Complementary Therapies in Medicine (2014) 22, 235—243

Available online at www.sciencedirect.com

ScienceDirect journal homepage: www.elsevierhealth.com/journals/ctim

Core muscle function during specific yoga poses Meng Ni a, Kiersten Mooney b, Kysha Harriell a, Anoop Balachandran a, Joseph Signorile a,∗ a

Laboratory of Neuromuscular Research and Active Aging, University of Miami, Coral Gables, FL, United States b BalaVinyasa Yoga, Naples, FL, United States Available online 4 February 2014

KEYWORDS Electromyography; Yoga; Rehabilitation

Summary Objective: To assess the potential use of 11 yoga poses in specific training and rehabilitation programs via examination of the muscle activation patterns in selected trunk and hip muscles. Design: Repeated-measures descriptive study. Setting: University laboratory, US. Participants: : Thirty healthy yoga practitioners with more than 3 months yoga practice experience (mean age ± SD, 32.0 ± 12.3 y; 8 M/22 F) participated. Interventions: : Surface electromyographic signals of upper rectus abdominis, lower rectus abdominis, longissimus thoracis, external oblique abdominis and gluteus maximum muscle were recorded in 11 yoga poses: Halfway lift, Forward fold, Downward facing dog, Upward facing dog, High plank, Low plank, Chair, Mountain with arms down, Mountain with arms up, Warrior 1 (both sides). Main outcome measures: : Root mean square values of each muscle during each pose, normalized by the maximal voluntary contraction. Results: There were significant main effects of pose (p < .001) and muscle (p < .001), and a significant pose × muscle interaction (p = .001). The post hoc analysis revealed unique patterns for the five muscles of interest for each of the 11 poses (p < .024).

Abbreviations: EMG, electromyography; RAU, upper fibers of rectus abdominis; RAL, lower fibers of rectus abdominis; LT, Longissimus thoracis; EOA, external oblique abdominis; GM, gluteus maximum; MVC, maximum voluntary contraction. ∗ Corresponding author at: Department of Kinesiology and Sport Sciences, University of Miami, 1507 Levante Ave, Rm MO114, Coral Gables, FL 33146, United States. Tel.: +1 305 284 3105; fax: +1 305 284 4183. E-mail address: [email protected] (J. Signorile). 0965-2299/$ — see front matter © 2014 Elsevier Ltd. All rights reserved. http://dx.doi.org/10.1016/j.ctim.2014.01.007

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M. Ni et al. Conclusions: Variations in core muscle firing patterns depend on the trunk and pelvic positions during these poses. Training programs can be developed by choosing particular poses to target specific core muscles for addressing low back pain and declines in performance. The High plank, Low plank and Downward facing dog poses are effective for strengthening external oblique abdominis, Chair and Warrior 1 poses for targeting gluteus maximum, and Chair and Halfway lift poses for strengthening longissimus thoracis. And these three muscles could be strengthened by the Upward facing dog pose. © 2014 Elsevier Ltd. All rights reserved.

The core, or the lumbopelvic-hip complex, acts as an anatomical and functional linkage for the transfer of force from the distal segments throughout the body.1 The core is composed of a number of muscles, and strengthening these muscles is critical for providing local and global stabilization of trunk.2 More precisely, the hip muscles support the trunk structures and play a significant role in force transfer from the lower extremity upward through the spine.3 Muscular atrophy of the paraspinal muscles,4,5 excessive loads on the lumbar spine,6 poor endurance7 and imbalance of hip extensors8 are associated with back injuries and lower extremity instability. Core stability is also an important component for enhancing athletic performance9 and reducing the probability of back injury,10 improving functionality,11 and augmenting responses to training and therapy.12 Strengthening and stabilization exercises have been utilized to increase core strength and stability, decrease spinal and pelvic viscosity, and facilitate motor patterns.10 Several intervention studies have demonstrated the positive effects of core training on pain attenuation13,14 and performance.15 In addition to more traditional techniques, alternative conditioning methods such as Tai Chi, yoga and Pilates have also been employed.16 Yoga, originated in ancient India, aims to improve health conditions and address a wide range of health issues. The practice of yoga poses, or asanas, was developed as an approach to align, strengthen, and balance the structures of body.17 Yoga asanas consist of the basic positions of standing, sitting, forward bend, back bend, twisting, inversion, and lying down. Although yoga has been used to enhance dynamic control of the stabilizing muscles and reduce lower back pain18 through increased hip19 and spinal flexibility,20 the muscle activation patterns employed during specific yoga poses have yet to be investigated. Of special interest in the current study were the Vinyasa poses most commonly used to increase trunk muscle strength and balance, thereby improving stability and maximizing kinetic chain interactions between the upper and lower extremities.21 The objective of this study was to assess the potential use of 11 yoga poses in specific training and rehabilitation programs via examination of the muscle activation patterns in selected trunk and hip muscles. We hypothesized that different poses would produce unique variations in core muscle activation patterns that could provide guidelines for designing exercise prescriptions for training and rehabilitation.

Methods Participants A total of 30 yoga practitioners participated in the study (8 men, 22 women; mean age ± SD, 32.0 ± 12.3 y; mean weight ± SD, 62.3 ± 8.1 kg; mean height ± SD, 1.68 ± .075 m). Subjects were recruited on a voluntary basis through fliers, and personal contacts at yoga studios and wellness centers. The initial criterion for inclusion into the study was that the individual must have practiced yoga for more than three months or possessed a yoga instructor certification. Additionally, subjects must have participated in yoga training at least one time per week for at least three months, and must have been capable of completing the yoga sequence used in this study without assistance. Individuals with musculoskeletal and neurologic impairments, or existing or unresolved injuries that would limit movement in any way, were excluded from participating in this study. The length of time the subjects in our sample had been practicing yoga was 5.7 ± 5.5 years. All participants were informed of experimental procedures and completed a written consent approved by the University’s Subcommittee for the Use and Protection of Human Subjects. A power analysis using an effect size of 0.25, an ˛ value of 5% and a power of 95% yielded a minimal sample size requirement of 20.

Procedures When the subjects arrived at the laboratory, they were asked to complete the consent form and health questionnaire. They were then allowed to warm up by performing the Vinyasa (breath synchronized movement) Yoga Sun Salutation A three times and Sun Salutation B twice at a self-determined pace. Following the warm-up, electrodes were placed on the skin over the muscles of interest on the participant’s dominant side (27 right handed/3 left handed). A total of 5 muscle groups were tested, upper fibers of rectus abdominis (RAU), lower fibers of rectus abdominis (RAL), longissimus thoracis (LT), external oblique abdominis (EOA) and gluteus maximum (GM) muscle. To allow normalization of electromyography (EMG) data across subjects and collection days, 3 s maximal voluntary contractions (MVC) targeting each muscle were performed and EMG data from that muscle were collected. Following preparation and

Core muscle function during specific yoga poses Table 1

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Normalized rmsEMG amplitude for core muscles. Upper fibers of rectus abdominis

Pose Halfway lift Forward fold Downward facing dog Upward facing dog High plank Low plank Chair Mountain arms up Mountain arms down Dominant side warrior 1 Non-dominant side warrior 1

.077 .145 .080 .150 .270 .155 .085 .112 .087 .119 .082

± ± ± ± ± ± ± ± ± ± ±

.015 .026 .013 .035 .068 .030 .015 .023 .018 .027 .015

Lower fibers of rectus abdominis .060 .133 .067 .099 .225 .135 .057 .085 .064 .057 .066

± ± ± ± ± ± ± ± ± ± ±

.010 .030 .011 .015 .035 .039 .010 .019 .011 .011 .015

Longissimus thoracis

.288 .057 .123 .337 .143 .258 .320 .940 .105 .244 .212

± ± ± ± ± ± ± ± ± ± ±

.027 .011 .023 .058 .069 .088 .039 .020 .016 .036 .030

External oblique abdominis .224 .308 .383 .660 .784 .697 .287 .415 .318 .392 .363

± ± ± ± ± ± ± ± ± ± ±

.035 .070 .087 .121 .097 .102 .054 .081 .049 .072 .057

Gluteus maximus

.155 .183 .203 .410 .175 .164 .168 .226 .155 .397 .671

± ± ± ± ± ± ± ± ± ± ±

.022 .029 .058 .185 .038 .039 .033 .048 .029 .070 .252

All Normalized rmsEMG values (relative to MVC) are reported as mean ± SE.

normalization procedures, each subject was asked to perform 11 of the Vinyasa Yoga Sun Salutation poses maintaining each for a period of 15 s. The sequences in which poses were performed were randomized for each subject to minimize any order effect that may have resulted due to fatigue or post-activation potentiation produced by previous poses. The 11 poses are: Halfway lift (Urdhva Mukha Uttanasana), Forward fold (Uttanasana), Downward facing dog (Adho Mukha Svanasana), Upward facing dog (Urdhva Mukha Svanasana), High plank (Dandasana), Low plank (Chaturanga Dandasana), Chair (Utka.tasana), Mountain arms up (Urdhva Hastasana), Mountain arms down (Tadasana), Dominant side warrior 1 (Virabhadrasana I) and Non-dominant side warrior 1 pose.

EMG measurement procedures Disposable bipolar electrodes (Noraxon USA, Scottsdale, AZ) were positioned using established landmarks for the following muscles: RAU, 3 cm from the sagittal plane and 5 cm above the umbilicus22 ; RAL, 3 cm from the sagittal plane and 5 cm below the umbilicus22 ; LT, parallel to the spine and 4 cm from the L1 spine process over the muscle mass23 ; EOA, midway between the anterior superior iliac spine and the rib cage at a slightly oblique angle24 ; GM, half the distance between the trochanter (hip) and the sacral vertebrae in the middle of the muscle on an oblique angle at the level of the trochanter or slightly above.24 After electrode placement sites were established, the skin surface at each site was shaved, rubbed with a disposable, light abrasive paper, and cleansed with alcohol to remove dead surface tissues and oil that had the potential to reduce the strength and quality of the signal. The electrodes were then positioned parallel with the underlying muscle fibers, as determined by the pennation of the muscle. Five channels of raw EMG data were collected using a wireless EMG telemetry system (BTS Bioengineering, Milano, Italy) at a sampling rate of 1000 Hz, using band-pass filtering between 1 and 500 Hz, digitized using a 16-bit A/D converter,

amplified (gain = 2000, CMRR > 110 [email protected]—60 Hz), and stored on a personal computer. To allow normalization the EMG signals across subjects, poses and days, a maximum voluntary contraction (MVC) was performed for each muscle while EMG data were recorded. Each maximum contraction was held for 5 s and repeated 3 times for each muscle, with an intervening 30-second passive recovery period.23 The MVC exercise performed targeting the rectus abdominis (RA) muscle was a curl-up against maximal manual resistance applied by the tester on the subjects’ shoulder.25 The MVC exercise for the LT was a prone trunk extension performed at the end range of motion against a supramaximal load applied at the upper thoracic area.26 For the EOA, the subject performed an oblique curlup, attempting to move the resisted shoulder toward the opposite knee while this movement was prevented through the application of manual resistance.26 The MVC test for the GM was performed in the standing position, with a strap placed just above the knee. Subjects were asked to flex the knee approximately 1.57 rad and push the thigh posteriorly against the strap, attempting to extend the thigh.27

EMG data analysis Recorded EMG signals from each muscle were analyzed using a dedicated Labview Software program (National Instruments, Austin, TX). The root mean square of the EMG signal (rmsEMG) collected from the third to thirteenth second of each 15 s pose period was used as a measure of average muscle activity for each muscle during that pose. All data collected during the poses were normalized using the rmsEMG values collected during the middle 3 s of each 5 s MVC.

Statistical analyses Data were analyzed using a 5 (muscle) × 11 (pose) repeatedmeasures analysis of variance (ANOVA). This analysis was designed to examine the difference in muscle activities by muscle groups and poses. When statistically significant

238 main effects or interactions were detected, Bonferroni post hoc tests were used to determine the sources of these differences.28 The threshold for significance was set at p < 0.05.

Results Normalized EMG values (mean ± SE) for all muscles across poses are presented in Table 1. Significant differences among muscles for each pose are shown in the figures associated with each pose. There were significant main effects of pose (p < .001, 2 = .318) and muscle (p < .001, 2 = .214), and a significant pose × muscle interaction (p = .001, 2 = .134). The post hoc analysis revealed that unique patterns of difference were seen for the five muscles of interest for each of the 11 poses (p < .024). Table 1 presents the means and standard errors of the NrmsEMG values for each muscle during each pose. In the Halfway lift pose (Fig. 1a), the longissimus thoracis, external oblique abdominis and gluteus maximum showed significantly higher muscle activities than the upper and lower fibers of rectus abdominis (p < .002), and the LT also generated significantly higher muscle activity than the GM (p < .024). In the Forward fold pose (Fig. 1b), the EOA and GM generated significantly higher muscle activities than LT (p < .018). In the Downward facing dog pose (Fig. 2a), the EOA showed significantly higher activity than RAU and RAL (p < .018). In the Upward facing dog pose (Fig. 2b), the LT and EOA produced significantly higher muscle activities than RAU and RAL (p < .019). In the High plank pose (Fig. 2c), the EOA produced significantly greater electrical activity than all other muscles (p < .001). In the Low plank pose (Fig. 2d), the EOA produced significantly higher activity level than RAU, RAL and GM (p < .001). In the Chair pose (Fig. 3a) , the RAU, LT, EOA and GM produced significantly higher activity levels than RAL (p < .003). In the Mountain arms up (Fig. 3b) and arms down (Fig. 3c) pose, the EOA produced significantly greater muscle activities than RAU, RAL and LT (p < .006). In the Dominant side warrior 1 pose (Fig. 3d), the LT, EOA and GM produced significantly greater activities than the RAU and RAL (p < .022); while in the Non-dominant side warrior 1 pose (Fig. 3e), the LT and EOA muscle produced significantly higher EMG levels than the RAL, and the EOA generated significantly greater muscle activity than the RAU (p < .009).

Discussion We examined the activity levels of selected trunk and hip muscles during 11 poses commonly used during yoga training. The results supported our hypothesis that different poses would produce variations in the core muscle activation patterns. These findings can be beneficial for targeting specific muscles during training and rehabilitation programs designed to strengthen and stabilize the core. The Halfway lift pose (Fig. 1a) produced a level of muscle activity in the LT higher than activity levels seen for the RA or GM. The LT originates on the lumbar vertebrae and the sacrum and iliac crest and inserts on thoracic vertebrae 1 through 12. It is activated during trunk extension.29 In the Halfway lift pose, the spine is parallel to the ground

M. Ni et al. or slightly extended and the pelvis is in the anteverted (forward rotated) position producing increased LT activity. The structure and function of the LT also explain its low activity level during the Forward fold pose where the trunk is in forward flexion (Fig. 1b). When comparing these two poses, the activity level of the RA was nearly twice as great during the Forward fold versus the Halfway lift due to the increased need to activate this trunk flexor to produce a deeper forward bend.6,29 The Downward facing dog (Fig. 2a) is a recovery pose in the Vinyasa sequence, and is used to stretch the backs of the legs and shoulders. Our results reveal the importance of the EOA and GM in holding this position. In the Upward facing dog pose (Fig. 2b), the hip is extended and internally rotated, and the trunk is extended. Based on our results, the increased activity level of the GM was necessary to support these movement patterns. Given that this pose can effectively target the GM, it could be a tool for improving lower extremity alignment during single leg support30 and reducing the potential for lower extremity injury,31 such as damage to the knee ligaments.32 During this pose, the LT generated significantly higher muscle activities than RAU and RAL. This back extension pose stretches the anterior aspect of trunk muscles and mobilizes the posterior trunk musculature. Although this pose may not be appropriate for alleviating acute lower back pain,33 it may still be an effective intervention to reduce chronic lower back pain.34,35 This pose also could be used as an exercise for strengthening the EOA. In the High plank (Fig. 2c) and Low plank (Fig. 2d) poses, the EOA activity levels were the highest seen for any poses; however, the activity levels for the RAU and RAL were relatively low compared to the values seen for the EOA. Our results differ from those noted by Ekstrom et al.,23 who reported that the EOA and RA produced activity levels of 43% and 47%MVC for the prone-bridge pose, and suggested this exercise might not be appropriate to strengthen the abdominal muscles. The differences in the activation levels between the two studies may be attributed to the difference in the pose characteristics. The prone-bridge pose is a plank pose supported at the elbows, whereas the High and Low plank poses requires hand-support with elbow straight and flexed to 1.57 rad, respectively. Because of the smaller base of support inherent in the High and Low plank poses, the activity levels of EOA would be expected to exceed that seen with the prone-bridge plank since these higher activity levels would be required to maintain the stability of the core segment. In contrast, Stokes et al. reported no significant differences in activation levels among the RA, erector spinae and GM, indicating that the co-contraction of these muscles may have augmented core stability by increasing axial load and inducing greater intervertebral stiffness36 ; however, elevated axial loading of the lumbar spine may cause lower back pain.37 In our study, no external load was applied to the spine and the LT was activated to reduce flexing the pelvis and maintain the back in the plank position. Additionally, the GM contracted to retrovert (backward rotation) the pelvis and the RAU and RAL were used to keep the hip in a neutral position. In the Chair pose (Fig. 3a), the hip was in a flexed position and GM activity was modest. This counterbalanced the forward tilt of the pelvis and created a stable foundation

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Figure 1 Normalized root mean square of the EMG signal for the core muscles during forward bending poses including the Halfway lift (a), and Forward fold (b). Upper fibers of rectus abdominis (RAU), lower fibers of rectus abdominis (RAL), Longissimus thoracis (LT), external oblique abdominis (EOA) and gluteus maximus (GM). **greater than RAU and RAL, †greater than RAU, RAL and GM, §greater than LT.

for the trunk structures. This is important when transferring forces from the lower extremities to the trunk and adjusting activation levels of key lower extremity muscles during physical activity.38 During this pose contraction of the EOA also created a retroverted torque to resist hip flexion and stabilize the pelvis. Additionally, the moderately high activity level seen for the LT was consistent with the level of trunk extension required for the Chair pose. However, the muscle activation levels for the LT and RAU were similar, which is not consistent with previous findings which indicated that RA muscle activity showed low activity levels during trunk extension.39 This may be due to the small degree of trunk extension during the Chair pose which required an equally low level of RA and LT co-contraction to stabilize the spine. In the Mountain pose with arms down (Fig. 3c), a starting position of the Vinyasa flow, the lack of significant difference between the RA and LT activity suggests that co-contraction of the core muscles was required to stabilize the lumbopelvic-hip segment. Co-contraction of muscles on the dorsal and ventral aspects of the trunk increases intra-abdominal pressure and produces significant trunk stiffness.3 This pattern was also apparent during the Mountain pose with arms up (Fig. 3b). These two standing poses are designed to elevate the back, open the pelvic region, and compress the ribcage to increase stabilization. The significantly higher muscle activity in EOA compared to RAU, RAL and LT indicates that pelvis is moving to a retroverted

position. This assertion is supported by the findings of Queiroz et al.,40 that pelvic retroversion requires an increase in EOA activity. In the warrior 1 pose (Fig. 3d and e), the hip and knee of the dominant and non-dominant sides were respectively flexed and extended, while the spine was kept extended. When the front leg was flexed, the back-leg GM was activated to extend and externally rotate the hip producing a very high activity level. This pose could be an effective tool for increasing GM strength; however, the level of GM activity during the non-dominant side warrior 1 did not produce significantly higher activity than other muscle groups; this may have been due to the high variation in the activation pattern of this muscle among subjects. Meanwhile, contracting the LT maintained a limited level of back extension, which could potentially develop muscular endurance and reduce fatigue. Therefore, this pose could be an effective treatment for chronic lower back pain, where individuals show a reduction in muscle endurance and great fatigability compared with healthy controls.41 When examining the levels of activation of the LT, OEA and GM, our results meet the criteria stated by Cresswell et al.,42 who noted that contractions as low as 25% of MVC could effectively increase support offered by muscles that stabilize the lower back. McGill et al.,43 have presented an even more conservative goal of 10% MVC as an effective level of activation to improve trunk muscle performance

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Figure 2 Normalized root mean square of the EMG signal for the core muscles during the downward facing dog (a), upward facing dog (b), high plank (c), and low plank (d). Upper fibers of rectus abdominis (RAU), lower fibers of rectus abdominis (RAL), longissimus thoracis (LT), external oblique abdominis (EOA) and gluteus maximus (GM). **greater than RAU and RAL, †greater than RAU, RAL and GM, ‡greater than RAU, RAL, LT and GM.

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Figure 3 Normalized root mean square of the EMG signal for the core muscles during Chair (a), mountain pose arms up (b), mountain pose arms down (c), dominant side warrior (d), and non-dominant side warrior (e). Upper fibers of rectus abdominis (RAU), lower fibers of rectus abdominis (RAL), longissimus thoracis (LT), external oblique abdominis (EOA) and gluteus maximus (GM). *greater than RAL, **greater than RAU and RAL. §§greater than RAU, RAL and LT.

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Figure 3

for stability during activities of daily living. In contrast to the increased levels of activity seen in these three muscles, increases in activation of the URA and LRA were limited, indicating that the poses examined should be supplemented using other poses or exercises if the goal is the targeting of the RA musculature. While the current study provides insight into the targeting of specific muscles for training and rehabilitation, the research was conducted using healthy yoga practitioners. These finding may not be generalizable to other populations such as persons without yoga experience, older individuals or patients undergoing rehabilitation for specific injuries or disease states. Additionally, our study provides results related to muscle activity levels but suffers from a lack of kinematic or kinetic data. Therefore, we suggest that future studies examine specific yoga poses in special populations and that these studies include biomechanical analyses.

(Continued)

thoracis. By selectively choosing particular poses, prevention and rehabilitation programs can be developed that address strength and endurance insufficiencies in specific muscle groups that might, for instance, cause low back pain and declines in performance. Clinicians can feel secure in using the poses presented in this study for both preventative and rehabilitative purposes since they reach critical activation levels necessary to generate improvements, but do not provide levels of activation that may put the core muscles and related structures at high levels of risk for injury.

Conflict of interest We wish to confirm that there are no known conflicts of interest associated with this publication and there has been no significant financial support for this work that could have influenced its outcome.

Conclusion Our study provides data on the core muscle activation patterns during the eleven most commonly practiced yoga poses. Variation in core muscle firing patterns depends on the trunk and pelvic positions in these poses. The High plank, Low plank and Upward facing dog poses could be used as effective exercises for strengthening external oblique abdominis. The Chair, Upward facing dog and Warrior 1 poses appear effective for building gluteus maximus strength. The Chair, Halfway lift and Upward facing dog poses could be appropriate to develop muscle strength for longissiums

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Core muscle function during specific yoga poses.

To assess the potential use of 11 yoga poses in specific training and rehabilitation programs via examination of the muscle activation patterns in sel...
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