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Physiological responses to Tai Chi in stable patients with COPD
Respiratory Physiology & Neurobiology 221 (2016) 30–34
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Physiological responses to Tai Chi in stable patients with COPD Zhi-Hui Qiu a , Hong-Xi Guo a , Gan Lu b , Ning Zhang a , Bai-Ting He a , Lian Zhou a , Y.M. Luo a,∗ , M.I. Polkey c a b c
State Key Laboratory of Respiratory Disease, Guangzhou Medical University, 151 Yanjiang Road, Guangzhou, China Jiangsu Province Official Hospital, Nanjing 210024, China NIHR Respiratory Biomedical Research Unit at the Royal Brompton and Harefield NHS Foundation Trust and Imperial College, London, UK
a r t i c l e
i n f o
Article history: Received 1 July 2015 Received in revised form 29 October 2015 Accepted 30 October 2015 Available online 11 November 2015 Keyword: COPD Exercise Pulmonary rehabilitation
a b s t r a c t We compared the physiological work, judged by oxygen uptake, esophageal pressure swing and diaphragm electromyography, elicited by Tai Chi compared with that elicited by constant rate treadmill walking at 60% of maximal load in eleven patients with COPD (Mean FEV1 61% predicted, FEV1 /FVC 47%). Dynamic hyperinflation was assessed by inspiratory capacity and twitch quadriceps tension (TwQ) elicited by supramaximal magnetic stimulation of the femoral nerve was also measured before and after both exercises. The EMGdi and esophageal pressure at the end of exercise were similar for both treadmill exercise and Tai Chi (0.109 ± 0.047 mV vs 0.118 ± 0.061 mV for EMGdi and 22.3 ± 7.1 cmH2 O vs 21.9 ± 8.1 cmH2 O for esophageal pressure). Moreover the mean values of oxygen uptake during Tai Chi and treadmill exercise did not differ significantly: 11.3 ml/kg/min (51.1% of maximal oxygen uptake derived from incremental exercise) and 13.4 ml/kg/min (52.5%) respectively, p > 0.05. Respiratory rate during Tai Chi was significantly lower than that during treadmill exercise. Both Tai Chi and treadmill exercise elicited a fall in IC at end exercise, indicating dynamic hyperinflation, but this was statistically significant only after treadmill exercise. TwQ decreased significantly after Tai Chi but not after treadmill. We conclude that Tai Chi constitutes a physiologically similar stimulus to treadmill exercise and may therefore be an acceptable modality for pulmonary rehabilitation which may be culturally more acceptable in some parts of the world. © 2015 Elsevier B.V. All rights reserved.
1. Introduction Pulmonary rehabilitation (PR) is a therapy of proven efficacy in Chronic Obstructive Pulmonary Disease (COPD) (Griffiths et al., 2000), but classical PR entails the provision of centralized facilities with dedicated exercise equipment and staff. This can limit uptake of this therapy both because it confers a finite limit to the number of patients that can be treated at any one time, and because patients may find travelling to a central facility a deterrent (O’Shea et al., 2007; Keating et al., 2011). Secondly, where PR can only be given for fixed periods a detarining effect occurs so that both exercise capacity and quality of life usually decline gradually after completion of PR (Griffiths et al., 2000).
∗ Corresponding author at: Professor of Respiratory Medicine, State Key Laboratory of Respiratory Disease, 151 Yanjiang Road, Guangzhou 510120, China. Fax: +86 20 34284122. E-mail address: [email protected] (Y.M. Luo). http://dx.doi.org/10.1016/j.resp.2015.10.019 1569-9048/© 2015 Elsevier B.V. All rights reserved.
Tai Chi is a traditional form of exercise developed in China, originally as a martial art for combat purposes. Tai Chi consists of a series of slow but continuous movements of many parts of the body. There is experimental evidence from both cross-sectional and longitudinal studies that Tai Chi exercise has beneficial effects on cardiovascular fitness (Chang et al., 2011), balance control and psychological well-being (Chyu et al., 2010). Since the movements can be adapted to suit people with physical weaknesses or disabilities, Tai Chi has become increasingly popular among elderly people in Hong Kong, mainland China, and other parts of the world (Wang et al., 2010; Li et al., 2012; Leung et al, 2013). Tai Chi could therefore potentially replace western style PR with the advantages both that class sizes are not limited by the quantity of specialized exercise equipment and that the patient may continue the exercise at home after the end of formal training. However, whilst the clinical studies noted above support the value of Tai Chi, some physiologic questions remain unanswered. First, no study has assessed respiratory mechanics during Tai Chi probably because of the difficulty recording esophageal pressure and EMGdi during free movement. Consequently, it is unknown what level
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of respiratory load is elicited by this therapy. In particular, since Tai Chi requires control of breathing during exercise we hypothesized that this may reduce breathing frequency and thus confer a beneficial effect on dynamic hyperinflation compared with treadmill exercise. Secondly it is unknown whether Tai Chi is sufficient to elicit low frequency quadriceps fatigue, which would indicate that the exercise is sufficiently intense to produce a training effect (Mador et al., 2001). To address these questions we undertook a detailed physiological comparison of 24-form Yang style Tai Chi, the most widely practiced style today, and constant rate treadmill walking.
2. Methods Eleven patients with COPD (age 62 ± 8 years, FEV1 61 ± 27 % of predicted) were recruited from community. All patients had practiced Tai Chi for more than one year and were free of clinically significant coexistent diseases (e.g., cardiac disease, neuromuscular disorders or severe arthritis) that might preclude exercise and had not had an exacerbation of COPD within the preceding month. Patients with cancer or severe obesity were also excluded. The study was approved by the Ethical committee of the first affiliated hospital of Guangzhou Medical University. All participants provided written informed consent to participate.
2.1. Protocol Each patient visited the laboratory four times with a two-dayinterval between visits. At visit 1 patients received a physical examination and we measured spirometry. At visit 2 an incremental treadmill exercise to determine each individual’s maximal load was performed. The incremental treadmill exercise protocol consisted of 3 min standing still followed by an increase in the load every three minutes by increasing 0.5 km/h until intolerable dyspnea or exhaustion occurred; dyspnea was not quantified during the incremental test using a Borg or similar score, but patients were encouraged to continue until the limit of tolerability. Visits 3 and 4 were for the physiologic study of either Tai Chi or constant rate treadmill walking at 60% of maximal load determined at visit 2. Constant load exercise and Tai Chi which consisted of 10 repeated sections with 6 min duration for each section were performed in random order. Participants were asked to exercise on a treadmill for 60 min to match the duration of Tai Chi which is usually last 60 min. A five minute warm up was allowed before Tai Chi. A video of one of the participants undertaking Tai Chi may be viewed at online supplement (http://183.63.72.215:88/play/index. html).
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2.2. Measurements The same measurements were made before, during and after both Tai Chi and constant rate exercise as follows. A long (5 m) lead suspended from a pulley that was free to move at the level of the laboratory ceiling was used to permit recording of EMGdi and esophageal pressure during Tai Chi exercise without limiting the participants movement (Please see online video). Inspiratory capacity (IC) was performed before and immediately after exercise to quantify dynamic hyperinflation (Guenette et al., 2012). Oxygen uptake (VO2 ), carbon dioxide production (VCO2 ), minute ventilation (VE ), respiratory rate, heart rate and SpO2 were continually measured with a facemask and finger probe connected to a portable metabolic ‘cart’ worn by patient (K4b2 , COSMED,Italy) during exercise. Respiratory rate and VO2 during exercise were considered the average of 3 min before the end of exercise and compared with 3 min during rest. Since Tai Chi requires breathing control we did not feel it appropriate to perform interval measures of IC or to ask participants to vocalise to record Borg dyspnea or leg scores, and therefore did not undertake these during treadmill exercise either. Diaphragm electromyography (EMGdi) was recorded using a combined multipair esophageal electrode catheter with an esophageal balloon mounted on it passed pernasally, as previously described(Luo et al., 2009; Jensen et al., 2011). The EMG signals were bandpass filtered between 20 and 1000 Hz and amplified (Bioamplifier Model RA-8, Yinghui Guangzhou, China). The esophageal balloon was filled with 0.5 ml air and connected to a pressure transducer (DP15, Validyne Corp., Northrige, CA, USA). Quadriceps fatigue was evaluated by measuring the unpotentiated quadriceps twitch tension (TwQ) using the similar technique previously described (Polkey et al., 1996; Hamnegard et al., 2004). The participants were studied supine with the knee flexed at 90◦ over the end of the chair. An inextensible strap was placed around the ankle and connected to a strain gauge (strain stall range 0–100 kg) mounted to the back of the chair so that the strap ran perpendicular to the ankle and gauge. A 43-mm figure-of-eight coil powered by a Magstim 200 stimulator (Magstim Company Limited, Whitland, Dyfed, Wales) was used to stimulate the right femoral nerve; a minimum of 5 stimulations at 100% of stimulator output were given and the mean TwQ used for analysis. The unpotentiated TwQ was measured before, 20 min and 60 min after both constant load treadmill and Tai Chi exercise.
2.3. Statistical analysis Data were presented as mean ± SD. A two way repeated measures ANOVA and a paired t-test were used to assess the differences between Tai Chi and treadmill exercise.
Table 1 characteristic of patients with COPD. Subject no.
Sex
1 2 3 4 5 6 7 8 9 10 11 Mean SD
M M M M M M F M M M M ¡¡ ¡¡
Age (years) 62 63 63 57 66 71 54 67 46 72 57 62 8
Weight (kg) 64.0 67.0 83.6 67.5 65.0 71.0 59.0 57.0 76.0 56.0 56.0 65.6 8.8
Height (cm)
162 165 170 169 163 161 157 165 168 163 159 164 4
BMI (kg/m2 )
FEV1 (litre)
24.4 24.6 28.9 23.6 24.5 27.4 23.9 20.9 26.9 21.1 22.2 24.4 2.5
2.88 2.24 1.54 1.31 1.10 1.52 1.45 0.59 2.02 2.36 0.76 1.62 0.70
FEV1 (% pred) 108 85 54 44 44 67 66 22 60 97 28 61 27
VC (litre)
FEV1 /VC (%)
IRV (litre)
IC (litre)
Smoking (years)
4.80 3.82 3.76 3.25 2.31 2.78 2.70 2.72 3.90 3.73 3.33 3.37 0.72
60.0 58.6 41.0 40.3 47.6 54.7 53.7 21.7 51.8 63.3 22.8 46.9 14.2
3.12 1.46 1.19 1.52 0.84 1.48 1.01 0.57 1.17 0.53 0.56 1.22 0.73
3.62 2.24 2.82 1.56 1.81 2.01 2.41 1.40 2.47 2.34 1.61 2.21 0.64
30 40 40 30 10 30 0 40 30 30 30 28 13
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Fig. 1. EMGdi recorded from five pairs of electrode and esophageal pressure during rest, beginning, middle and end of Tai Chi exercise and treadmill exercise.
3. Results 3.1. Tai Chi and constant rate treadmill exercise compared Eleven stable patients with GOLD I to IV COPD (10 men and 1 women) were studied; demographic data are shown in Table 1. Good quality EMGdi signals were recorded during both treadmill exercise and Tai Chi (Fig. 1). Borg breathlessness and leg scores were 5.3 ± 1.3 and 4.9 ± 1.2 at the end of treadmill exercise and 5.5 ± 1.4 and 4.9 ± 1.2 after Tai Chi, respectively (p > 0.05). Mean values of oxygen uptake during Tai Chi and treadmill exercise were similar and were 11.28 ml/kg/min (51.1% of maximal VO2 ) and 13.41 ml/kg/min (52.5% of maximal VO2 ) respectively, p > 0.05. An example of breath by breath VO2 over the one hour recording period are shown for Tai Chi and constant rate treadmill exercise (Fig. 2). It is evident that due to the cyclical nature of Tai Chi these parameters fluctuate but remain relatively constant during treadmill walking. Two participants during Tai Chi and three participants during treadmill could not exercise for 60 min (Table 2). Data obtained during the hour of exercise are shown in Table 3, with esophageal pressure (Pes ) and EMGdi in Fig. 3. Both EMGdi and esophageal pressure decreased slightly during treadmill while they were stable during Tai Chi. However, the EMGdi and esophageal pressure at the end of exercise are almost the same between treadmill exercise and Tai Chi (0.109 ± 0.047 mV vs 0.118 ± 0.061 mV for EMGdi and 22.3 ± 7.1 cmH2 O vs 21.9 ± 8.1 cmH2 O for Pes ). For most physiological responses entailed by Tai Chi did not differ from treadmill walking at 60% VO2max (Fig. 4). Significant differences were observed after exercise in tidal volume which was higher at the end of exercise after Tai Chi (1.2 ± 0.5 l) than after treadmill walking (1.0 ± 0.3 l) while respiratory frequency at the end of treadmill exercise (30 ± 6 breaths/min) was higher than that at the end of Tai Chi (25 ± 4 breaths/min) although oxygen uptake was not significantly different between Tai Chi and treadmill exercise (0.81 ± 0.28 l/min vs 0.70 ± 0.16 l/min) (Table 2). As expected both Tai Chi and treadmill exercise elicited a fall in IC from 2.20 ± 0.71 l to 2.01 ± 0.79 l (p = 0.065) for Tai Chi and 2.26 ± 0.68–1.92 ± 0.67 l
Fig. 2. Oxygen uptake over a 1 h period in which the subject either did Tai Chi (upper panel) and on another occasion walking at 60% of VO2max . In the Tai Chi panel the periodicity of 10 six minutes cycles is evident.
Fig. 3. Oxygen uptake, EMGdi and Pes during Tai Chi and treadmill exercise; mean data from all participants.
(p < 0.01) for treadmill exercise, but this was statistically significant only after treadmill exercise. 3.2. Exercise tasks and quadriceps fatigue TwQ data are shown in Table 4. TwQ decreased significantly at 20 min and 60 min after Tai Chi but there was no difference between before and after constant treadmill exercise at 60% of maximal load. 4. Discussion This is the first study to record the EMGdi and esophageal pressure during Tai Chi which requires free movement. The main finding of the current study is that Tai Chi exercise is similar to treadmill exercise at 60% of maximal load in terms of the elicited EMGdi and esophageal pressure. Respiratory rate during Tai Chi was less than that during treadmill and dynamic hyperinflation as judged by IC is also less severe after Tai Chi than after treadmill at 60% of maximal work rate. Tai Chi induced low frequency
Fig. 4. Relation between ventilation and oxygen uptake (A), oxygen saturation and oxygen uptake (B), carbon dioxide production (Vco2 ) and oxygen uptake (C), heart rate and oxygen uptake (D) and the relation between EMGdi and ventilation (E), Pes and ventilation (F), tidal volume and ventilation (G), respiratory frequency (RF) and ventilation (H) during Tai Chi and treadmill exercise. Values presented are the mean of all participants at epochs of 10% total exercise time (6 min unless patient failed to complete 1 h task).
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Table 2 Respiratory frequency and oxygen uptake during treadmill and Tai Chi exercises.
Subject no.
Respiratory frequency (breaths/min)
VO2 (l/min)
Tai Chi
Tai Chi
Treadmill
Rest 1 2 3 4 5 6 7 8 9 10 11 Mean SD
End
21 21 23 21 23 18 15 34 17 25 19 21 5
22 24 26 25 27 24 27 37 20 22 26 25 4
Rest
End
25 18 24 19 24 20 14 23 16 22 20 21 3
23 32 35 29 27 39 24 40 21 28 29 30 6
Exercise duration Treadmill
Tai Chi
Treadmill
Rest
End
Rest
End
(min)
(min)
0.51 0.50 0.30 0.31 0.55 0.49 0.20 0.22 0.26 0.37 0.29 0.36 0.13
1.27 0.74 0.97 0.36 1.17 0.60 0.75 0.54 1.04 0.74 0.71 0.81 0.28
0.37 0.32 0.49 0.30 0.34 0.31 0.18 0.30 0.34 0.23 0.25 0.31 0.08
0.98 0.75 0.97 0.53 0.78 0.60 0.68 0.51 0.69 0.55 0.65 0.70 0.16
60 60 60 44 60 60 60 25 60 60 60 55 11
60 60 60 28 60 35 60 12 60 60 60 50 17
Table 3 Cardiopulomonary data including esophageal pressure (Pes) and EMGdi during Tai Chi and treadmill exercise. Parameter
Tai Chi exercise
RF(b/m) VT(L) VE(L/m) VO2 (L/m) VCO2 (L/m) HR(bpm) SpO2 (%) EMGdi (V) Pes (cmH2 O)
Treadmill exercise
Rest
Mean
End
Rest
Mean
End
21.5 (5.1) 0.8 (0.2) 15.7 (3.7) 0.36 (0.13) 0.36 (0.09) 80 (12) 96 (1) 58.3 (28.6) 12.8 (6.7)
*
*
20.7 (3.5) 0.7 (0.1) 14.2 (2.9) 0.31 (0.08) 0.31 (0.06) 78 (11) 96 (1) 54 (19) 12.2 (4.2)
28.7 (4.6) 1.1 (0.3) 32.9 (11.5) 0.88 (0.30) 0.90 (0.28) 111 (13) 93 (4) 119 (56) 23.8 (7.0)
29.8 (6.2) 1.0 (0.3) 27.3 (6.5) 0.70 (0.16) 0.71 (0.16) 112 (13) 94 (5) 109 (47) 22.3 (7.1)
24.7 (2.4) 1.1 (0.3) 27.4 (5.7) 0.74 (0.22) * 0.74 (0.17) 104 (21) 95 (4) 113 (57) 21.4 (7.7)
25.5 (4.5) ** 1.2 (0.5) 30.0 (8.2) 0.81 (0.28) * 0.81 (0.25) 110 (22) 94 (5) 118 (61) 21.9 (8.1)
RF, respiratory frequency; HR, heart rate; bpm, beats per minute; mean, mean of 60 min; end, mean value of the last three minutes. * p < 0.05 between Tai Chi and treadmill. ** p < 0.01. Table 4 Quadriceps twitch force (kg) measured by magnetic stimulation before and 20 min and 60 min after exercise. Subject no.
1 2 3 4 5 6 7 8 9 10 11 Mean SD
Tai Chi
Treadmill
Before
20 min
60 min
Before
20 min
60 min
8.3 7.3 7.5 9.4 9.4 7.4 10.2 11.9 5.8 7.8 11.0 8.7 1.8
6.5 7.6 6.5 9.1 8.1 6.8 8.4 11.3 3.7 6.4 9.6 7.6 2.0
7.0 7.2 6.7 8.4 8.2 6.9 8.7 11.8 4.6 6.6 9.9 7.8 1.9
7.7 7.1 8.0 8.3 7.4 7.0 9.8 11.3 4.8 7.2 10.2 8.1 1.8
7.9 11.0 6.9 7.4 7.3 7.1 10.6 10.9 4.9 7.9 11.1 8.5 2.1
7.7 9.7 6.4 8.1 7.4 7.1 10.2 10.7 4.8 6.9 10.9 8.2 2.0
quadriceps fatigue, suggesting that Tai Chi may constitute an adequate exercise load to be an effective form of PR in patients with COPD.
4.1. Critique of the method This is a physiological study performed on a small number of participants with a range of disease severity. While the purpose of the study was to further evaluate the potential suitability of Tai Chi as a form of rehabilitation, the present data themselves cannot be interpreted as an evidence base for Tai chi as a form of PR.
4.2. Significance of the findings Since the seminal work of Casaburi et al. (1991) over 20 years ago it has been accepted that greater training benefits are realized if higher training intensities are used. Current recommendations are that intensities greater than 60% of maximal load are prescribed for COPD patients undertaking physical training (Troosters et al., 2005), although the exercise prescription may be obtained from a field test of exercise performance such as the incremental shuttle walk test (British Thoracic Society Standards of Care Subcommittee on Pulmonary, 2001). The principal finding of the current study is that the mean oxygen uptake observed during Tai Chi did not differ from that obtained during treadmill exercise at 60% of maximal load. Interestingly however the respiratory pattern adopted differed between the exercise modality so that Tai Chi was characterized by less increase in respiratory rate and a greater increase in tidal volume. As a consequence of this walking, Tai Chi was less associated with dynamic hyperinflation. Our data thus suggest that Tai Chi produces a sufficiently vigorous exercise to constitute a training modality. These data are consistent with those of Leung et al., (2013) but add to it both because in their study VO2max was inferred from a field exercise test rather than measured directly as was the case in this study, as well as the other physiologic data gathered in the present study. Tai Chi may be regarded as a composite form of exercise. As can be seen from the video link (see methods) key features of the technique in comparison to constant rate exercise are the fluctuating level of exercise intensity, the focus on posture and on breathing control. By its nature Tai Chi is cyclical whereas treadmill exercise is not; it may therefore be considered that Tai Chi is more analogous to interval training in some respects. The
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principle of interval training is that, by taking breaks, the patient may be able to reach a higher training intensity for short periods and thus provide a greater training stimulus. However, despite the cyclical nature of Tai Chi, respiratory neural output as assessed by EMGdi or esophageal pressure is overall remarkably constant (Fig. 3) during Tai Chi exercise, which is in contrast to gradually decrease of respiratory neural output over the treadmill after the initial increase, indicating that breathing effort and respiratory frequency have been better controlled during Tai Chi than during treadmill exercise. Tai Chi places an emphasis on posture which entails prolonged contraction of the locomotor muscles which are often weak (Seymour et al., 2010) and atrophied (Seymour et al., 2012; Shrikrishna et al., 2012) in patients with COPD, who may have reduced short physical performance battery scores (Patel et al., 2014). Indeed, as can be seen in the video, the exercise even entails standing on one leg for periods. Isolated leg muscle training has been reported to be superior to high intensity whole body exercise training (Dolmage and Goldstein, 2008) and isolated high-intensity leg muscle training can restore aspects of quadriceps function, such as mitochondrial respiration, to the normal range (Bronstad et al., 2012). In this regard we note that Tai Chi seems likely to be an effective method of training the quadriceps (Wu et al., 2002; Tsang and Hui-Chan 2005; Wu, 2008) because this modality, but not constant rate treadmill exercise, induced low frequency fatigue of the quadriceps as manifest by a fall in the unpotentiated twitch tension elicited by femoral nerve stimulation. Lastly Tai Chi entails breathing control; this is relevant since both Tai Chi and treadmill exercise induced dynamic hyperinflation. In this connection we note that although both exercise modalities produced similar increases in respiratory load as manifest by EMGdi and esophageal pressure, only Tai Chi produced a greater tidal volume and slower respiratory frequency in the recovery phase presumably because the breathing control practiced during Tai Chi to some extent had carried over into recovery. In conclusion Tai Chi produces a physiologic response similar to that elicited by constant rate treadmill at 60% of maximal load and therefore deserves evaluation as an exercise modality for patients with COPD, particularly for those with limited access to PR facilities. Conflict of interest The authors declare that there are no conflicts of interest. Acknowledgments This project was mainly funded by National Natural Science Foundation of China (Grant # 81270143). Professor Polkey’s contribution to this project was supported by the NIHR Respiratory Biomedical Research Unit at the Royal Brompton and Harefield NHS Foundation Trust and Imperial College, London UK, who part fund his salary. Dr Lu’s contribution to this project was supported by Department of Science and Technology of Jiangsu Province, Jiangsu, China (Grant # BL2012065). All authors contributed to study design, data acquisition and manuscript writing. Zhi-Hui Qiu, Hong-Xi Guo and Gan Lu contributed equally to the work. References British Thoracic Society Standards of Care Subcommittee on Pulmonary, R., 2001. Pulmonary rehabilitation. Thorax 56 (11), 827–834. Bronstad, E., Rognmo, O., Tjonna, A.E., Dedichen, H.H., Kirkeby-Garstad, I., Haberg, A.K., Bjork Ingul, C., Wisloff, U., Steinshamn, S., 2012. High-intensity knee
extensor training restores skeletal muscle function in COPD patients. Eur. Respir. J. 40 (5), 1130–1136. Casaburi, R., Patessio, A., Ioli, F., Zanaboni, S., Donner, C.F., Wasserman, K., 1991. Reductions in exercise lactic acidosis and ventilation as a result of exercise training in patients with obstructive lung disease. Am. Rev. Respir. Dis. 143 (1), 9–18. Chang, J.Y., Tsai, P.F., Beck, C., Hagen, J.L., Huff, D.C., Anand, K.J., Roberson, P.K., Rosengren, K.S., Beuscher, L., 2011. The effect of tai chi on cognition in elders with cognitive impairment. Medsurg Nurs. 20 (2), 63–69, quiz 70. Chyu, M.C., James, C.R., Sawyer, S.F., Brismee, J.M., Xu, K.T., Poklikuha, G., Dunn, D.M., Shen, C.L., 2010. Effects of tai chi exercise on posturography, gait, physical function and quality of life in postmenopausal women with osteopaenia: a randomized clinical study. Clin. Rehabil. 24 (12), 1080–1090. Dolmage, T.E., Goldstein, R.S., 2008. Effects of one-legged exercise training of patients with COPD. Chest 133 (2), 370–376. Griffiths, T.L., Burr, M.L., Campbell, I.A., Lewis-Jenkins, V., Mullins, J., Shiels, K., Turner-Lawlor, P.J., Payne, N., Newcombe, R.G., Ionescu, A.A., Thomas, J., Tunbridge, J., 2000. Results at 1 year of outpatient multidisciplinary pulmonary rehabilitation: a randomised controlled trial. Lancet 355 (9201), 362–368. Guenette, J.A., Webb, K.A., O’Donnell, D.E., 2012. Does dynamic hyperinflation contribute to dyspnoea during exercise in patients with COPD? Eur. Respir. J. 40 (2), 322–329. Hamnegard, C.H., Sedler, M., Polkey, M.I., Bake, B., 2004. Quadriceps strength assessed by magnetic stimulation of the femoral nerve in normal subjects. Clin. Physiol. Funct. Imaging 24 (5), 276–280. Jensen, D., O’Donnell, D.E., Li, R., Luo, Y.M., 2011. Effects of dead space loading on neuro-muscular and neuro-ventilatory coupling of the respiratory system during exercise in healthy adults: implications for dyspnea and exercise tolerance. Respir. Physiol. Neurobiol. 179 (2-3), 219–226. Keating, A., Lee, A., Holland, A.E., 2011. What prevents people with chronic obstructive pulmonary disease from attending pulmonary rehabilitation? A systematic review. Chron. Respir. Dis. 8 (2), 89–99. Leung, R.W., McKeough, Z.J., Peters, M.J., Alison, J.A., 2013. Short-form sun-style tai chi as an exercise training modality in people with COPD. Eur. Respir. J. 41 (5), 1051–1057. Li, F., Harmer, P., Fitzgerald, K., Eckstrom, E., Stock, R., Galver, J., Maddalozzo, G., Batya, S.S., 2012. Tai chi and postural stability in patients with Parkinson’s disease. N Engl J Med 366 (6), 511–519. Luo, Y.M., Tang, J., Jolley, C., Steier, J., Zhong, N.S., Moxham, J., Polkey, M.I., 2009. Distinguishing obstructive from central sleep apnea events: diaphragm electromyogram and esophageal pressure compared. Chest 135 (5), 1133–1141. Mador, M.J., Kufel, T.J., Pineda, L.A., Steinwald, A., Aggarwal, A., Upadhyay, A.M., Khan, M.A., 2001. Effect of pulmonary rehabilitation on quadriceps fatiguability during exercise. Am. J. Respir. Crit. Care Med. 163 (4), 930–935. O’Shea, S.D., Taylor, N.F., Paratz, J.D., 2007. A predominantly home-based progressive resistance exercise program increases knee extensor strength in the short-term in people with chronic obstructive pulmonary disease: a randomised controlled trial. Aust. J. Physiother. 53 (4), 229–237. Patel, M.S., Mohan, D., Andersson, Y.M., Baz, M., Kon, S.S., Canavan, J.L., Jackson, S.G., Clark, A.L., Hopkinson, N.S., Natanek, S.A., Kemp, P.R., Bruijnzeel, P.L., Man, W.D., Polkey, M.I., 2014. Phenotypic characteristics associated with reduced short physical performance battery score in COPD. Chest 145 (5), 1016–1024. Polkey, M.I., Kyroussis, D., Hamnegard, C.H., Mills, G.H., Green, M., Moxham, J., 1996. Quadriceps strength and fatigue assessed by magnetic stimulation of the femoral nerve in man. Muscle Nerve 19 (5), 549–555. Seymour, J.M., Spruit, M.A., Hopkinson, N.S., Natanek, S.A., Man, W.D., Jackson, A., Gosker, H.R., Schols, A.M., Moxham, J., Polkey, M.I., Wouters, E.F., 2010. The prevalence of quadriceps weakness in COPD and the relationship with disease severity. Eur. Respir. J. 36 (1), 81–88. Seymour, J.M., Ward, K., Raffique, A., Steier, J.S., Sidhu, P.S., Polkey, M.I., Moxham, J., Rafferty, G.F., 2012. Quadriceps and ankle dorsiflexor strength in chronic obstructive pulmonary disease. Muscle Nerve 46 (4), 548–554. Shrikrishna, D., Patel, M., Tanner, R.J., Seymour, J.M., Connolly, B.A., Puthucheary, Z.A., Walsh, S.L., Bloch, S.A., Sidhu, P.S., Hart, N., Kemp, P.R., Moxham, J., Polkey, M.I., Hopkinson, N.S., 2012. Quadriceps wasting and physical inactivity in patients with COPD. Eur. Respir. J. 40 (5), 1115–1122. Troosters, T., Casaburi, R., Gosselink, R., Decramer, M., 2005. Pulmonary rehabilitation in chronic obstructive pulmonary disease. Am. J. Respir. Crit. Care Med. 172 (1), 19–38. Tsang, W.W., Hui-Chan, C.W., 2005. Comparison of muscle torque, balance, and confidence in older tai chi and healthy adults. Med. Sci. Sports Exerc. 37 (2), 280–289. Wang, C., Schmid, C.H., Rones, R., Kalish, R., Yinh, J., Goldenberg, D.L., Lee, Y., McAlindon, T., 2010. A randomized trial of tai chi for fibromyalgia. N. Engl. J. Med. 363 (8), 743–754. Wu, G., 2008. Muscle action pattern and knee extensor strength of older Tai Chi exercisers. Med. Sport Sci. 52, 30–39. Wu, G., Zhao, F., Zhou, X., Wei, L., 2002. Improvement of isokinetic knee extensor strength and reduction of postural sway in the elderly from long-term Tai Chi exercise. Arch. Phys. Med. Rehabil. 83 (10), 1364–1369.
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Physiological responses to Tai Chi in stable patients with COPD Zhi-Hui Qiu a , Hong-Xi Guo a , Gan Lu b , Ning Zhang a , Bai-Ting He a , Lian Zhou a , Y.M. Luo a,∗ , M.I. Polkey c a b c
State Key Laboratory of Respiratory Disease, Guangzhou Medical University, 151 Yanjiang Road, Guangzhou, China Jiangsu Province Official Hospital, Nanjing 210024, China NIHR Respiratory Biomedical Research Unit at the Royal Brompton and Harefield NHS Foundation Trust and Imperial College, London, UK
a r t i c l e
i n f o
Article history: Received 1 July 2015 Received in revised form 29 October 2015 Accepted 30 October 2015 Available online 11 November 2015 Keyword: COPD Exercise Pulmonary rehabilitation
a b s t r a c t We compared the physiological work, judged by oxygen uptake, esophageal pressure swing and diaphragm electromyography, elicited by Tai Chi compared with that elicited by constant rate treadmill walking at 60% of maximal load in eleven patients with COPD (Mean FEV1 61% predicted, FEV1 /FVC 47%). Dynamic hyperinflation was assessed by inspiratory capacity and twitch quadriceps tension (TwQ) elicited by supramaximal magnetic stimulation of the femoral nerve was also measured before and after both exercises. The EMGdi and esophageal pressure at the end of exercise were similar for both treadmill exercise and Tai Chi (0.109 ± 0.047 mV vs 0.118 ± 0.061 mV for EMGdi and 22.3 ± 7.1 cmH2 O vs 21.9 ± 8.1 cmH2 O for esophageal pressure). Moreover the mean values of oxygen uptake during Tai Chi and treadmill exercise did not differ significantly: 11.3 ml/kg/min (51.1% of maximal oxygen uptake derived from incremental exercise) and 13.4 ml/kg/min (52.5%) respectively, p > 0.05. Respiratory rate during Tai Chi was significantly lower than that during treadmill exercise. Both Tai Chi and treadmill exercise elicited a fall in IC at end exercise, indicating dynamic hyperinflation, but this was statistically significant only after treadmill exercise. TwQ decreased significantly after Tai Chi but not after treadmill. We conclude that Tai Chi constitutes a physiologically similar stimulus to treadmill exercise and may therefore be an acceptable modality for pulmonary rehabilitation which may be culturally more acceptable in some parts of the world. © 2015 Elsevier B.V. All rights reserved.
1. Introduction Pulmonary rehabilitation (PR) is a therapy of proven efficacy in Chronic Obstructive Pulmonary Disease (COPD) (Griffiths et al., 2000), but classical PR entails the provision of centralized facilities with dedicated exercise equipment and staff. This can limit uptake of this therapy both because it confers a finite limit to the number of patients that can be treated at any one time, and because patients may find travelling to a central facility a deterrent (O’Shea et al., 2007; Keating et al., 2011). Secondly, where PR can only be given for fixed periods a detarining effect occurs so that both exercise capacity and quality of life usually decline gradually after completion of PR (Griffiths et al., 2000).
∗ Corresponding author at: Professor of Respiratory Medicine, State Key Laboratory of Respiratory Disease, 151 Yanjiang Road, Guangzhou 510120, China. Fax: +86 20 34284122. E-mail address: [email protected] (Y.M. Luo). http://dx.doi.org/10.1016/j.resp.2015.10.019 1569-9048/© 2015 Elsevier B.V. All rights reserved.
Tai Chi is a traditional form of exercise developed in China, originally as a martial art for combat purposes. Tai Chi consists of a series of slow but continuous movements of many parts of the body. There is experimental evidence from both cross-sectional and longitudinal studies that Tai Chi exercise has beneficial effects on cardiovascular fitness (Chang et al., 2011), balance control and psychological well-being (Chyu et al., 2010). Since the movements can be adapted to suit people with physical weaknesses or disabilities, Tai Chi has become increasingly popular among elderly people in Hong Kong, mainland China, and other parts of the world (Wang et al., 2010; Li et al., 2012; Leung et al, 2013). Tai Chi could therefore potentially replace western style PR with the advantages both that class sizes are not limited by the quantity of specialized exercise equipment and that the patient may continue the exercise at home after the end of formal training. However, whilst the clinical studies noted above support the value of Tai Chi, some physiologic questions remain unanswered. First, no study has assessed respiratory mechanics during Tai Chi probably because of the difficulty recording esophageal pressure and EMGdi during free movement. Consequently, it is unknown what level
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of respiratory load is elicited by this therapy. In particular, since Tai Chi requires control of breathing during exercise we hypothesized that this may reduce breathing frequency and thus confer a beneficial effect on dynamic hyperinflation compared with treadmill exercise. Secondly it is unknown whether Tai Chi is sufficient to elicit low frequency quadriceps fatigue, which would indicate that the exercise is sufficiently intense to produce a training effect (Mador et al., 2001). To address these questions we undertook a detailed physiological comparison of 24-form Yang style Tai Chi, the most widely practiced style today, and constant rate treadmill walking.
2. Methods Eleven patients with COPD (age 62 ± 8 years, FEV1 61 ± 27 % of predicted) were recruited from community. All patients had practiced Tai Chi for more than one year and were free of clinically significant coexistent diseases (e.g., cardiac disease, neuromuscular disorders or severe arthritis) that might preclude exercise and had not had an exacerbation of COPD within the preceding month. Patients with cancer or severe obesity were also excluded. The study was approved by the Ethical committee of the first affiliated hospital of Guangzhou Medical University. All participants provided written informed consent to participate.
2.1. Protocol Each patient visited the laboratory four times with a two-dayinterval between visits. At visit 1 patients received a physical examination and we measured spirometry. At visit 2 an incremental treadmill exercise to determine each individual’s maximal load was performed. The incremental treadmill exercise protocol consisted of 3 min standing still followed by an increase in the load every three minutes by increasing 0.5 km/h until intolerable dyspnea or exhaustion occurred; dyspnea was not quantified during the incremental test using a Borg or similar score, but patients were encouraged to continue until the limit of tolerability. Visits 3 and 4 were for the physiologic study of either Tai Chi or constant rate treadmill walking at 60% of maximal load determined at visit 2. Constant load exercise and Tai Chi which consisted of 10 repeated sections with 6 min duration for each section were performed in random order. Participants were asked to exercise on a treadmill for 60 min to match the duration of Tai Chi which is usually last 60 min. A five minute warm up was allowed before Tai Chi. A video of one of the participants undertaking Tai Chi may be viewed at online supplement (http://183.63.72.215:88/play/index. html).
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2.2. Measurements The same measurements were made before, during and after both Tai Chi and constant rate exercise as follows. A long (5 m) lead suspended from a pulley that was free to move at the level of the laboratory ceiling was used to permit recording of EMGdi and esophageal pressure during Tai Chi exercise without limiting the participants movement (Please see online video). Inspiratory capacity (IC) was performed before and immediately after exercise to quantify dynamic hyperinflation (Guenette et al., 2012). Oxygen uptake (VO2 ), carbon dioxide production (VCO2 ), minute ventilation (VE ), respiratory rate, heart rate and SpO2 were continually measured with a facemask and finger probe connected to a portable metabolic ‘cart’ worn by patient (K4b2 , COSMED,Italy) during exercise. Respiratory rate and VO2 during exercise were considered the average of 3 min before the end of exercise and compared with 3 min during rest. Since Tai Chi requires breathing control we did not feel it appropriate to perform interval measures of IC or to ask participants to vocalise to record Borg dyspnea or leg scores, and therefore did not undertake these during treadmill exercise either. Diaphragm electromyography (EMGdi) was recorded using a combined multipair esophageal electrode catheter with an esophageal balloon mounted on it passed pernasally, as previously described(Luo et al., 2009; Jensen et al., 2011). The EMG signals were bandpass filtered between 20 and 1000 Hz and amplified (Bioamplifier Model RA-8, Yinghui Guangzhou, China). The esophageal balloon was filled with 0.5 ml air and connected to a pressure transducer (DP15, Validyne Corp., Northrige, CA, USA). Quadriceps fatigue was evaluated by measuring the unpotentiated quadriceps twitch tension (TwQ) using the similar technique previously described (Polkey et al., 1996; Hamnegard et al., 2004). The participants were studied supine with the knee flexed at 90◦ over the end of the chair. An inextensible strap was placed around the ankle and connected to a strain gauge (strain stall range 0–100 kg) mounted to the back of the chair so that the strap ran perpendicular to the ankle and gauge. A 43-mm figure-of-eight coil powered by a Magstim 200 stimulator (Magstim Company Limited, Whitland, Dyfed, Wales) was used to stimulate the right femoral nerve; a minimum of 5 stimulations at 100% of stimulator output were given and the mean TwQ used for analysis. The unpotentiated TwQ was measured before, 20 min and 60 min after both constant load treadmill and Tai Chi exercise.
2.3. Statistical analysis Data were presented as mean ± SD. A two way repeated measures ANOVA and a paired t-test were used to assess the differences between Tai Chi and treadmill exercise.
Table 1 characteristic of patients with COPD. Subject no.
Sex
1 2 3 4 5 6 7 8 9 10 11 Mean SD
M M M M M M F M M M M ¡¡ ¡¡
Age (years) 62 63 63 57 66 71 54 67 46 72 57 62 8
Weight (kg) 64.0 67.0 83.6 67.5 65.0 71.0 59.0 57.0 76.0 56.0 56.0 65.6 8.8
Height (cm)
162 165 170 169 163 161 157 165 168 163 159 164 4
BMI (kg/m2 )
FEV1 (litre)
24.4 24.6 28.9 23.6 24.5 27.4 23.9 20.9 26.9 21.1 22.2 24.4 2.5
2.88 2.24 1.54 1.31 1.10 1.52 1.45 0.59 2.02 2.36 0.76 1.62 0.70
FEV1 (% pred) 108 85 54 44 44 67 66 22 60 97 28 61 27
VC (litre)
FEV1 /VC (%)
IRV (litre)
IC (litre)
Smoking (years)
4.80 3.82 3.76 3.25 2.31 2.78 2.70 2.72 3.90 3.73 3.33 3.37 0.72
60.0 58.6 41.0 40.3 47.6 54.7 53.7 21.7 51.8 63.3 22.8 46.9 14.2
3.12 1.46 1.19 1.52 0.84 1.48 1.01 0.57 1.17 0.53 0.56 1.22 0.73
3.62 2.24 2.82 1.56 1.81 2.01 2.41 1.40 2.47 2.34 1.61 2.21 0.64
30 40 40 30 10 30 0 40 30 30 30 28 13
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Fig. 1. EMGdi recorded from five pairs of electrode and esophageal pressure during rest, beginning, middle and end of Tai Chi exercise and treadmill exercise.
3. Results 3.1. Tai Chi and constant rate treadmill exercise compared Eleven stable patients with GOLD I to IV COPD (10 men and 1 women) were studied; demographic data are shown in Table 1. Good quality EMGdi signals were recorded during both treadmill exercise and Tai Chi (Fig. 1). Borg breathlessness and leg scores were 5.3 ± 1.3 and 4.9 ± 1.2 at the end of treadmill exercise and 5.5 ± 1.4 and 4.9 ± 1.2 after Tai Chi, respectively (p > 0.05). Mean values of oxygen uptake during Tai Chi and treadmill exercise were similar and were 11.28 ml/kg/min (51.1% of maximal VO2 ) and 13.41 ml/kg/min (52.5% of maximal VO2 ) respectively, p > 0.05. An example of breath by breath VO2 over the one hour recording period are shown for Tai Chi and constant rate treadmill exercise (Fig. 2). It is evident that due to the cyclical nature of Tai Chi these parameters fluctuate but remain relatively constant during treadmill walking. Two participants during Tai Chi and three participants during treadmill could not exercise for 60 min (Table 2). Data obtained during the hour of exercise are shown in Table 3, with esophageal pressure (Pes ) and EMGdi in Fig. 3. Both EMGdi and esophageal pressure decreased slightly during treadmill while they were stable during Tai Chi. However, the EMGdi and esophageal pressure at the end of exercise are almost the same between treadmill exercise and Tai Chi (0.109 ± 0.047 mV vs 0.118 ± 0.061 mV for EMGdi and 22.3 ± 7.1 cmH2 O vs 21.9 ± 8.1 cmH2 O for Pes ). For most physiological responses entailed by Tai Chi did not differ from treadmill walking at 60% VO2max (Fig. 4). Significant differences were observed after exercise in tidal volume which was higher at the end of exercise after Tai Chi (1.2 ± 0.5 l) than after treadmill walking (1.0 ± 0.3 l) while respiratory frequency at the end of treadmill exercise (30 ± 6 breaths/min) was higher than that at the end of Tai Chi (25 ± 4 breaths/min) although oxygen uptake was not significantly different between Tai Chi and treadmill exercise (0.81 ± 0.28 l/min vs 0.70 ± 0.16 l/min) (Table 2). As expected both Tai Chi and treadmill exercise elicited a fall in IC from 2.20 ± 0.71 l to 2.01 ± 0.79 l (p = 0.065) for Tai Chi and 2.26 ± 0.68–1.92 ± 0.67 l
Fig. 2. Oxygen uptake over a 1 h period in which the subject either did Tai Chi (upper panel) and on another occasion walking at 60% of VO2max . In the Tai Chi panel the periodicity of 10 six minutes cycles is evident.
Fig. 3. Oxygen uptake, EMGdi and Pes during Tai Chi and treadmill exercise; mean data from all participants.
(p < 0.01) for treadmill exercise, but this was statistically significant only after treadmill exercise. 3.2. Exercise tasks and quadriceps fatigue TwQ data are shown in Table 4. TwQ decreased significantly at 20 min and 60 min after Tai Chi but there was no difference between before and after constant treadmill exercise at 60% of maximal load. 4. Discussion This is the first study to record the EMGdi and esophageal pressure during Tai Chi which requires free movement. The main finding of the current study is that Tai Chi exercise is similar to treadmill exercise at 60% of maximal load in terms of the elicited EMGdi and esophageal pressure. Respiratory rate during Tai Chi was less than that during treadmill and dynamic hyperinflation as judged by IC is also less severe after Tai Chi than after treadmill at 60% of maximal work rate. Tai Chi induced low frequency
Fig. 4. Relation between ventilation and oxygen uptake (A), oxygen saturation and oxygen uptake (B), carbon dioxide production (Vco2 ) and oxygen uptake (C), heart rate and oxygen uptake (D) and the relation between EMGdi and ventilation (E), Pes and ventilation (F), tidal volume and ventilation (G), respiratory frequency (RF) and ventilation (H) during Tai Chi and treadmill exercise. Values presented are the mean of all participants at epochs of 10% total exercise time (6 min unless patient failed to complete 1 h task).
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Table 2 Respiratory frequency and oxygen uptake during treadmill and Tai Chi exercises.
Subject no.
Respiratory frequency (breaths/min)
VO2 (l/min)
Tai Chi
Tai Chi
Treadmill
Rest 1 2 3 4 5 6 7 8 9 10 11 Mean SD
End
21 21 23 21 23 18 15 34 17 25 19 21 5
22 24 26 25 27 24 27 37 20 22 26 25 4
Rest
End
25 18 24 19 24 20 14 23 16 22 20 21 3
23 32 35 29 27 39 24 40 21 28 29 30 6
Exercise duration Treadmill
Tai Chi
Treadmill
Rest
End
Rest
End
(min)
(min)
0.51 0.50 0.30 0.31 0.55 0.49 0.20 0.22 0.26 0.37 0.29 0.36 0.13
1.27 0.74 0.97 0.36 1.17 0.60 0.75 0.54 1.04 0.74 0.71 0.81 0.28
0.37 0.32 0.49 0.30 0.34 0.31 0.18 0.30 0.34 0.23 0.25 0.31 0.08
0.98 0.75 0.97 0.53 0.78 0.60 0.68 0.51 0.69 0.55 0.65 0.70 0.16
60 60 60 44 60 60 60 25 60 60 60 55 11
60 60 60 28 60 35 60 12 60 60 60 50 17
Table 3 Cardiopulomonary data including esophageal pressure (Pes) and EMGdi during Tai Chi and treadmill exercise. Parameter
Tai Chi exercise
RF(b/m) VT(L) VE(L/m) VO2 (L/m) VCO2 (L/m) HR(bpm) SpO2 (%) EMGdi (V) Pes (cmH2 O)
Treadmill exercise
Rest
Mean
End
Rest
Mean
End
21.5 (5.1) 0.8 (0.2) 15.7 (3.7) 0.36 (0.13) 0.36 (0.09) 80 (12) 96 (1) 58.3 (28.6) 12.8 (6.7)
*
*
20.7 (3.5) 0.7 (0.1) 14.2 (2.9) 0.31 (0.08) 0.31 (0.06) 78 (11) 96 (1) 54 (19) 12.2 (4.2)
28.7 (4.6) 1.1 (0.3) 32.9 (11.5) 0.88 (0.30) 0.90 (0.28) 111 (13) 93 (4) 119 (56) 23.8 (7.0)
29.8 (6.2) 1.0 (0.3) 27.3 (6.5) 0.70 (0.16) 0.71 (0.16) 112 (13) 94 (5) 109 (47) 22.3 (7.1)
24.7 (2.4) 1.1 (0.3) 27.4 (5.7) 0.74 (0.22) * 0.74 (0.17) 104 (21) 95 (4) 113 (57) 21.4 (7.7)
25.5 (4.5) ** 1.2 (0.5) 30.0 (8.2) 0.81 (0.28) * 0.81 (0.25) 110 (22) 94 (5) 118 (61) 21.9 (8.1)
RF, respiratory frequency; HR, heart rate; bpm, beats per minute; mean, mean of 60 min; end, mean value of the last three minutes. * p < 0.05 between Tai Chi and treadmill. ** p < 0.01. Table 4 Quadriceps twitch force (kg) measured by magnetic stimulation before and 20 min and 60 min after exercise. Subject no.
1 2 3 4 5 6 7 8 9 10 11 Mean SD
Tai Chi
Treadmill
Before
20 min
60 min
Before
20 min
60 min
8.3 7.3 7.5 9.4 9.4 7.4 10.2 11.9 5.8 7.8 11.0 8.7 1.8
6.5 7.6 6.5 9.1 8.1 6.8 8.4 11.3 3.7 6.4 9.6 7.6 2.0
7.0 7.2 6.7 8.4 8.2 6.9 8.7 11.8 4.6 6.6 9.9 7.8 1.9
7.7 7.1 8.0 8.3 7.4 7.0 9.8 11.3 4.8 7.2 10.2 8.1 1.8
7.9 11.0 6.9 7.4 7.3 7.1 10.6 10.9 4.9 7.9 11.1 8.5 2.1
7.7 9.7 6.4 8.1 7.4 7.1 10.2 10.7 4.8 6.9 10.9 8.2 2.0
quadriceps fatigue, suggesting that Tai Chi may constitute an adequate exercise load to be an effective form of PR in patients with COPD.
4.1. Critique of the method This is a physiological study performed on a small number of participants with a range of disease severity. While the purpose of the study was to further evaluate the potential suitability of Tai Chi as a form of rehabilitation, the present data themselves cannot be interpreted as an evidence base for Tai chi as a form of PR.
4.2. Significance of the findings Since the seminal work of Casaburi et al. (1991) over 20 years ago it has been accepted that greater training benefits are realized if higher training intensities are used. Current recommendations are that intensities greater than 60% of maximal load are prescribed for COPD patients undertaking physical training (Troosters et al., 2005), although the exercise prescription may be obtained from a field test of exercise performance such as the incremental shuttle walk test (British Thoracic Society Standards of Care Subcommittee on Pulmonary, 2001). The principal finding of the current study is that the mean oxygen uptake observed during Tai Chi did not differ from that obtained during treadmill exercise at 60% of maximal load. Interestingly however the respiratory pattern adopted differed between the exercise modality so that Tai Chi was characterized by less increase in respiratory rate and a greater increase in tidal volume. As a consequence of this walking, Tai Chi was less associated with dynamic hyperinflation. Our data thus suggest that Tai Chi produces a sufficiently vigorous exercise to constitute a training modality. These data are consistent with those of Leung et al., (2013) but add to it both because in their study VO2max was inferred from a field exercise test rather than measured directly as was the case in this study, as well as the other physiologic data gathered in the present study. Tai Chi may be regarded as a composite form of exercise. As can be seen from the video link (see methods) key features of the technique in comparison to constant rate exercise are the fluctuating level of exercise intensity, the focus on posture and on breathing control. By its nature Tai Chi is cyclical whereas treadmill exercise is not; it may therefore be considered that Tai Chi is more analogous to interval training in some respects. The
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principle of interval training is that, by taking breaks, the patient may be able to reach a higher training intensity for short periods and thus provide a greater training stimulus. However, despite the cyclical nature of Tai Chi, respiratory neural output as assessed by EMGdi or esophageal pressure is overall remarkably constant (Fig. 3) during Tai Chi exercise, which is in contrast to gradually decrease of respiratory neural output over the treadmill after the initial increase, indicating that breathing effort and respiratory frequency have been better controlled during Tai Chi than during treadmill exercise. Tai Chi places an emphasis on posture which entails prolonged contraction of the locomotor muscles which are often weak (Seymour et al., 2010) and atrophied (Seymour et al., 2012; Shrikrishna et al., 2012) in patients with COPD, who may have reduced short physical performance battery scores (Patel et al., 2014). Indeed, as can be seen in the video, the exercise even entails standing on one leg for periods. Isolated leg muscle training has been reported to be superior to high intensity whole body exercise training (Dolmage and Goldstein, 2008) and isolated high-intensity leg muscle training can restore aspects of quadriceps function, such as mitochondrial respiration, to the normal range (Bronstad et al., 2012). In this regard we note that Tai Chi seems likely to be an effective method of training the quadriceps (Wu et al., 2002; Tsang and Hui-Chan 2005; Wu, 2008) because this modality, but not constant rate treadmill exercise, induced low frequency fatigue of the quadriceps as manifest by a fall in the unpotentiated twitch tension elicited by femoral nerve stimulation. Lastly Tai Chi entails breathing control; this is relevant since both Tai Chi and treadmill exercise induced dynamic hyperinflation. In this connection we note that although both exercise modalities produced similar increases in respiratory load as manifest by EMGdi and esophageal pressure, only Tai Chi produced a greater tidal volume and slower respiratory frequency in the recovery phase presumably because the breathing control practiced during Tai Chi to some extent had carried over into recovery. In conclusion Tai Chi produces a physiologic response similar to that elicited by constant rate treadmill at 60% of maximal load and therefore deserves evaluation as an exercise modality for patients with COPD, particularly for those with limited access to PR facilities. Conflict of interest The authors declare that there are no conflicts of interest. Acknowledgments This project was mainly funded by National Natural Science Foundation of China (Grant # 81270143). Professor Polkey’s contribution to this project was supported by the NIHR Respiratory Biomedical Research Unit at the Royal Brompton and Harefield NHS Foundation Trust and Imperial College, London UK, who part fund his salary. Dr Lu’s contribution to this project was supported by Department of Science and Technology of Jiangsu Province, Jiangsu, China (Grant # BL2012065). All authors contributed to study design, data acquisition and manuscript writing. Zhi-Hui Qiu, Hong-Xi Guo and Gan Lu contributed equally to the work. References British Thoracic Society Standards of Care Subcommittee on Pulmonary, R., 2001. Pulmonary rehabilitation. Thorax 56 (11), 827–834. Bronstad, E., Rognmo, O., Tjonna, A.E., Dedichen, H.H., Kirkeby-Garstad, I., Haberg, A.K., Bjork Ingul, C., Wisloff, U., Steinshamn, S., 2012. High-intensity knee
extensor training restores skeletal muscle function in COPD patients. Eur. Respir. J. 40 (5), 1130–1136. Casaburi, R., Patessio, A., Ioli, F., Zanaboni, S., Donner, C.F., Wasserman, K., 1991. Reductions in exercise lactic acidosis and ventilation as a result of exercise training in patients with obstructive lung disease. Am. Rev. Respir. Dis. 143 (1), 9–18. Chang, J.Y., Tsai, P.F., Beck, C., Hagen, J.L., Huff, D.C., Anand, K.J., Roberson, P.K., Rosengren, K.S., Beuscher, L., 2011. The effect of tai chi on cognition in elders with cognitive impairment. Medsurg Nurs. 20 (2), 63–69, quiz 70. Chyu, M.C., James, C.R., Sawyer, S.F., Brismee, J.M., Xu, K.T., Poklikuha, G., Dunn, D.M., Shen, C.L., 2010. Effects of tai chi exercise on posturography, gait, physical function and quality of life in postmenopausal women with osteopaenia: a randomized clinical study. Clin. Rehabil. 24 (12), 1080–1090. Dolmage, T.E., Goldstein, R.S., 2008. Effects of one-legged exercise training of patients with COPD. Chest 133 (2), 370–376. Griffiths, T.L., Burr, M.L., Campbell, I.A., Lewis-Jenkins, V., Mullins, J., Shiels, K., Turner-Lawlor, P.J., Payne, N., Newcombe, R.G., Ionescu, A.A., Thomas, J., Tunbridge, J., 2000. Results at 1 year of outpatient multidisciplinary pulmonary rehabilitation: a randomised controlled trial. Lancet 355 (9201), 362–368. Guenette, J.A., Webb, K.A., O’Donnell, D.E., 2012. Does dynamic hyperinflation contribute to dyspnoea during exercise in patients with COPD? Eur. Respir. J. 40 (2), 322–329. Hamnegard, C.H., Sedler, M., Polkey, M.I., Bake, B., 2004. Quadriceps strength assessed by magnetic stimulation of the femoral nerve in normal subjects. Clin. Physiol. Funct. Imaging 24 (5), 276–280. Jensen, D., O’Donnell, D.E., Li, R., Luo, Y.M., 2011. Effects of dead space loading on neuro-muscular and neuro-ventilatory coupling of the respiratory system during exercise in healthy adults: implications for dyspnea and exercise tolerance. Respir. Physiol. Neurobiol. 179 (2-3), 219–226. Keating, A., Lee, A., Holland, A.E., 2011. What prevents people with chronic obstructive pulmonary disease from attending pulmonary rehabilitation? A systematic review. Chron. Respir. Dis. 8 (2), 89–99. Leung, R.W., McKeough, Z.J., Peters, M.J., Alison, J.A., 2013. Short-form sun-style tai chi as an exercise training modality in people with COPD. Eur. Respir. J. 41 (5), 1051–1057. Li, F., Harmer, P., Fitzgerald, K., Eckstrom, E., Stock, R., Galver, J., Maddalozzo, G., Batya, S.S., 2012. Tai chi and postural stability in patients with Parkinson’s disease. N Engl J Med 366 (6), 511–519. Luo, Y.M., Tang, J., Jolley, C., Steier, J., Zhong, N.S., Moxham, J., Polkey, M.I., 2009. Distinguishing obstructive from central sleep apnea events: diaphragm electromyogram and esophageal pressure compared. Chest 135 (5), 1133–1141. Mador, M.J., Kufel, T.J., Pineda, L.A., Steinwald, A., Aggarwal, A., Upadhyay, A.M., Khan, M.A., 2001. Effect of pulmonary rehabilitation on quadriceps fatiguability during exercise. Am. J. Respir. Crit. Care Med. 163 (4), 930–935. O’Shea, S.D., Taylor, N.F., Paratz, J.D., 2007. A predominantly home-based progressive resistance exercise program increases knee extensor strength in the short-term in people with chronic obstructive pulmonary disease: a randomised controlled trial. Aust. J. Physiother. 53 (4), 229–237. Patel, M.S., Mohan, D., Andersson, Y.M., Baz, M., Kon, S.S., Canavan, J.L., Jackson, S.G., Clark, A.L., Hopkinson, N.S., Natanek, S.A., Kemp, P.R., Bruijnzeel, P.L., Man, W.D., Polkey, M.I., 2014. Phenotypic characteristics associated with reduced short physical performance battery score in COPD. Chest 145 (5), 1016–1024. Polkey, M.I., Kyroussis, D., Hamnegard, C.H., Mills, G.H., Green, M., Moxham, J., 1996. Quadriceps strength and fatigue assessed by magnetic stimulation of the femoral nerve in man. Muscle Nerve 19 (5), 549–555. Seymour, J.M., Spruit, M.A., Hopkinson, N.S., Natanek, S.A., Man, W.D., Jackson, A., Gosker, H.R., Schols, A.M., Moxham, J., Polkey, M.I., Wouters, E.F., 2010. The prevalence of quadriceps weakness in COPD and the relationship with disease severity. Eur. Respir. J. 36 (1), 81–88. Seymour, J.M., Ward, K., Raffique, A., Steier, J.S., Sidhu, P.S., Polkey, M.I., Moxham, J., Rafferty, G.F., 2012. Quadriceps and ankle dorsiflexor strength in chronic obstructive pulmonary disease. Muscle Nerve 46 (4), 548–554. Shrikrishna, D., Patel, M., Tanner, R.J., Seymour, J.M., Connolly, B.A., Puthucheary, Z.A., Walsh, S.L., Bloch, S.A., Sidhu, P.S., Hart, N., Kemp, P.R., Moxham, J., Polkey, M.I., Hopkinson, N.S., 2012. Quadriceps wasting and physical inactivity in patients with COPD. Eur. Respir. J. 40 (5), 1115–1122. Troosters, T., Casaburi, R., Gosselink, R., Decramer, M., 2005. Pulmonary rehabilitation in chronic obstructive pulmonary disease. Am. J. Respir. Crit. Care Med. 172 (1), 19–38. Tsang, W.W., Hui-Chan, C.W., 2005. Comparison of muscle torque, balance, and confidence in older tai chi and healthy adults. Med. Sci. Sports Exerc. 37 (2), 280–289. Wang, C., Schmid, C.H., Rones, R., Kalish, R., Yinh, J., Goldenberg, D.L., Lee, Y., McAlindon, T., 2010. A randomized trial of tai chi for fibromyalgia. N. Engl. J. Med. 363 (8), 743–754. Wu, G., 2008. Muscle action pattern and knee extensor strength of older Tai Chi exercisers. Med. Sport Sci. 52, 30–39. Wu, G., Zhao, F., Zhou, X., Wei, L., 2002. Improvement of isokinetic knee extensor strength and reduction of postural sway in the elderly from long-term Tai Chi exercise. Arch. Phys. Med. Rehabil. 83 (10), 1364–1369.