Abstract
Background:
The metabolic rate is an indicator of autonomic activity. Reduced sympathetic arousal probably resulting in hypometabolic states has been reported in several yogic studies.
Aim:
The main objective of this study was to assess the effect of yoga training on diurnal metabolic rates in yoga practitioners at two different times of the day (at 6 a.m. and 9 p.m.).
Materials and Methods:
Eighty eight healthy volunteers were selected and their metabolic rates assessed at 6 a.m. and 9 p.m. using an indirect calorimeter at a yoga school in Bangalore, India. Results and conclusions: The results show that the average metabolic rate of the yoga group was 12% lower than that of the non-yoga group (P < 0.001) measured at 9 p.m. and 16% lower at 6 a.m. (P < 0.001). The 9 p.m. metabolic rates of the yoga group were almost equal to their predicted basal metabolic rates (BMRs) whereas the metabolic rate was significantly higher than the predicted BMR for the non-yoga group. The 6 a.m. metabolic rate was comparable to their predicted BMR in the non-yoga group whereas it was much lower in the yoga group (P < 0.001). The lower metabolic rates in the yoga group at 6 a.m. and 9 p.m. may be due to coping strategies for day-to-day stress, decreased sympathetic nervous system activity and probably, a stable autonomic nervous system response (to different stressors) achieved due to training in yoga.
Keywords: Basal Metabolic Rate (BMR), decreased arousal response, yoga, yoga training
An understanding of metabolism at different times of the day has significant implications due to its link to sleep, health, stress and fatigue, ultimately determining the quality of life. BMR is the lowest (basal) metabolic rate measured just after waking from a night's sleep.[1] It is well known that sleep is a restorative process wherein the body synthesizes its necessary chemicals for growth, maintenance and development. Rejuvenation and repair take place during sleep.[2] Sleep generally brings down the metabolic rate by about 10%.[1,3] Low basal metabolic rates of yoga practitioners have been reported.[4] Hypometabolic states have been reported in yogic studies[5–8] wherein short and immediate effects of meditation and relaxation were observed.
Yoga which is a way of life is characterized by balance, health, harmony and bliss.[9] In yoga lore, three normal states of consciousness have been identified[10]—they are wakeful state (jagratha), dream or rapid eye movement (REM, swapna or dream state) and deep sleep without dreams (sushupti). Meditation is a part of yoga which is the seventh limb of Astanga yoga[11]—a state of alert rest as stated by Maharshi Mahesh Yogi.[12] This leads to superconsciousness or the fourth state of consciousness called the Samadhi, which is beyond the deep sleep state in terms of metabolism.[5,6]
Practice of yoga brings about changes such as slowing of the breath, calming of the mind and relaxation of the body leading to efficiency/balance or homeostasis.[9] The earliest study on metabolism by Anand et al.[13] has demonstrated that a yogi could reduce oxygen consumption while sealed in an airtight box for nearly ten hours, thus changing metabolism at will. Studies on meditation have demonstrated that Transcendental meditation (TM),[5,6] Zen Meditation,[8] Om Meditation[7] and Yogic Relaxation[14] reduce oxygen consumption, respiratory and heart rates and spontaneous Galvanic Skin Response (GSR).[15,16] The above changes are attributed mainly to reduced sympathetic activity / arousal response and decreased mental and muscular activities.
Studies done on a certain type of Pranayama (breathing technique) called UJJAYI demonstrated a 19% increase in oxygen consumption.[17] Right nostril breathing increased oxygen consumption by 28%.[18] Practice of Asanas or specific postures also increased oxygen consumption.[19,20] All these changes have been seen as the immediate acute effect of yoga practices. There is no literature report as to how long these changes last or the influence these practices have on the diurnal metabolic rates measured at two different times of the day in experienced yoga practitioners.
A typical yoga capsule usually consists of Asana, Pranayama and deep relaxation or meditation, which has a combined effect but ultimately leads to deep relaxation and reduced oxygen consumption.[4] It is believed that all these must have some permanent effect on metabolism when practised over a period of time, leading to efficiency and relief from stress, thereby resulting in certain changes in the diurnal metabolism, BMR and sleep.
Wallace et al. have reported the effect of acute practices resulting in the reduction in metabolic rate in meditation as compared to sleep.[5,6] The present study examines whether there is also a long-term effect of the combined practices.
With this background, the present study was conducted to know: (1) Is there any difference in the diurnal metabolic rate at two different times of the day (6 a.m. and 9 p.m.) of trained yoga subjects compared to those in the non-yoga group? (2) To compare the metabolic rate at 6 a.m. with that of the subjects' BMR values predicted by the 1985 Food and Agricultural Organization/World Health Organization/United Nations University (FAO/WHO/UNU) equations.[21]
SUBJECTS AND METHODS
The study was conducted at VYASA, a residential yoga research foundation near Bangalore. Out of 140 subjects screened, 88 (39 women, 49 men) normal, healthy subjects (as assessed by clinical examination) were selected for the study. These subjects were not taking any medication and did not have any sleep disorder. They were in the age range of 20–55 years (mean age = 33 yrs ± 9.88) with a mean weight of 58.36 ± 8.94 kg, mean height of 1.48 meters ± 0.23 and a mean body mass index (BMI) of 21.59 ± 3.09). The yoga group consisted of 27 men and 24 women who were trained in yoga for a minimum period of six months and who had been practising yoga for at least two hours a day, five days a week for 25 days a month (Appendix A). The non-yoga control group consisted of 22 men and 15 women who did not practice yoga but were staying in the same yoga institute under similar environmental conditions performing day-to-day activities of the center. Both the groups had similar activity profiles (other than yoga) and took the same simple vegetarian meal. The two groups were matched for weight, age and BMI [Table 1].
Table 1.
Age and anthropometrical characteristics of men and women of Yoga and Non-Yoga groups
| Groups | Total | Men | Women | |
|---|---|---|---|---|
| n | 51 | 27 | 24 | |
| Yoga | Age (y)ns | 33.44± 10.17 | 33.96±9.1 | 32.92±11.24 |
| Weight (kg)ns | 58.23± 8.53 | 60.59±8.89 | 55.88±8.18 | |
| Height (m)ns | 1.49±3.4 | 1.55±0.23 | 1.43±0.21 | |
| BMI (kg/m2)ns | 21.61±3.40 | 21.02±3.03 | 22.21±3.78 | |
| n | 37 | 22 | 15 | |
| Non-Yoga | Age (y)ns | 33.75± 9.59 | 34.18±9.65 | 33.33±9.53 |
| Weight (kg)ns | 58.5±9.34 | 61.73±9.43 | 55.27±9.26 | |
| Height (m)ns | 1.48± 0.24 | 1.55±0.25 | 1.42±0.24 | |
| BMI (kg/m2)ns | 21.58±2.78 | 21.12±2.77 | 22.04±2.79 |
Values are mean ± 1 standard deviation.
ns: Non-Significant between groups (Independent t test.)
m: Meters, BMI: Body mass index
All subjects had an early, simple, non-spicy vegetarian dinner at 6 p.m. The assessments were made early in the morning at around 6 a.m. and between 8.30 and 9 p.m. to eliminate the thermic effect of food on metabolism. The subjects were randomized for assessment, 50% of them being assessed at 9 p.m. and the other 50% at 6 a.m. Assessments were made in the morning only after the subjects had reported that they had slept for about seven hours.
The subjects were made to rest in a supine position for 20–30 minutes before the assessments were made twice for 15 min each with a gap of 15 minutes. The measurements were made in thermoneutral conditions at approximately 25°C in quiet surroundings and the average of two readings was taken.
The assessments were done by indirect calorimetry using OXYCON PRO from JAEGER, Germany. The instrument was calibrated daily for flow volume and gas analysis by using certified gases (mixture of 5.2% CO2 in nitrogen and atmospheric air, BOC, UK). VO2 (volume of oxygen), VCO2 (volume of carbon dioxide), VE (Ventilation), BF (Breath Flow), EE (Energy Expenditure) and RQ (Respiratory Quotient) were measured by triple V sensors-fast response gas analyzer based on the differential paramagnetic principle using a face mask. The gas analyzer is designed to analyze gases with a speed of 10 msec (100 Hz) with a breathing level of up to 80 breaths per minute.
The 1985 FAO/WHO/UNU equations (26) were used to predict values of BMR based on age, sex and body weight.
Statistical analysis
The data was analyzed using independent t test for comparing the yoga and non-yoga groups, paired t test for analyzing the intragroup effects. Analysis of co-variance was used to adjust the BMR for differences in body weights between the groups. SPSS 10 package was used for all the analyses. Differences were considered significant at P < 0.05 for all statistical procedures. The data is presented as mean ± standard deviation (SD).
RESULTS
Table 2 gives the details of energy expenditure of the yoga and non-yoga groups and their predicted values of two different assessments taken at 6 a.m. and 9 p.m. The yoga group showed significantly lower metabolic rates both at 6 a.m. and at 9 p.m. when compared to the non-yoga group (P < 0.001, P < 0.05). The 9 p.m. measurements of the yoga group were almost equal to their predicted values (before sleep). On the other hand, the non-yoga group had significantly higher metabolic rates before sleep and basal metabolic rates (SMR and BMR) comparable to their predicted values at 6 a.m. The EE/kg body weight values were also significantly lower in the yoga group at 6 a.m. and 9 p.m. (P < 0.01) when compared to the non-yoga group. The yoga group had significantly lowered values in other measured parameters as well such as VO2 (P < 0.03), VCO2 (P < 0.05), heart rate (P < 0.01) at 9 pm when compared with the non-yoga group and had lower values in VO2 (p < 0.001), VCO2 (p < 0.05), Breath rate (p < 0.05).
Table 2.
Energy Expenditure of Yoga and Non-yoga groups at 9 p.m. and 6 a.m.
| Metabolic rate at two different times of the day | Yoga n = 51 | Non-Yoga n = 37 |
|---|---|---|
| 9 p.m. MR (Kcal.d-1) | 1413.79±402.2* | 1604.17±326.86 |
| 6 a.m. MR (Kcal.d-1) | 1200.57±242.41**‡ | 1415.17±278.22 |
| 6 a.m. MR (Kcal.d-1.kg-1) | 20.61±4.16*‡ | 24.19±4.76 |
| Predicted BMR (Kcal.d-1) | 1385.36±165.24 | 1399.51±159.94 |
| Predicted BMR (Kcal.d-1.kg-1) | 23.79±2.84 | 23.92±2.73 |
Values are expressed as mean ± 1 SD.
MR: Metabolic Rate, BMR: basal metabolic rate
2. Significant at P < 0.05 comparisons between yoga and non-yoga groups, independent t test
** Significant at P< 0.001 using 9 p.m. values as covariate (Ancova), adjusted for body weight.
‡ Significant at P < 0.001 comparisons between yoga and non-yoga groups.
Independent † test compared with measured energy expenditure using predicted values.
ns Not Significant
Gender differences in energy expenditure and VO2 continued even after adjusting for body weight in the yoga group whereas no gender differences existed in the non-yoga group after adjusting for body weight (Ancova).
DISCUSSIONS
The main result of this study is that the yoga group had significantly lower metabolic rates at two different times of the day, i.e., 6 a.m. and 9 p.m. when compared to the non-yoga group. The yoga training had a beneficial effect on metabolism in general as seen in the lowered metabolic rate of the yoga group at 9 p.m. and reduced EE/kg body weight suggesting greater metabolic efficiency.
An earlier study by Anand et al.[13] on a yogi shut in an airtight box for ten hours showed reduced metabolic rate at the end of this period. However, the basal metabolic rate of the yogi had been within the normal range.
Wallace et al.[5,6] has shown that the practice of transcendental meditation leads to hypometabolic states (lowered metabolic rates) and proposed to call it the fourth state of consciousness, different from sleep yet metabolically equivalent or even below metabolic rates seen during sleep. He observed a 17% reduction in oxygen consumption during 20 min of transcendental meditation whereas after sleep, the metabolic rate was usually reduced by 10%.[2,3] Our study demonstrates that the acute effects of yoga practiced over a period of time, will have long-term effects on metabolism, leading to metabolic efficiency (as seen in the lowered EE/kg body weight).
High-intensity exercises increase the basal metabolic rates in subjects aged between 59–77[22] years whereas low and moderate intensity exercises do not have any effect on these rates.[23,24] All these exercises are mainly related to central or sympathetic activation[25] whereas yoga is reported to bring down sympathetic activity.[5,8,14] However, Yoga Asana (physical posture) is an energy expenditure activity[19,20] and hence, it was hypothesized that it would increase the resting metabolic rate. Contrary to this hypothesis, our study shows that Asanas when practised along with pranayama and meditation over a period of time actually reduce the metabolic rate. This may be due to alterations in autonomic nervous functions leading to autonomic stability as observed by Orme-Johnson,[15] who found that those practising TM showed stability in the rate of habituation, number of multiple responses and spontaneous GSR when compared to non-meditators. Silverman et al.[16] also observed low levels of sympathetic activity which have been correlated with greater resistance to stresses such as sensory deprivation. This deprivation can be attributed to decreased arousal response (reduced sympathetic activation) after TM meditation.
Table 3.
Genderwise comparison of BMR of Yoga and Non-Yoga groups along with their predicted values
| Yoga | Non-Yoga | |||
|---|---|---|---|---|
| Metabolic rates at two different times of the day | Women n = 24 | Men n = 15 | Women n = 27 | Men n = 22 |
| 9 p.m. MR (Kcal.d-1) | 1141.71±299.87ns | 1639.78±265.4§ | 1358.16±340.02ns | 1781.51±234.35 |
| 9 p.m. (Kcal.d-1.kg-1) | 20.75±5.47 | 24.32±4.8 | 27.06±5.61 | 28.86±3.8 |
| 6 a.m. MR (Kcal.d-1) | 1045.57±201.9**‡ | 1324.62±226.16**‡ | 1283.90±207.32ns | 1510.67±273.92ns |
| 6 a.m. MR (Kcal.d-1.kg-1) | 18.99±3.61**‡ | 22.07±4.09*‡ | 23.37±3.42 | 24.76±4.44 |
| Predicted BMR Kcal.d-1) | 1242.14±93.36 | 1505.96±108.77 | 1256.06±90.92 | 1504.9±103.24 |
Values are in mean ± 1 SD
MR = Metabolic rate
** Significant at P < 0.005 comparisons between yoga and non-yoga groups
2. Significant at P < 0.05 comparisons between yoga and non-yoga groups, multivariate analysis using 9 p.m. values as covariate
‡ Significant at P < 0.001 compared to predicted values
ns: Not Significant when compared with predicted values.
Table 4.
Genderwise comparison of yoga and non-yoga groups in all parameters other than energy expenditure
| Yoga | Non-Yoga | |||
|---|---|---|---|---|
| Ventilatory parameter and heart rate | Women n = 24 | Men n = 15 | Women n = 27 | Men n = 22 |
| 9 p.m. VE [l/min] | 6.15±1.64 | 7.96±1.83 | 6.56±1.55 | 8.53±1.11 |
| 6 a.m. VE [l/min] | 5.35±1.03ns | 6.17±1.00** | 6.22±1.25 | 7.4±1.46 |
| 9 p.m. BF [1/min] | 17.52±10.54 | 14.44±4.57 | 19.50±2.38 | 14.8±4.13 |
| 6 a.m. BF [1/min] | 14.49±3.52* | 12.43±3.72** | 17.86±2.14 | 14.38±3.09 |
| 9 p.m. VO2, [ml/min] | 166.15±38.83 | 237.44±45.17 | 195.99±37.74 | 253.28±33.65 |
| 6 a.m. VO2 [ml/min] | 153.35±26.23** | 195.46±27.62* | 186.47±31.93 | 216.29±38.8 |
| 9 p.m. VCO2 [ml/min] | 154.07±38.22 | 220.00±47.09 | 174.52±31.86 | 238.16±30.5 |
| 6 am VCO2 [ml/min] | 140.36±25.08* | 173.21 ±26.92** | 161.81 ±26.41 | 198.87±36.31 |
| 9 pm HR [beats/min] | 69.06±9.32 | 68.16±9.06 | 78.63±8.56 | 72.62±8.29 |
| 6 am HR [beats/min] | 69.64±8.99ns | 65.09±9.9ns | 72.09±5.76 | 67.84±12.45 |
Values mean ± SD
Significant at P <0.005 genderwise comparison between yoga and non-yoga groups, multivariate analysis using 9 p.m. values as covariate.
2. Significant at P < 0.05 genderwise comparison between yoga and non-yoga groups, multivariate analysis using 9 p.m. values as covariate
ns: Not Significant, VE: Ventilation, BF: Breath flow, VO2: Volume of oxygen
VCO2: Volume of carbon dioxide, HR: Heart rate.
There are other yoga techniques such as Om meditation,[7] Zen meditation,[8] Cyclic meditation[14] and certain pranayamas (breathing techniques),[17,26] in which decreased metabolic rate, heart rate, reduction in Oxygen consumption, carbon dioxide elimination, breath rate, breath volume and pulse rate were observed as acute effects (pre- compared to post- levels). Electroencephalograms (EEGs) recorded by Banquet et al.[27] showed predominant alpha wave activities with increased amplitude and frequency but few theta waves during the practice of Transcendental meditation. Our study not only endorses this view but also adds that the integrated approach of yoga training can convert these short-term changes into more permanent expressions as noticed in the changes in metabolic rates of the yoga group at 6 a.m. and 9 p.m. and the changes in EE/kg body weight.
The BMR which includes the cost of arousal, represents the activation of the central and sympathetic nervous systems from sleep to basal levels[28] and may be influenced by various factors including control over the state of one's mind.[9]
The lower 6 a.m. metabolic rate of the yoga group suggests that the combined practice of yoga has an overall calming effect and is manifested as decreased sympathetic activity.[6,7,14] Orme Johnson[15] has further demonstrated that greater the regularity of practice, greater was the increase in autonomic stability. This is also amply demonstrated by the lowered metabolic rates of the yoga group both at 6 a.m. and 9 p.m. compared to the metabolic rates of the non-yoga group in our study. These lower metabolic rates can be attributed to the decreased sympathetic tone and decreased arousal response in general and a greater ability to recover from stressful conditions quickly. This is evident when we look at the differences in the yoga and non-yoga groups at 9 p.m., which existed even after adjusting for body weight (using Ancova).
Furthermore, studies on the long-term effects of yoga on the BMR of normal healthy volunteers have shown that yoga groups had lower BMR compared to non-yoga groups[4] which has also been confirmed by our study.
There are however, contradictory reports about gender differences in SMR/BMR, a few claiming that the differences do not exist when adjusted for Body weight, Fat mass or Fat-Free Mass[28–30] while others claim that gender differences exist even after accounting for these parameters.[31,32] In our study, gender differences although not found in the non-yoga group, existed in the yoga group. This suggests that training in yoga may have different effects on men and women as women respond differently to stress.[33,34] A further detailed study on the effect of training on gender differences along with a detailed analysis of body composition (Fat mass, Fat-free mass and Fat distribution) may be necessary to determine the precise cause of these differences.
We conclude that the long-term practice of yoga leads to lower metabolic rates and probably greater metabolic efficiency mainly due to reduced sympathetic activity and / or stabilized nervous system. The main limitation of this study is that it is not a prospective randomized control study and hence, conclusions can not be drawn based on these results. However, the results are consistent with expectations based on other studies and thus, encouraging to conduct further investigations.
APPENDIX A
Details of yoga practices done by the yoga group selected for the study
All the subjects practise a 60–90 min capsule consisting of Asana, Pranayama and Meditation daily for six days a week.
Breathing
Hands in and out
Ankle stretch
Tiger
Rabbit
Loosening
Heals touching
Tadasana techniques
Asana Practices: Standing posture
Trikona asana
Parivrutha trikonasana
Ardha kati Chakrasana
Ardha Chakrasana
Sitting Asanas
Paschimothanasan
Ushtrasana
Vakrasna/Matyendrasana
Supine postures
Halasana
Chakrasana
Sarvangasana
Matsyasana
Prone postures
Bhujanghasana
Shalabhasana
Dhanurasana
Pranayama
Kapala Bhathi.
Nadi shuddi
Omkar chanting
Meditation 5–10 minutes
REFERENCES
- 1.Robinson CH, Lawler MR, Chenoweth WL, et al. Normal and therapeutic Nutrition. 7th ed. New York: Mc Milan Publishing Co; 1986. p. 103. [Google Scholar]
- 2.Adam K. Sleep as a restorative process and a theory to explain why. Prog Brain Res. 1980;53:289–305. doi: 10.1016/S0079-6123(08)60070-9. [DOI] [PubMed] [Google Scholar]
- 3.Bijlani RL. Understanding medical physiology. 2nd ed. New Delhi: Jaypee Brother's Medical Publishers; 1977. p. 421. [Google Scholar]
- 4.Chaya MS, Kurpad AV, Nagendra HR, Nagarathna R. The effect of long term combined yoga practice on the basal metabolic rate of healthy adults. BMC Complement Altern Med. 2006;6:28. doi: 10.1186/1472-6882-6-28. [DOI] [PMC free article] [PubMed] [Google Scholar]
- 5.Wallace RK, Benson H. Altered States of awareness. Readings from scientific American. San Francisco: WH Freeman and Co; 1972. The physiology of meditation; p. 2. [Google Scholar]
- 6.Wallace RK, Benson H, Wilson AF. A Wakeful hypo metabolic physiologic state. Am J Physiol. 1971;221:795–9. doi: 10.1152/ajplegacy.1971.221.3.795. [DOI] [PubMed] [Google Scholar]
- 7.Telles S, Nagaratna R, Nagendra HR. Autonomic changes during OM meditation. Indian J Physiol Pharmacol. 1995;39:418–20. [PubMed] [Google Scholar]
- 8.Sugi Y, Akutsu K. Studies on respiration and energy metabolism during sitting in Za Zen. Res J Physiol Educ. 1968;12:190–206. [Google Scholar]
- 9.Nagendra HR, Nagaratna R. New perspective in stress management. Bangalore India: Vivekananda Kendra Prakashana; 1977. [Google Scholar]
- 10.Swami Nikhilananda. Calcutta: Advaitha Ashram; 1995. Mandokya Upanishad with Gaudapada Karika and sankara's commentary. [Google Scholar]
- 11.Taimini LK. The science of yoga. Madras, India: The Theosophical Publishing House; 1961. [Google Scholar]
- 12.Maharshi Mahesh Yogi. The science and art of living Los Angeles. New York: International SRM Publications; 1972. [Google Scholar]
- 13.Anand BK, Chhina GS, Singh B. Studies on Shri Ramanada Yogi during his stay in an air tight box. Indian J Med Res. 1961;49:82–9. [PubMed] [Google Scholar]
- 14.Telles S, Reddy SK, Nagendra HR. Oxygen consumption and respiration following two Yoga based relaxation techniques. Appl Psychophysiol Biofeedback. 2000;25:221–7. doi: 10.1023/a:1026454804927. [DOI] [PubMed] [Google Scholar]
- 15.Orme-Johnson DW. Autonomic stability and transcendental meditation. Psychosom Med. 1973;35:341–9. doi: 10.1097/00006842-197307000-00008. [DOI] [PubMed] [Google Scholar]
- 16.Silverman AJ, Cohen SI, Shmavonian BM. Psycho physiologic investigation in sensory deprivation. Psychosomat Med. 1961;23:48–62. [Google Scholar]
- 17.Miles WR. Oxygen consumption during 3-yoga type breathing pattern. J Appl Physiol. 1964;19:75–82. doi: 10.1152/jappl.1964.19.1.75. [DOI] [PubMed] [Google Scholar]
- 18.Telles S, Nagaratna R, Nagendra HR. Breathing through a particular nostril can alter metabolic and autonomic activities. Indian J Physiol Pharmacol. 1994;38:133–7. [PubMed] [Google Scholar]
- 19.Rai L, Ram K. Energy expenditure and ventilatory responses during Siddasana: A yogic seated posture. Indian J Physiol Pharmocol. 1994;38:29–33. [PubMed] [Google Scholar]
- 20.Rai L, Ram K. Energy expenditure and ventilatory responses during veerasana a yogic standing posture. Indian J Physiol Pharmacol. 1993;37:45–50. [PubMed] [Google Scholar]
- 21.FAO/WHO/UNU expert consultation. Energy and protein requirements. WHO tech rep ser. 1985:724. [PubMed] [Google Scholar]
- 22.Williamson DL, Kirwn JP. A single bout of concentric resistance exercise increases basal metabolic rate in 48 hours after exercise in healthy 59-77 yrs old men. J Gerontol A Biol Sci Med Sci. 1997;52:M352–5. doi: 10.1093/gerona/52a.6.m352. [DOI] [PubMed] [Google Scholar]
- 23.Gilliat-Wimberly M, Manore MM, Wooly K, Swan PD, Carrrol SS. Effects of habitual activity on resting metabolic rates and Body composition of women aged 35-50 yrs. J Am Diet Assoc. 2001;101:1181–8. doi: 10.1016/S0002-8223(01)00289-9. [DOI] [PubMed] [Google Scholar]
- 24.Ribeyre J, Fellmann N, Montaurier C, Delaitre M, Vernet J, Coudert J, et al. Daily energy expenditure and its main components as measured by indirect calorimetry in athletes and non-athletic adolescents. Br J Nutr. 2000;83:355–62. [PubMed] [Google Scholar]
- 25.McArdle WD, Katch FI, Katch VL. Exercise physiology. 4th ed. Baltimore: Williams and Wilkins; 1996. pp. 339–55. [Google Scholar]
- 26.Telles S, Desi Raju T. Oxygen consumption during pranayama type of very slow rate breathing. Indian J Med Res. 1991;94:357–63. [PubMed] [Google Scholar]
- 27.Banquet JP. Spectral analysis of the EEG in meditation. Electroencephalogr Clin Neurophysiol. 1973;35:143–51. doi: 10.1016/0013-4694(73)90170-3. [DOI] [PubMed] [Google Scholar]
- 28.Fontvielle AM, Ferraro RT, Rising R, Larsol DE, Ravussine E. Energy cost of arousal: Effect of sex race and obesity. Int J Obes Relat Metab Disord. 1993;17:705–9. [PubMed] [Google Scholar]
- 29.Goldberg GR, Prentice AM, Davies HL, Murgatroyd PR. Overnight and basal metabolic rate in men and women. Eur J Clin Nutr. 1988;42:137–44. [PubMed] [Google Scholar]
- 30.Seal JL, Conway JM. Relationship between overnight energy expenditure and BMR measured in a room sized calorimeter. Eur J Clin Nutr. 1999;53:107–11. doi: 10.1038/sj.ejcn.1600685. [DOI] [PubMed] [Google Scholar]
- 31.Ferro-Luzzi A, Petrachi C, Kurian R, Kurpad AV. Basal metabolism of weight-stable chronically undernourished men and women: Lack of metabolic adaptation and ethnic differences. Am J Clin Nutr. 1997;66:1086–93. doi: 10.1093/ajcn/66.5.1086. [DOI] [PubMed] [Google Scholar]
- 32.Kanady AN, Gokhale MK, Rao S. Energy costs of standard activities among Indian adults. Eur J Clin Nurt. 2001;55:708–13. doi: 10.1038/sj.ejcn.1601211. [DOI] [PubMed] [Google Scholar]
- 33.al'Absi M, Wittermers LE., Jr Enhanced adreno cortical responses to stress in hyper tension prone men and women. Ann Behav Med. 2003;25:25–33. doi: 10.1207/S15324796ABM2501_04. [DOI] [PubMed] [Google Scholar]
- 34.Traustadottir T, Bosch PR, Matt KS. Gender differences in cardiovascular and hypothalamic-pituitary-adrenal axis responses to psychological stress in healthy older adult men and women. Stress. 2003;6:133–40. doi: 10.1080/1025389031000111302. [DOI] [PubMed] [Google Scholar]