STRUCTURE AND FUNCTION of the human locomotor

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1 717 A Randomized, Prospective Study of the Effects of Tai Chi Chun Exercise on Bone Mineral Density in Postmenopausal Women Kaiming Chan, FRCS, Ling Qin, PhD, Mingchu Lau, MD, Jean Woo, MD, Szeki Au, MPhil, Wingyee Choy, BSc, Kwongman Lee, PhD, Shiuhung Lee, MD ABSTRACT. Chan K, Qin L, Lau M, Woo J, Au S, Choy W, Lee K, Lee S. A randomized, prospective study of the effects of Tai Chi Chun exercise on bone mineral density in postmenopausal women. Arch Phys Med Rehabil 2004;85: Objective: To evaluate the potential benefits of programmed Tai Chi Chun (TCC) exercise on the weight-bearing bones of early postmenopausal women. Design: Age-matched and randomized prospective intervention. Setting: University medical school. Participants: One hundred thirty-two healthy postmenopausal women (mean age, y) within 10 years of menopause onset were recruited and randomized into the TCC exercise group (n 67) or the sedentary control group (n 65). Intervention: Supervised TCC exercise was performed by the TCC group for 45 minutes a day, 5 days a week, for 12 months; control subjects retained a sedentary life style. Main Outcome Measures: Bone mineral density (BMD) was measured in the lumbar spine and proximal femur by using dual-energy x-ray absorptiometry and in the distal tibia by using multislice peripheral quantitative computed tomography (pqct). All BMD measurements were repeated after 12 months in both groups. Fracture rate was also documented. Results: Baseline measurements showed homogeneity in age, anthropometric variables, and menstruation status between the TCC and control groups. Exactly 81.6% of the subjects in the TCC group and 83.1% of subjects in the control group completed the 12-month follow-up study. BMD measurements revealed a general bone loss in both TCC and sedentary control subjects at all measured skeletal sites, but with a reportedly slower rate in the TCC group. A significant 2.6- to 3.6-fold retardation of bone loss (P.01) was found in both trabecular and cortical compartments of the distal tibia in the TCC group as compared with the controls, as measured by pqct. A total of 4 fracture cases were documented during follow-up, including 3 subjects in the control group and 1 in the TCC group. Conclusions: This is the first prospective and randomized study to show that a programmed TCC exercise intervention is From the Department of Orthopaedics and Traumatology (Chan, Qin, Au, Choy) and Community and Family Medicine (K Lee), Chinese University of Hong Kong (CUHK); CUHK-WHO Center of Sports Medicine and Health Promotion (Chan, Qin); and Hong Kong Jockey Club Center for Osteoporosis Care and Control (Qin, Lau, Woo, Au, S Lee), Hong Kong. Supported by Hong Kong Health Services Research Committee (grant no. 97/ ) and the Hong Kong Jockey Club Center for Osteoporosis Care and Control. No commercial party having a direct financial interest in the results of the research supporting this article has or will confer a benefit upon the authors(s) or upon any organization with which the author(s) is/are associated. Reprint requests to Ling Qin, PhD, Dept of Orthopaedics & Traumatology, Prince of Wales Hospital, Chinese University of Hong Kong, Hong Kong, Lingqin@chuk.edu.hk /04/ $30.00/0 doi: /j.apmr beneficial for retarding bone loss in weight-bearing bones in early postmenopausal women. Long-term follow-up is needed to substantiate the role of TCC exercise in the prevention of osteoporosis and its related fracture. Key Words: Bone density; Densitometry, x-ray; Exercise; Fractures; Osteoporosis, postmenopausal; Rehabilitation; Tai Chi; Tomography, x-ray computed by the American Congress of Rehabilitation Medicine and the American Academy of Physical Medicine and Rehabilitation STRUCTURE AND FUNCTION of the human locomotor system deteriorate with aging, leading to bone loss, reduction of muscle mass and strength, impaired mobility and neuromuscular coordination, and increased risk of falls. 1-8 Studies 8-14 of osteoporosis show that bone loss is a major health problem in postmenopausal women and fracture risks are associated with both low bone mineral density (BMD) and rate of bone loss. In women, bone loss starts after entering the fourth decade of life and accelerates after the onset of menopause. The level of BMD in one s later life is determined by both peak bone mass and subsequent rate of bone loss. 7,8,14,15 A preventative approach should already have been started to achieve maximum peak bone mass and to reduce subsequent bone loss, that is, before onset of menopause. It is still not clear whether the postmenopausal acceleration in bone loss is just an effect of estrogen deficiency and age itself or is associated with secondary factors such as malnutrition, vascular changes, or deterioration of locomotor system because of decreased physical activity. No matter what underlies the etiology of this bone loss, adequate exercises have a beneficial effects on the locomotor system, including prevention of osteoporosis, thereby reducing fracture risks in postmenopausal women. 5,16-25 Tai Chi Chun (TCC) is a low-impact, weight-bearing exercise regularly practiced by older people. Previous studies 5,16,21,24-33 have shown that TCC exercise is effective in maintaining the normal functioning of cardiorespiratory and immunoendocrine systems, in improving muscle strength, flexibility, and neuromuscular coordination, and thus in reducing fall-related fractures among older and elderly populations. TCC has also been recommended and adopted as a therapeutic means for treatment of degenerative diseases in the elderly. 5,16,29-33 Our recent small-scale case-control study 17 with a 12-month follow-up revealed that postmenopausal women who have been practicing TCC for more than 4 years revealed high baseline BMD as a result of retardation of bone loss at multiskeletal sites, including the spine and hip as measured by the dualenergy x-ray absorptiometry (DXA), coupled with an approximately 50% significant reduction in the rate of bone loss in both cortical and trabecular compartments of distal tibia as measured by a multislice and precise peripheral quantitative computed tomography (pqct).

2 718 TAI CHI EXERCISE RETARDS BONE LOSS IN WOMEN, Chan To substantiate the findings obtained from our earlier casecontrol study, this study was designed as a randomized and prospective intervention to explore the potential beneficial effects of a supervised TCC exercise on the prevention of early postmenopausal bone loss a fast bone loss phase of a woman s life by monitoring BMD changes in the weight-bearing bones at the spine and hip using DXA and the distal tibia using pqct. METHODS Participants Postmenopausal Chinese women, who ceased menstruation between 1 and 10 years prior to study enrollment and who had no history of regular participation in physical exercise, were recruited through local communities and newspaper advertisements. After completing a questionnaire on their health condition, diet, medical history, lifestyle, and menstrual status, 132 women were recruited into the study under the following inclusion criteria: (1) no regular participation in physical exercise (not 0.5h/wk); (2) no hormone replacement therapy or drug treatment known to affect bone metabolism or cause spontaneous bone loss; (3) no conditions such as hypo- or hyperparathyroidism and hypo- or hyperthyroidism, or renal or liver disease; (4) no history of fractures; and (5) a body mass index (BMI) above 30kg/m 2. Subjects were subsequently agematched and randomly divided into a TCC group (n 67) and a sedentary control group (n 65). All subjects gave their written consent before anthropometric and BMD measurements were made. The study protocol was approved by the Clinical Research Ethics Committee of the Chinese University of Hong Kong. A sample size of 45 for each group was estimated to achieve a statistical power of 0.8 after excluding a dropout rate of approximately 25% during 12-month follow-up. This calculation was based on an average annual bone loss in trabecular bone loss of 2.8% in normal nonexercising postmenopausal women of the same reference population reported in a previous follow-up study, 8 with an expectation of a 50% reduction in rate of bone loss after a 12-month period of exercise intervention. Baseline Measurements Anthropometric measurements. Body height and body weight were measured. BMI (in kg/m 2 ) was also calculated. BMD Measurement at Baseline DXA measurements. Areal BMD (in g/cm 2 ) measurements were made at the anteroposterior (AP) lumbar spine (L2-4) and nondominant proximal femur (neck and trochanter) by using DXA. a Quality control scans were performed daily with a manufacture-supplied anthropometric spine phantom, which gave a 1.2% long-term error rate in its repeated measurements. 12 pqct measurements. Volumetric BMD (in mg/cm 3 )of the nondominant distal tibia was measured by using a highly precise multislice pqct. b Phantom measurements were performed daily, with 3 measurement values within the given reference ranges provided by the manufacturer, that is, a total volume of 0.447% 0.323%; a core 50% volume of 0.287% 0.53%; and an area of 6.331% 0.409%. This gave an in vivo precision error of.32%, which was obtained from early postmenopausal women in our subjects. 7,8,17 A pqct scan was performed with the lower leg positioned in an individually selected radiolucent cast suitable for the subject. Details of the pqct measurement procedures and evaluations for distal tibia are described elsewhere. 17 After displaying an AP projection scout view, a reference line was set at right angles to the long axis of distal tibia, and then fixed on the midpoint of the distal tibial endplate. A standard scanning program of 16 tomograms was used. The distal 10 tomograms of the ultradistal tibia were used to obtain the average trabecular BMD (tbmd) in a core volume (central 50% of the total bone area) and the integral BMD (ibmd) within the total volume of the ultradistal tibia, whereas the 6 proximal tomograms obtained from distal tibial diaphysis were used to measure the pure cortical compartment as cortical tissue density (cbmd). Follow-Up Protocols TCC exercise. Subjects in the TCC group participated in a supervised TCC exercise (Yang style) for 50 minutes a day, 5 times a week, over 12 months, whereas control subjects retained their sedentary lifestyle without participation in physical exercises. There are several TCC styles practiced in the Asian culture, such as Chen, Wu or Sun, and Yong. Each style has its own unique features, although they share common kinematics with regard to musculoskeletal function. In general, TCC is a low-impact, weight-bearing exercise characterized by gentle movements designed to dissipate force throughout the body while the subject changes poses, with well-coordinated sequences of both isometric and isotonic segmental movements in the trunk and 4 extremities. 5,21,26,28,34 Yang TCC was selected for this study because this style emphasizes slow and smooth movement involving major muscle groups, at a constant speed while practicing. The sway of its moment is usually centered, which makes it more safe for the elderly to practice. 5,34 Attendance in the TCC exercise group was recorded and summarized at the end of a 12-month follow-up. Changes in BMD. Both DXA and pqct measurements were repeated after 12 months. The DXA follow-up measurement was carried out for calculating the changes of areal BMD by repeating the same measurement procedure as described earlier. Computer software, b designed for continuous pqct thin tomograms, evaluated the results of the baseline and follow-up measurements and their volumetric BMD changes within a common or the same scanned regions through an anatomic pattern recognition program, as described by Ruegsegger in detail. 35 Occurrence of fractures. Fractures that occurred in control subjects were self-reported during the follow-up period during regular telephone interviews conducted by a research assistant; in the TCC group, they were recorded with the help of the TCC master. All fractures were confirmed by radiography. Statistics Independent 2-tailed Student t tests were used to detect differences in age, anthropometric variables, menstruation status, and the BMD measurements between the TCC and control groups at baseline. Paired t tests were used to compare the BMD changes measured by both DXA and pqct between the baseline and follow-up measurements after excluding dropouts. The statistical significance level was set at P equal to.05 or less. The SPSS, version 9.0, c for Windows was used for data evaluation. RESULTS Comparison of Subjects Randomization at Baseline Table 1 shows the homogeneity in age, anthropometric variables (body weight, body height, BMI), and menstruation sta-

3 TAI CHI EXERCISE RETARDS BONE LOSS IN WOMEN, Chan 719 Table 1: Baseline Anthropometric Variables and Postmenopausal State of the TCC and Sedentary Control Groups Variables TCC Exercisers (n 67) Controls (n 65) P Values* Anthropometric Age (y) Body height (m) Body weight (kg) BMI (kg/m 2 ) Hormonal Reproductive years Years since menopause Age at menopause (y) NOTE. Values are mean standard deviation (SD). *Independent Student t test (all P.05). tus (reproductive years, years since menopause, age at menopause) between the TCC exercisers and controls at baseline. Both DXA areal and pqct volumetric BMD measurements revealed no statistical differences at baseline between the 2 groups (table 2). Attendance at TCC Exercise and Dropouts at 12-Month Follow-Up Average attendance rate of the TCC exercise was d/ wk. The dropout rate was 19.4% in the TCC group (13/67 subjects) and 16.9% in the control group (11/65 subjects), from either losing contact with subjects because of greater mobility of the population in Hong Kong or their starting drugs known to affect bone metabolism. In the control group, 5 other subjects completed pqct follow-up measurements but missed the DXA measurements (table 2). The number of dropouts did not differ from the rest of the study population at baseline, as calculated for both anthropometric data and BMD measurements. Changes of BMD at 12-Month Follow-Up Table 2 shows that the follow-up measurements reveal a generalized bone loss (average range, 0.10% 1.80%) in both areal BMD as measured by DXA and volumetric BMD as measured by pqct at the corresponding measurement sites in the control and TCC groups. DXA measurements showed significant bone loss in the femoral neck (1.80%, P.01) and trochanter (.56%, P.05) in the control group, and in the trochanter (1.19%, P.01) but not in the femoral neck (.94%, P.05) in the TCC group. Except for cbmd in the TCC group, pqct measurements at distal tibia also revealed significant bone loss at follow-up in tbmd, ibmd, and cbmd in both groups, ranging from 0.53% to 1.58%. However, there was a 2.6- to 3.6-fold significantly slower loss in the TCC group as compared with the control group, including tbmd (0.53% vs 1.46%, P.01), ibmd (0.61% vs 1.58%, P.01), and cbmd (0.39% vs 1.40%, P.01). DXA measurements showed a trend toward decelerated bone loss in the TCC group as compared with the control group, but the results were not consistent: although there was a slower rate of bone loss at the spine (.10% vs.89%) and femoral neck (0.94% vs 1.80%), the rate of bone loss in the femoral trochanter was faster (1.19% vs 0.56%). However, because of the large standard deviations all individual DXA measurements at both the spine and proximal femur did not show any statistical significance (all, P.05) (table 2, fig 1). Fractures occurred during the follow-up. During the 12- month study period, a total of 4 fracture cases were documented, including 3 fracture in the control group (1 vertebral fracture, 1 Colles fractures, 1 fracture at the fifth metacarpal) and 1 in the TCC group (proximal fibular fracture). All injury cases resulted from overloading during work (the case with vertebral fracture) or falls (the other 3 cases). DISCUSSION Evidence on the bone-stimulating effects of physical exercise largely comes from studies involving high-impact or power-trained athletes such as jumpers or weight lifters. 16,36-39 However, high-impact or strengthening exercises are not appropriate for older people because of the degenerative changes in the musculoskeletal systems that occur with aging and the associated injury risks. 5,16,30-33 TCC exercise is a unique form of physical activity, characterized by a high demand for neuromuscular coordination, low velocity of muscle contraction, low impact, and no jumping. Therefore, TCC has also been recommended as a suitable exercise for older people or patients with rheumatoid arthritis and osteoporotic conditions. 5,16,21-33 In this first prospective and randomized study, we investigated low-impact weight-bearing TCC exercise as a technique for preventing bone loss in postmenopausal women. Although the BMD measurement results show the expected generalized bone loss at all skeletal sites, as measured by DXA and pqct in both the TCC and control groups, 12 months of a supervised TCC exercise training intervention revealed some beneficial effects in retardation of bone loss, with a significantly reduced rate of bone loss in both trabecular and cortical compartments of distal tibia. Similar findings have been reported in previously. 17 Level of physical activity reduces with advancing age in older persons and such inactivity accelerates bone loss. 2,4,16 The most probable explanation for the beneficial effects of TCC exercise on reducing bone loss found in our study may be attributed to the TCC exercise intervention and its association with a more active lifestyle. 16,17-20,40 Not being able to increase or even maintain BMD in postmenopausal women after 12 months of TCC exercise may be explained by the fact that bone in one s late adult life becomes less responsive or even unresponsive to mechanical stimuli induced either by weight bearing or muscle contraction. This is evidenced by an age-related deterioration in the osteogenic mechanobiologic osteocyte-osteoblast network and retardation of osteocyte apoptosis because of mechanical stimulation The pqct measurements in the present study revealed a significant 2.6- to 3.6-fold deceleration of bone loss at the distal tibia in the TCC group in all compartments including tbmd, ibmd, and cbmd, as compared with the sedentary control group. The DXA data showed a general deceleration of bone loss in the TCC group; however, the deceleration did not reach statistical significance. This inconsistent finding may be attributed to differences in measurement precision, with a 3 times lower precision error (.32%) in pqct as compared with DXA (1.2%). 8,35 Use of multislice pqct for monitoring BMD changes may imply a 3-fold higher or earlier detection power of BMD difference, that is, a difference of 2.8 times in the pqct precision error at a 95% confidence level. 17,35,44,45 Similar results were found elsewhere. 17 It is thus not surprising that some previous controlled studies of relatively short duration in postmenopausal women, which used DXA for monitoring BMD changes, did not show any benefits of regular aerobic exercise for retardation of bone loss, which is also inconsistent with findings in BMD changes in the proximal femoral regions between the great trochanter and femoral neck. 46,47 Besides the use of different types of densi-

4 Measurement Region and Variables Table 2: Comparison of BMD and Its Changes Between the Groups at Baseline and After 12-Month Follow-Up TCC Exercisers Sedentary Controls Baseline Follow-Up Diff (%) P Values Baseline Follow-Up Diff (%) P Values At Baseline (TCC/CON) P Values* Changes (%) (TCC/CON) No. of subjects measured DXA pqct DXA (g/cm 2 ) Spine L Proximal femur Neck Trochanter pqct (mg/cm 3 ) Ultradistal tibia tbmd ibmd Distal tibial diaphysis cbmd NOTE. Values are mean SD. Abbreviations: Diff, difference; CON, sedentary control. *Unpaired t test comparing BMD differences between the TCC and control groups at baseline and paired t test comparing BMD changes after 12-month follow-up between the TCC and control groups. Actual BMD measurements for subjects at baseline and follow-up, without dropouts. P.05. P TAI CHI EXERCISE RETARDS BONE LOSS IN WOMEN, Chan

5 TAI CHI EXERCISE RETARDS BONE LOSS IN WOMEN, Chan 721 Fig 1. The annual changes of BMD at different anatomic sites measured by pqct and DXA in the control group (CON) and the TCC exercise group (values are mean SD). Multivariance analysis for combined evaluation of DXA and pqct measurements shows a significantly decelerated rate of bone loss at multiskeletal sites in the TCC group as compared with the control group (P<.05). When BMD was separately evaluated, only pqct data showed significant deceleration of rate of bone loss in the TCC group as compared with the control group. Abbreviations: See Baseline Measurements section. *Significant at P<01. tometers, the inconsistency may also be because of differences in study design, types of exercise intervention, subject selections, numbers of subjects for statistical analysis, and the skeletal sites selected for the BMD measurements. However, it has been suggested that if the duration for follow-up has been long enough, the beneficial effects of regular and low-impact exercise could be demonstrable by using DXA for measuring changes in BMD. 17,44,45 This has also been shown in previous DXA studies lifetime leisure sports or low-impact aerobic exercises in adult life maintained bone mass or retarded bone loss in pre-, peri-, and postmenopausal women ,36 For example, our recent study 17 showed a 10% to 15% higher areal BMD in the spine and proximal femur and an approximately 14% higher volumetric BMD in the distal tibia in postmenopausal women who had participated regularly in TCC exercise for, on average, more than 8 years as compared with the ageand gender-matched controls. A few previous large-scale, long-term, follow-up studies have suggested that an 8% to 10% higher baseline or increased areal BMD resulted from pharmaceutical or nonpharmaceutical approaches for prevention of osteoporosis was associated with about a 50% decreased risk of osteoporotic fracture. However, these studies did not delineate whether the reduced fracture occurrence was attributable to BMD alone or to the potential beneficial effects in fall prevention. It has been reported that approximately 30% of persons over 65 years of age sustain a fall annually, about 10% to 15% of falls result in serious injuries like hip and distal radius fracture or soft tissue injuries, and 90% of osteoporotic fractures are largely the result of falls. 1,6,23 In our current 12-month follow-up study, we observed 4 fractures (3 in control subjects, 1 in TCC subjects). Long-term follow-up and large-scale interventional studies are required to substantiate our primary observation that regular participation in TCC exercise may prevent fall-related fractures. Available studies of other groups 5,6,16,21,23,25-28,48,49 show that regular participation in TCC or similar exercises improves or maintains neuromuscular coordination by improving balance, posture stability, and flexibility, thereby reducing fall incidences and fall-related fractures among older individuals. Therefore, physical exercises that are suitable for older people for preventing osteoporosis should have beneficial effects not only in retarding bone loss but also in decreasing the risks of fall and fractures; improving balance, muscular strength, range of motion, endurance, and posture control; lessening pain; and, in general, improving quality of life. Although the present study was designed to evaluate potential beneficial effects of programmed TCC exercise on prevention of postmenopausal bone loss, it also emphasized that the level of BMD in one s later life is determined by both peak bone mass and subsequent rate of bone loss. Correspondingly, our approach to prevention of osteoporosis aims at achieving maximum peak bone mass in young adult and bone loss before onset of menopause. 7,8,14,15 The results of our randomized and prospective study might have eliminated some evaluation bias, as described in our previous study, 17 including no previous exercise history, identical TCC (Yang) style for exercise intervention, and controlled exercise frequency (times per week) and intensity (duration of each exercise unit). 17,40 However, a few limitations may still influence the magnitude of BMD measurements, including (1) the variations in attendance of TCC exercise group (on average d/wk instead of the initially defined 5d/wk), (2) the potential increase in the level of physical activity associated with participation in TCC exercise (eg, additional walking needed between home and the teaching venue while attending the supervised TCC exercise sessions), and (3) no quality control in kinetics and kinematics of each movement during Yang TCC exercise. 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