín V, et al. Regulation of antioxidant enzymes: a significant role for melatonin. J Pineal Res ( 2004;) 36:: 1–9.[CrossRef][Web of Science][Medline]
  48. Reiter RJ, Tan DX, Maldonado MD. Melatonin as an antioxidant: physiology versus pharmacology. J Pineal Res ( 2005;) 39:: 215–6.[Web of Science][Medline]
  49. Winiarska K, Fraczyk T, Malinska D, Drozak J, Bryla J. Melatonin attenuates diabetes induced oxidative stress in rabbits. J Pineal Res ( 2006;) 40:: 168–76.[CrossRef][Web of Science][Medline]
  50. Baydas G, Canatan H, Turkoglu A. Comparative analysis of the protective effects of melatonin and vitamin E on streptozocin-induced diabetes mellitus. J Pineal Res ( 2002;) 32:: 225–30.[CrossRef][Web of Science][Medline]
  51. Wahab MH, Akoul ES, Abdel-Aziz AA. Modulatory effects of melatonin and vitamin E on doxorubicin-induced cardiotoxicity in Ehrlich ascites carcinoma-bearing mice. Tumori ( 2000;) 86:: 157–62.[Web of Science][Medline]
  52. Montilla P, Cruz A, Padillo FJ, Túnez I, Gascon F, Muñoz MC, et al. Melatonin versus vitamin E as protective treatment against oxidative stress after extra-hepatic bile duct ligation in rats. J Pineal Res ( 2001;) 31:: 138–44.[CrossRef][Web of Science][Medline]
  53. Hsu C, Han B, Liu M, Yeh C, Casida JE. Phosphine-induced oxidative damage in rats: attenuation by melatonin. Free Radic Biol Med ( 2000;) 28:: 636–42.[CrossRef][Web of Science][Medline]
  54. Gultekin F, Delibas N, Yasar S, Kilinc I. In vivo changes in antioxidant systems and protective role of melatonin and a combination of vitamin C and vitamin E on oxidative damage in erythrocytes induced by chlorpyrifos-ethyl in rats. Arch Toxicol ( 2001;) 75:: 88–96.[CrossRef][Web of Science][Medline]
  55. Rosales-Corral S, Tan DX, Reiter RJ, Valdivia-Velázquez M, Martínez-Barboza G, Acosta-Martínez JP, et al. Orally administered melatonin reduces oxidative stress and proinflammatory cytokines induced by amyloid-beta peptide in rat brain: a comparative, in vivo study versus vitamin C and E. J Pineal Res ( 2003;) 35:: 80–4.[CrossRef][Web of Science][Medline]
  56. Deaton CM, Marlin DJ. Exercise-associated oxidative stress. Clin Tech Equine Prac ( 2003;) 2:: 278–91.[CrossRef]
  57. Ilhan N, Kamanli A, Ozmerdivenli R, Ilhan N. Variable effects of exercise intensity on reduced glutathione, thiobarbituric acid reactive substance levels, and glucose concentration. Arch Med Res ( 2004;) 35:: 294–300.[CrossRef][Web of Science][Medline]
  58. Skenderi KP, Tsironi M, Lazaropoulou C, Anastasiou CA, Matalas AL, Kanavaki I, et al. Changes in free radical generation and antioxidant capacity during ultramarathon foot race. Eur J Clin Invest ( 2008;) 38:: 159–65.[CrossRef][Web of Science][Medline]
  59. Leeuwenburgh C, Heinecke JW. Oxidative stress and antioxidants in exercise. Curr Med Chem ( 2001;) 8:: 829–38.[Web of Science][Medline]
  60. Kraemer WJ, Loebel CC, Volek JS, Ratamess NA, Newton RU, Wickham RB, et al. The effect of heavy resistance exercise on the circadian rhythm of salivary testosterone in men. Eur J Appl Physiol ( 2001;) 84:: 13–8.[CrossRef][Web of Science][Medline]
  61. Bird SP, Tarpenning KM. Influence of circadian time structure on acute hormonal responses to a single bout of heavy-resistance exercise in weight-trained men. Chronobiol Int ( 2004;) 21:: 131–46.[CrossRef][Web of Science][Medline]
  62. Ponjee GA, De Rooy HA, Vader HL. Androgen turnover during marathon running. Med Sci Sports Exerc ( 1994;) 26:: 1274–77.[Web of Science][Medline]
  63. Luger A, Deuster PA, Kyle SB, Gallucci WT, Montgomery LC, Gold PW, et al. Acute hypothalamic-pituitary-adrenal responses to the stress of treadmill exercise. Physiologic adaptations to physical training. N Engl J Med ( 1987;) 316:: 1309–15.[Abstract]
  64. Carr DB, Reppert SM, Bullen B, Skrinar G, Beitins I, Arnold M, et al. Plasma melatonin increases during exercise in women. J Clin Endocrinol Metab ( 1981;) 53:: 224–5.[Web of Science][Medline]
  65. Theron JJ, Oosthuizen JM, Rautenbach MM. Effect of physical exercise on plasma melatonin levels in normal volunteers. S Afr Med J ( 1984;) 66:: 838–41.[Web of Science][Medline]
  66. Monteleone P, Maj M, Fusco M, Orazzo C, Kemali D. Physical exercise at night blunts the nocturnal increase of plasma melatonin levels in healthy humans. Life Sci ( 1990;) 47:: 1989–95.[CrossRef][Web of Science][Medline]
  67. Monteleone P, Maj M, Fuschino A, Kemali D. Physical stress in the middle of the dark phase does not affect light-depressed plasma melatonin levels in humans. Neuroendocrinology ( 1992;) 55:: 367–71.[Web of Science][Medline]
  68. Yaga K, Tan DX, Reiter RJ, Manchester LC, Hattori A. Unusual responses of nocturnal pineal melatonin synthesis and secretion to swimming: attempts to define mechanisms. J Pineal Res ( 1993;) 14:: 98–103.[CrossRef][Web of Science][Medline]
  69. Miyazaki T, Hashimoto S, Masubuchi S, Honma S, Honma KI. Phase-advance shifts of human circadian pacemaker are accelerated by daytime physical exercise. Am J Physiol Regul Integr Comp Physiol ( 2001;) 281:: R197–205.[Abstract/Free Full Text]
  70. Elias AN, Wilson AF, Pandian MR, Rojas FJ, Kayaleh R, Stone SC, et al. Melatonin and gonadotropin secretion after acute exercise in physically active males. Eur J Appl Physiol Occup Physiol ( 1993;) 66:: 357–361.[CrossRef][Web of Science][Medline]
  71. Laughlin GA, Loucks AB, Yen SS. Marked augmentation of nocturnal melatonin secretion in amenorrheic athletes, but not in cycling athletes: unaltered by opioidergic or dopaminergic blockade. J Clin Endocrinol Metab ( 1991;) 73:: 1321–26.[Abstract/Free Full Text]
  72. Martarelli D, Pompei P. Oxidative stress and antioxidant changes during a 24-hours mountain bike endurance exercise in master athletes. J Sports Med Phys Fitness ( 2009;) 49:: 122–7.[Web of Science][Medline]
  73. McIntyre I, Norman TR, Burrows GD, Armstrong SM. Human melatonin suppression by light is intensity dependent. J Pineal Res ( 1988;) 6:: 149–56.[CrossRef][Web of Science]
  74. Trinder J, Armstrong SM, O’Brien C, Luke D, Martin M. Inhibition of melatonin secretion onset by low levels of illumination. J Sleep Res ( 199;) 65:: 77–82.
  75. Baron Short E, Kose S, Mu Q, Borckardt J, Newberg A, George MS, et al. Regional brain activation during meditation shows time and practice effects: an exploratory FMRI study. eCAM ( 2007;) [Epub ahead of print: doi:10.1093/ecam/nem163].
  76. Ilhan N, Kamanli A, Ozmerdivenli R, Ilhan N. Variable effects of exercise intensity on reduced glutathione, thiobarbituric acid reactive substance levels, and glucose concentration. Arch Med Res ( 2004;) 35:: 294–300.[CrossRef][Web of Science][Medline]
  77. Cesarone MR, Belcaro G, Carratelli M, Cornelli U, De Sanctis MT, Incandela L. A simple test to monitor oxidative stress. Int Angiol ( 1999;) 18:: 127–30.[Web of Science][Medline]
  78. Alberti A, Bolognini L, Macciantelli D, Caratelli M. The radical cation of N,N-diethyl-para phenylendiamine: a possible indicator of oxidative stress in biological samples. Res Chem Intermed ( 2000;) 26:: 253–67.[CrossRef]
  79. Dohi K, Satoh K, Ohtaki H, Shioda S, Miyake Y, Shindo M, et al. Elevated plasma levels of bilirubin in patients with neurotrauma reflect its pathophysiological role in free radical scavenging. In Vivo ( 2005;) 19:: 855–60.[Abstract/Free Full Text]
  80. Watson TA, Callister R, Taylor RD, Sibbritt DW, MacDonald-Wicks LK, Garg ML. Antioxidant restriction and oxidative stress in short-duration exhaustive exercise. Med Sci Sports Exerc ( 2005;) 37:: 63–71.[CrossRef][Web of Science][Medline]
  81. Alcaraz-García MJ, Albaladejo MD, Acevedo C, Olea A, Zamora S, Martínez P, et al. Effects of hyperoxia on biomarkers of oxidative stress in closed-circuit oxygen military divers. Physiol Biochem ( 2008;) 64:: 135–41.[CrossRef]
  82. Phillips M, Cataneo RN, Greenberg J, Grodman R, Gunawardena R, Naidu A. Effect of oxygen on breath markers of oxidative stress. Eur Respir J ( 2003;) 21:: 48–51.[Abstract/Free Full Text]
  83. Reiter RJ, Tan DX, Manchester LC, Pilar Terron M, Flores LJ, Koppisepi S. Medical implications of melatonin: receptor-mediated and receptor-independent actions. Adv Med Sci ( 2007;) 52:: 11–28.[Web of Science][Medline]
  84. Orme-Johnson D. Medical care utilization and the transcendental meditation program. Psychosom Med ( 1987;) 49:: 493–507.[Abstract/Free Full Text]
  85. Orme-Johnson D. Evidence that the Transcendental Meditation program prevents or decreases diseases of the nervous system and is specifically beneficial for epilepsy. Med Hypotheses ( 2006;) 67:: 240–6.[CrossRef][Web of Science][Medline]
  86. Mourya M, Mahajan AS, Singh NP, Jain AK. J Effect of slow- and fast-breathing exercises on autonomic functions in patients with essential hypertension. Altern Complement Med ( 2009;) 15:: 711–17.[CrossRef]
  87. Yang K, Bernardo LM, Sereika SM, Conroy MB, Balk J, Burke LE. Utilization of 3-month Yoga program for adults at high risk for type 2 diabetes: a pilot study. eCAM ( 2009;).
  88. Adams JD, Garcia C. Palliative care among Chumash people. eCAM ( 2005;) 2:: 143–7.[Medline]
  89. Yang K. A review of yoga programs for four leading risk factors of chronic diseases. eCAM ( 2007;) 4:: 487–91.[Medline]
  90. Khalfa S, Bella SD, Roy M, Peretz I, Lupien SJ. Effects of relaxing music on salivary cortisol level after psychological stress. Ann N Y Acad Sci ( 2003;) 999:: 374–76.[CrossRef][Medline]
  91. Jevning R, Wilson AF, Smith WR, Morton ME. Redistribution of blood flow in acute hypometabolic behaviour. Am J Physiol ( 1978;) 235:: R89–92.[Web of Science][Medline]
  92. Lang R, Dehof K, Meurer KA, Kaufmann W. Sympathetic activity and transcendental meditation. J Neural Trans ( 1979;) 44:: 117–35.[CrossRef]
  93. Bujatti M, Riederer P. Serotonin, noradrenaline, dopamine metabolites in transcendental meditation technique. J Neural Trans ( 1976;) 39:: 257–67.[CrossRef]
  94. Moore RY. The innervation of the mammalian pineal gland. Prog Reprod Biol ( 1978;) 4:: 1–29.
  95. Zisapel N, Tarrasch R, Laudon M. The relationship between melatonin and cortisol rhythms: clinical implications of melatonin therapy. Drug Dev Res ( 2005;) 65:: 119–25.[CrossRef][Web of Science]
  96. Monteleone P, Fuschino A, Nolfe G, Maj M. Temporal relationship between melatonin and cortisol responses to nighttime physical stress in humans. Psychoneuroendocrinology ( 1992;) 17:: 81–6.[CrossRef][Web of Science][Medline]
Received March 31, 2009; accepted October 2, 2009


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