Physiotherapy Theory and Practice

An International Journal of Physiotherapy

ISSN: 0959-3985 (Print) 1532-5040 (Online) Journal homepage: http://www.tandfonline.com/loi/iptp20

Effect of a six-month yoga exercise intervention on

fitness outcomes for breast cancer survivors

Daniel C. Hughes PhD, Nydia Darby DPT, Krystle Gonzalez DPT, Terri Boggess
PhD, Ruth M. Morris MPH & Amelie G. Ramirez DrPH

To cite this article: Daniel C. Hughes PhD, Nydia Darby DPT, Krystle Gonzalez DPT, Terri
Boggess PhD, Ruth M. Morris MPH & Amelie G. Ramirez DrPH (2015) Effect of a six-month yoga
exercise intervention on fitness outcomes for breast cancer survivors, Physiotherapy Theory
and Practice, 31:7, 451-460, DOI: 10.3109/09593985.2015.1037409

To link to this article: http://dx.doi.org/10.3109/09593985.2015.1037409

Published online: 23 Sep 2015.

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ISSN: 0959-3985 (print), 1532-5040 (electronic)

Physiother Theory Pract, 2015; 31(7): 451–460

! 2015 Taylor & Francis. DOI: 10.3109/09593985.2015.1037409

RESEARCH REPORT

Effect of a six-month yoga exercise intervention on fitness outcomes for

breast cancer survivors
Daniel C. Hughes, PhD1, Nydia Darby, DPT2, Krystle Gonzalez, DPT3, Terri Boggess, PhD4, Ruth M. Morris, MPH1, and
Amelie G. Ramirez, DrPH1
1
Institute for Health Promotion Research, University of Texas Health Science Center at San Antonio, San Antonio, TX, USA, 2Nydia’s Yoga Therapy,
San Antonio, TX, USA, 3Doctor of Physical Therapy Program, School of Health Professions, University of Texas Health Science Center at San Antonio,
San Antonio, TX, USA, and 4Exercise and Sport Science Department, St. Mary’s University, San Antonio, TX, USA
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Abstract Keywords
Yoga-based exercise has proven to be beneficial for practitioners, including cancer survivors. Cancer survivors, fitness, yoga
This study reports on the improvements in physical fitness for 20 breast cancer survivors who
participated in a six-month yoga-based exercise program (YE). Results are compared to a History
comprehensive exercise (CE) program group and a comparison (C) exercise group who chose
their own exercises. ‘‘Pre’’ and ‘‘post’’ fitness assessments included measures of anthropomet- Received 9 April 2014
rics, cardiorespiratory capacity, strength and flexibility. Descriptive statistics, effect size (d), Revised 4 February 2015
dependent sample ‘t’ tests for all outcome measures were calculated for the YE group. Accepted 9 February 2015
Significant improvements included: decreased % body fat (3.00%, d ¼ 0.44, p50.001); Published online 8 September 2015
increased sit to stand leg strength repetitions (2.05, d ¼ 0.48, p ¼ 0.003); forward reach (3.59 cm,
d ¼ 0.61, p ¼ 0.01); and right arm sagittal range of motion (6.50 , d ¼ 0.92, p ¼ 0.05). To compare
YE outcomes with the other two groups, a one-way analysis of variance (ANOVA) was used. YE
participants significantly outperformed C participants on ‘‘forward reach’’ (3.59 cm gained
versus 2.44 cm lost), (p ¼ 0.009) and outperformed CE participants (3.59 cm gained versus
1.35 cm gained), but not statistically significant. Our results support yoga-based exercise
modified for breast cancer survivors as safe and effective.

Introduction active often do not return to their previous level of activity

(Schmitz et al, 2010b). Specifically, approximately four out of
Each year, over 226 000 new women are diagnosed with breast
every five breast cancer survivors do not meet national exercise
cancer (American Cancer Society, 2012). Breast cancer remains
recommendations at 10 years post diagnosis (Mason et al, 2013).
the most prevalent cancer for women, and for Latina women, it is
For centuries, yoga has been recognized as a form of exercise
still the number one cancer killer (American Cancer Society,
that can yield increased flexibility, weight management, strength
2009). A growing body of research documents the benefits of
and endurance for regular practitioners (Agte, Jahagirdar, and
exercise for breast cancer survivors, including improvements in
Tarwadi, 2011; Gordon et al, 2008; Olivo, 2009; Phoosuwan,
fitness, physical functioning, fatigue and emotional well-being
Kritpet, and Yuktanandana, 2009; Pullen et al, 2008; Ulger and
(Courneya 2003; Courneya et al, 2003; Pinto, Frierson, Trunzo,
Yagli, 2011). Yoga-based exercise is also emerging as an
and Marcus 2005; Schmitz et al, 2010b; Segal et al, 2001).
important practice to be used for cancer survivors and shown to
Indeed, cohort studies have shown a decreased risk of breast
improve cancer survivors self-reported quality of life (QOL)
cancer recurrence and lowered breast cancer mortality for those
(Banasik et al, 2011; Bower et al, 2012; Buffart et al, 2012; Culos-
breast cancer survivors who are more physically active (Ballard-
Reed, Carlson, Daroux, and Hately-Aldous, 2006; Danhauer et al,
Barbash et al, 2012; Holmes et al, 2005; Irwin et al, 2011;
2009; DiStasio, 2008; Kiecolt-Glaser et al, 2014; Lengacher et al,
Patterson, Cadmus, Emond, and Pierce 2010). Thus, engaging in
2012; Moadel et al, 2007; Mustian et al, 2013; Ulger and Yagli,
exercise activities is an important behavior for breast cancer
2010; Van Puymbroeck et al, 2013).
survivors (Courneya, Mackey, and Jones 2000; Schmitz et al,
Though most randomized trials using yoga-based exercise have
2010b).
looked at QOL parameters as primary outcomes (Buffart et al,
Although these benefits have been well documented, only a
2012), several studies have looked at physical fitness and physical
minority of breast cancer survivors are active at levels consistent
functioning outcomes specific for breast cancer survivors (Bower
with public health guidelines (Schmitz et al, 2010b). Like others
et al, 2012; Culos-Reed, Carlson, Daroux, and Hately-Aldous,
who experience cancer, many breast cancer survivors who were
2006; Littman et al, 2012). Based on these initial studies that
not active before diagnosis will stay inactive; and, those who were
provide strong evidence on the benefits of purposeful yoga-based
exercise and to better understand the effects of different
Address correspondence to Daniel C. Hughes, PhD, Institute for Health
modalities of exercise on a comprehensive array of fitness
Promotion Research, University of Texas Health Science Center at San outcomes, we sought to conduct a six-month randomized trial
Antonio, 7411 John Smith Drive, Suite 1000, San Antonio, TX 78229, comparing yoga-based exercise with ‘‘conventional’’ exercise and
USA. E-mail: [email protected] with exercise of individual’s own choosing. We randomized 94
 452 D. C. Hughes et al. Physiother Theory Pract, 2015; 31(7): 451–460

post-treatment breast cancer survivors either to a yoga-based completing the study, respectively. There were no reported
exercise program (YE), a ‘‘conventional’’ comprehensive exercise injuries in any group related to the exercise programs.
(CE) program (aerobic, resistance, flexibility) consistent with Specifically designed yoga exercise classes were taught to the
public health guidelines for physical activity for U.S. adults participants in a local yoga studio. YE participants were asked to
(United States Department of Health and Human Services 2008), attend three 1-hour yoga classes per week. Participants were
or to a comparison group (C) where participants chose their own neither encouraged nor discouraged from seeking other forms of
exercise activities. Here we detail the methodology and the fitness exercise but were highly encouraged to attend the yoga classes
outcomes for the YE group and compare the results to the other offered. In addition, an audio CD and an instruction booklet for
two groups. We expected that the YE group would have equal to the specific protocol were provided to the participants for use at
or better outcomes when compared to the CE group and both the home when class attendance was not feasible. For the CE group
CE and YE groups would have better outcomes than the C group. individualized exercise programs were prescribed by an ACSM
certified Clinical Exercise PhysiologistÕ . The program compo-
Methods nents were based on the participants’ individual baseline fitness
results, following ACSM guidelines (American College of Sports
Recruitment Medicine, 2013), and consistent with the levels of activity as
After obtaining approval from the Institutional Review Board at described in the public health guidelines for physical activity for
the University of Texas Health Science Center at San Antonio adults (United States Department of Health and Human Services,
(UTHSCSA), and the Cancer Therapy and Research Center 2008). The exercise programs included components of aerobic,
Protocol Review Committee, participants were recruited with resistance and flexibility training focused on three 1-hour sessions
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assistance from the ThriveWellÕ Cancer Foundation’s DIVA per week. C group participants were asked to participate in three
(Deriving Inspiration and Vitality through Activity) program, a hours of exercise of their own choosing, though they were given a
self-referral program that offers support services for breast cancer DIVA class schedule and encouraged to attend DIVA activity
survivors. Potential participants who called in to register for classes. The DIVA program provides classes at five different
DIVA services or expressed interest in response to study flyers, locations across the city of San Antonio. More than 30 exercise
radio and TV advertisements were screened for eligibility by classes are held every week and the class offerings include
research staff. Inclusion criteria were: age 18 or older; previous aerobics, strength training, yoga, Tai Chi, Zumba, water aerobics
diagnosis of invasive breast cancer or ductal carcinoma in-situ; and belly dancing. CE and C participants were asked to log their
being at least two months post-treatment (surgery, chemotherapy, activities. Similar to the YE group, CE and C participants were
radiation, or any combination thereof); able to provide informed neither encouraged nor discouraged from seeking other forms of
consent; and free of any absolute contraindications for exercise exercise beside those prescribed. An assigned research staff
testing as stated in the American College of Sports Medicine member called all participants every two weeks to answer any
(ACSM) Guidelines for Exercise Testing (American College of questions, monitor possible safety concerns, and encourage
Sports Medicine, 2013). If interested in participating in the program participation.
research, participants were asked over the phone to complete the
Physical Activity Readiness Questionnaire (PAR-Q), as detailed Procedures
in the ACSM’s Guidelines for Exercise Testing and Prescription
Fitness assessment summary
(American College of Sports Medicine, 2013). Physician’s
clearance was required for all participants that answered ‘‘yes’’ The fitness assessments included tests for cardiorespiratory
to any of the seven questions listed on the PAR-Q prior to capacity, muscular strength, flexibility and body composition.
scheduling them for baseline appointments. Participants who For cardiorespiratory capacity, a ramped sub-maximal cycle
answered ‘‘no’’ to all questions or had received physician’s ergometer test was used with a metabolic cart for capturing
clearance were scheduled for a comprehensive fitness baseline expired respiratory gases and used to estimate VO2max (mlO2/kg/min)
assessment. Participants were asked to provide a detailed list of all based on a linear heart rate (HR) response to increased VO2
current medications at baseline assessment; any participants who uptake. Arm, shoulder and torso muscular strength were tested
were on maintenance therapies (e.g. Tamoxifen) were allowed to using a strength dynamometer. For leg strength, participants
participate in the study. performed a timed ‘‘sit-to-stand’’ test. Hip and lower back
flexibility were measured using a ‘‘sit-and-reach’’ flexibility box.
Study design Upper body flexibility and balance were assessed using a
‘‘forward reach’’ functional task. Shoulder flexion range of
Of the 130 women who expressed interest in the study, 121 met motion (ROM) in the sagittal and lateral planes was measured
the inclusion criteria, and 94 of those completed baseline fitness using an inclinometer. Body composition was assessed calculating
assessments (Figure 1). Informed consent was obtained with the body mass index (BMI) (kg/m2) and conducting a three-site
baseline assessments conducted at a cancer treatment center in the skinfold assessment (triceps, suprailium, and quadriceps). Arm
San Antonio, Texas area. Using a minimization adaptive volume for both arms was measured using water volume
randomization technique, participant covariates of age, body displacement. Participants received a $25 gift card as compen-
mass index (BMI), and cardiorespiratory capacity (estimated sation upon completion of the assessments.
VO2max) were used to assign 94 participants either to: (1) a yoga-
based exercise program (YE) group, n ¼ 31; 2) a comprehensive,
Yoga program specifics
individualized exercise program (CE) group, n ¼ 31; or 3) a
comparison group (C), in which participants performed exercises A structured Hatha yoga exercise program was developed
of their choice, n ¼ 32. Here we detail the results of the YE group specifically for this study. The program took into account the
and compare their results to the CE and C groups. Of the 31 potential limitations of limb movement, higher body fatness, and
participants randomized to the YE group, 20 completed the the lower aerobic and strength conditioning characteristic of post-
six-month trial and completed ‘‘post’’ fitness assessments. In the treatment breast cancer survivors (Schmitz et al, 2010b).
other two groups, a total of 11 participants dropped out, resulting The protocol was developed by an experienced yoga instructor
in 26 participants in both the CE group and the C group and a licensed clinically trained physical therapist with extensive
 DOI: 10.3109/09593985.2015.1037409 Yoga and fitness outcomes 453

Interested Population
n= 130 Inclusion Criteria
• 18 years old
• Breast cancer diagnosis
• ≥ 2 months post treatment
Met Inclusion Criteria
n= 121
Withdrawals n= 27
• Illness/surgery/family emergency
(n=6)
• New cancer diagnosis/
chemotherapy (n=2)
• Not enough time (n=1)
Complete Baseline • Decided not to participate (n= 19)

Assessments
n= 94
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Randomization

Comprehensive Yoga Focus Comparison

Exercise (CE) Exercise (YE) Exercise (C) CE Withdrawals n = 5
n=31 n=31 n=32 Lost to follow-up (n = 1)
Cited time/distance (n =2)
Did not make “post” (n =2)
Take care of parent (n =1)
Developed hernia (n =1)
YE Withdrawals n = 11
Lost to follow-up (n = 3)
Aerobic, Studio and/or at Exercise of Cited time/distance (n =2)
strength, home yoga choice 3 Did not make “post (n =2)
flexibility exercise 3 hours/week Dropped out (n =1)
exercise 3 hours/week Job conflict- travel (n =1)
hours/week Moved out of town (n =1)
Broke leg in accident (n =1)
C Withdrawals n = 6
Lost to follow-up (n = 3)
Did not make “post” (n =2)
Take care of parent (n =1)
Post Post Post
Assessments Assessments Assessments
n= 26 n= 20 n= 26

Figure 1. Study flow diagram.

experience in hospital, outpatient, home health, private and A total of five instructors were available to deliver six classes per
community education settings, including working with closely week at set times on six days per week (Monday–Saturday) to
with cancer survivors. allow for morning, evening and weekend access for participants.
The program included: an emphasis on breath awareness and Four of the five instructors were 200-h certified yoga instructors
practice (pranayama); a modified Sun Salutation; standing, receiving 50 h of direct training in the pertinent components for
seated, quadruped, twisting/rotation, prone, supine postures the actual class to be taught (specific language to be used, timing,
and the transition used between postures; modified inversion; modifications, specific cues, appropriate delivery style including
and guided relaxation and resting postures. The protocol and voice quality and pace of instruction given). In addition, the
sequencing of postures were designed with a great deal of instructors were required to practice individually and in groups
specificity to guarantee that the subjects would receive the same teaching each other for an additional 20 h. The physical therapist
instructions and perform the same routine, regardless of the who designed the class and provided the training served as the
instructor or class attended. Modifications were developed for fifth instructor.
each posture to accommodate the limitations that might be
encountered within this population. The instructors that led the Measures
classes for the study participants received training in specific
Co-morbidity index
language to be used, as well as timing/pacing for the class to
ensure consistency for the 60-min program used throughout the From the medical history information, a co-morbidity index was
duration of the research study. Breathwork was cued and directed calculated with a sum score of the number of a possible 17 items
through the entire asana practice. Asana practice was set for endorsed: (1) diagnosis of a heart attack; (2) heart failure;
50 min with guided savasana and closing for the final 10 min. (3) heart condition; (4) circulation problems; (5) blood clots;
 454 D. C. Hughes et al. Physiother Theory Pract, 2015; 31(7): 451–460

(6) hypertension; (7) stroke; (8) lung problems; (9) diabetes; assessing maximum effort during exercise testing than an RPE
(10) kidney problems; (11) rheumatoid arthritis; (12) osteoarth- level of 20 (Faulkner, Parfitt, and Eston, 2007). (3) For
ritis; (13) anemia; (14) thyroid problems; (15) neuropathy; participants who had difficulty wearing the face mask or preferred
(16) fibromyalgia; and (17) hepatitis. to not use the mask, an alternative protocol was used. Briefly,
research staff set the cycle ergometer to record W. Recording
Resting hemodynamics (resting heart rate, resting blood pressure) began after a 2-min warm-up with the participant cycling at 20 W.
Every 2 min resistance was increased by 20 W or 30 W depending
Before resting heart rate (RHR) resting systolic (SBP) and
on participants’ response to increased work level. W and
diastolic blood pressure (DBP) were taken, the participant was
corresponding HR were recorded every 2 minutes up to each
asked to rest in a seated position for at least five minutes. Resting
participant’s voluntary level of tolerance (usually RPE levels of
blood pressures (SBP and DBP) were taken manually using a
14–16). Work rate (kg-m/min) was obtained by multiplying W by
sphygmomanometer and a stethoscope via the right arm, (or in
the conversion factor 6.12, and VO2 uptake was calculated using
case of participants with lymphedema – an unaffected limb),
the formula based on ACSM-recommended calculations for
using the first and fifth Korotkoff sounds as indicated of SBP and
estimation of energy expenditure – Table 7.3 (American College
DBP, respectively according to ACSM guidelines for blood
of Sports Medicine, 2013): VO2 uptake ¼ 3.5(resting compo-
pressure testing (American College of Sports Medicine, 2013).
nent) + 3.5 (horizontal component) + ((1.8 X work rate)/body
Participants had their RHR measured via a pulse oximeter
mass (kg)). Estimated VO2max was then calculated by linear
attached on the opposite finger/hand.
regression of VO2 uptake on HR using the same linear regression
methods as detailed above. For those participants that expressed
Cardiorespiratory capacity
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the desire to ‘‘push on’’ during exercise testing and reached

For cardiorespiratory capacity, a ramped cycle ergometer test an RER41.1 for at least 30 s, the corresponding VO2 uptake
based on ACSM Guidelines for submaximal exercise testing was designated as their estimated VO2max and no regression
(American College of Sports Medicine, 2013) was conducted to equations were used.
obtain estimated VO2max (mlO2/kg/min). A Lode Corival Cycle
(Groningen, Netherlands) and a ParvoMedics TrueOneÕ 2400 Strength
metabolic cart (ParvoMedics, Sandy, UT) were used. A specific
Arm strength was tested using a Takei 5002 pull dynamometer
protocol for this population was developed by the lead author, an
system (Takei Scientific Instruments, Niigata City, Japan).
ACSM certified Clinical Exercise PhysiologistÕ , which has been
Participants stood on top of the dynamometer platform and
used previously in studies with endometrial cancer survivors
were asked to hold a handle bar chained to the sensor with wrists
(Hughes et al, 2010; Basen-Engquist et al, 2011).
in a supinated position, activating the biceps, at an approximate
In detail, participants began by pedaling with no resistance for
30 angle. Keeping their back vertically aligned, participants
60 s, followed by a warm-up stage of 2 minutes at 20 watts (W).
pulled with voluntary maximum effort for 5 s, rested 15 s and
During the exercise stage, resistance increased until the partici-
repeated the task. Peak force (kg) was noted for each trial and the
pant reached either: 85% of their age-predicted maximum heart
larger value was recorded.
rate (HR); a sustained respiratory exchange ratio (RER)41.0; or
Shoulder strength was tested similarly; except the participants
signaled that they wished to stop. During the exercise phase,
switched their wrists to a pronated position, activating the
blood pressure, HR and Rating of Perceived Exertion (RPE) using
deltoids. Torso strength was assessed in a similar fashion.
the Borg scale (Borg, 1998) were recorded every 2 min, and every
Participants were instructed to hold the handle bar with wrists
minute during the subsequent recovery stage. Real-time breath-
in a pronated position with arms extended flexing their trunk at
by-breath gas exchange data were obtained and included
approximately 30 to activate the torso. Participants were
measurements of VO2 (mlO2/kg/min), VCO2 (L), and RER
instructed to pull back with maximal force. The higher value
(VCO2/VO2).
(kg) of two trails was recorded.
As this was a submaximal test, in order to obtain more
For leg strength, participants were asked to perform a timed
accurate estimates of VO2max, one of either three calcula-
‘‘sit-to-stand’’ test. Research staff demonstrated the proper
tions was performed depending on participant characteristics. (1)
technique and then prompted the participants to begin. The
VO2max was estimated by linear regression analysis, regressing
number of times the participant stood fully erect and sat down in a
HR against corresponding VO2 uptake (ml O2/kg/min) levels
30-s time period was recorded.
during the period from the beginning of the exercise phase
(resistance421 W) to the exercise phase ‘‘termination point’’ of
Flexibility
either: RER  1.0 or a HR of 85% of age-predicted maximum
rate. To smooth out the inherently noisy breath-by-breath data, For flexibility, participants performed a ‘‘sit-and-reach’’ test,
15-s average HR and VO2 uptake levels were used in the a ‘‘forward reach’’ test and had passive arm range of motion
regression analysis. The linear relationship was then extrapolated (PROM) measured using an inclinometer. Hip and lower back
to the participants’ age-predicted maximum HR (220 – current flexibility were measured using a ‘‘sit-and-reach’’ task (Canadian
age), and the estimated VO2max level was then determined by the Society for Exercise Physiology, 2003) with a Lafayette model
regression equation. (2) For participants who reported taking 01285B sit and reach flexibility box (Lafayette Instruments,
beta-blocker type medications, a regression equation based on Lafayette IN). Participants were instructed to sit on the floor, with
RPE was used since HR response to increasing workload could be feet completely flat on the box and legs fully extended.
suppressed with this class of medications. In these cases, the RPE Participants were asked to extend their arms forward with one
level was regressed on VO2 levels during the period from the hand on top of the other, in a controlled motion while gently
beginning of the exercise phase (resistance greater than 21 W) to exhaling. The maximal distance reached (cm) in three trials was
the ‘‘termination point’’. The RPE was then extrapolated to a recorded.
‘‘maximum’’ RPE of 19, and the estimated VO2max level Upper body flexibility and balance were assessed using a
was determined on the basis of a linear relationship between VO2 functional forward reach assessment task (Duncan, Weiner,
and RPE. An RPE of 19 was used as the maximum point, as Chandler, and Studenski, 1990). Participants stood adjacent to a
previous studies have indicated this value is more realistic for meter stick on a wall with arm horizontal and parallel to the floor
 DOI: 10.3109/09593985.2015.1037409 Yoga and fitness outcomes 455

with the palm of the hand facing downward. Without moving their 2006; Chen et al, 2010). Effect sizes were defined as: small (0.2);
feet, participants reached forward as far as possible. The maximal medium (0.5); or large (0.8) (Cohen, 1988). To compare YE
distance reached (cm) in two trials was recorded. participant outcomes with the other two groups, we used a one-
Arm flexion PROM in the sagittal and lateral planes was way analysis of variance (ANOVA). Bonferroni post hoc tests
measured using an inclinometer. Participants were asked to point were applied when the difference was significant (p50.05)
their thumbs forward in the direction of a vertical line while according to the results of the ANOVA.
standing on pre-marked floor squares. The participants’ arm was
placed in a neutral resting position to the side and the
Results
inclinometer was placed across the elbow, PROM occurred in
the sagittal plane until resistance was felt at the shoulder girdle, Participant baseline characteristics are shown in Table 1. Prior to
avoiding compensation (e.g. shoulder hiking). PROM measure- randomization, our participants averaged 56.2 years of age, had
ment ( ) with the inclinometer was recorded at the point moderate levels of co-morbidities (2.3), were overweight
compensation was noted. When measuring in the lateral plane, (BMI ¼ 28.8 kg/m2) and presented with very low cardiorespira-
participants were asked to point their thumbs along a horizontal tory capacity (19.8 ml O2/kg/min). This low level of cardio-
line of the floor square employing the identical procedure. respiratory capacity is less than the 10th percentile for age and
gender as reported by ACSM fitness categories (American
Anthropometrics College of Sports Medicine, 2013). Our participants’ ethnicity
was one third Hispanic (32%), and race was predominately white
Anthropometric measures included BMI (kg/m2) calculated from
(80%). Our participants were highly educated with 60% having
height (cm) and weight (kg), body fat estimates from three-site
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obtained at least a bachelor’s degree. Approximately half of our

skinfold measures and arm volume by water displacement. Height
participants (49%) were fully employed and 36% reported as
(cm) and weight (kg) were measured using a wall-mounted
either retired or home-maker.
Stadiometer (Seca 644 Handrail Scale). For body fat esti-
There were no significant differences between groups in
mate, three-site (triceps, supra-ilium, and quadriceps) skinfold
baseline characteristics. However, in a comparison between
assessments were performed according to ACSM guidelines
participants that completed the study and those that dropped
(American College of Sports Medicine, 2013). Calipers (Lafayette
out, those that completed had higher ‘‘sit and reach’’ scores (29.7
Instruments, Lafayette IN) measured the skinfold tissue in mm
versus 25.4, p ¼ 0.046), (data not shown). This overall group
with duplicate measurements taken at each site. Unless contra-
difference in flexibility was consistent for the YE participants that
indicated by lymphedema, recent surgery, or participant prefer-
completed versus those that dropped out, (28.7 versus 21.7,
ence, all measurements were taken on the right side of the body.
p ¼ 0.009). For the CE group ‘‘sit and reach’’ was not different;
Skin fold measurements were summed. Body density (Db) and
however, lower BMI (28.1 versus 34.2, p ¼ 0.041), better
% body fat were calculated using ACSM-recommended formulas
‘‘forward reach’’ (38.4 versus 33, p ¼ 0.023), and higher left
(Table 4.4) (American College of Sports Medicine, 2013):
arm lateral ROM (170.0 versus 145.6, p ¼ 0.030) were different
between those that completed and those that did not. For the C
Db ¼ 1:099421  0:0009929 ðskinfold sumÞ group, there were no differences.
þ 0:0000023 ðskinfold sumÞ2 0:0001392 ðageÞ Descriptive results, tests for mean differences (‘‘pre’’ and
%body fat ¼ ð4:96=DbÞ  4:51 ‘‘post’’) and effect sizes specific to the YE group are shown in
Table 2. Participants improved in all outcome measures in the
expected direction with the exception of weight, cardiorespiratory
Arm volume was measured with a water displacement
capacity and systolic blood, with essentially no change in these
volumeter. Participants sat next to an arm volumeter
outcomes. Though weight remained essentially the same
(7’’  7’’  30’’) and slowly lowered their arm. The displaced
(+0.23 kg), significant improvements were seen in body compos-
water was collected and measured to calculate arm volume (ml).
ition with a reduction of % body fat, (3.00%, d ¼ 0.44,
In addition, Norman lymphedema self-report measures (Norman
p ¼ 0.001). Participants also improved in sit to stand leg strength
et al, 2001) were completed at baseline, every four weeks during
repetitions (2.05, d ¼ 0.48, p ¼ 0.003); forward reach (3.59 cm,
the intervention, and at the end of the intervention. Participants
d ¼ 0.61, p ¼ 0.01); and right arm sagittal PROM (6.50 , d ¼ 0.92,
were encouraged to immediately report any injuries incurred
p ¼ 0.05). Although not statistically significant, favorable small to
during exercise as well as any symptoms of hand, arm, and limb
moderate effect sizes occurred for diastolic blood pressure
change from the Norman self-report to the research staff and if
(d ¼ 0.20); arm strength (d ¼ 0.33); torso strength (d ¼ 0.28);
necessary seek medical attention.
right arm lateral PROM (d ¼ 0.49); and left arm sagittal PROM
(d ¼ 0.33).
Treatment of data
As can be seen in Table 3, when compared to the other groups,
All the analyses were performed using Statistical Package for the ‘‘forward reach’’ (a test of flexibility and balance) was signifi-
Social Sciences (version 21.0; IBM Corp., Armonk, NY). cantly different with YE participants outperforming C participants
Descriptive statistics were performed on all variables (range, (3.59 cm gained versus 2.44 cm lost), (p ¼ 0.009) and outper-
mean, standard deviation). Paired-sample ‘‘t-tests’’ were per- forming CE participants (3.59 cm gained versus 1.35 cm gained),
formed to compare ‘‘pre’’ and ‘‘post’’ values. Because we were but not statistically significant. Though not statistically signifi-
also interested in the magnitude of change for the YE participants, cant, other comparisons are noteworthy. All participants lost body
in addition to statistical significance, we calculated effect size as fat; however, the YE group lost the most with an average of 3.00%
ES ¼ (m1–m2)/s1 where m1 ¼ ‘‘pre’’ mean, m2 ¼ ‘‘post’’ mean with the CE group and C group losing 2.46% and 1.97%
and s1 ¼ ‘‘pre’’ standard deviation. Our original sample size respectively. Interestingly, though while losing the most % body
estimate was determined by logistics in how many participants fat, the YE group gained mass (0.23 kg), indicative of favorable
could be managed in each of the study arms given resource changes in body composition when compared to the other groups.
limitations. Our primary outcome variable was body composition The CE group, which had a specific aerobic training component
change (% body fat), as increased adiposity is associated with increased the most in VO2 (2.01%) while the YE group and C
breast cancer risk in post-menopausal women (McTiernan et al, group virtually maintained the same levels (0.77% and 1.01%
 456 D. C. Hughes et al. Physiother Theory Pract, 2015; 31(7): 451–460

Table 1. Participant characteristics at baseline, mean standard deviation or n (%).

Baseline characteristic All (N ¼ 94) YE (n ¼ 31) CE (n ¼ 31) C (n ¼ 32) p

Age 56.2 (7.9) 56.7 (9.6) 57.6 (6.6) 54.4 (7.0) 0.266
Comorbidity 2.3 (1.7) 2.1 (1.7) 2.1 (1.5) 2.7 (1.8) 0.323
BMI 28.8 (6.7) 29.1 (6.7) 29.1 (6.2) 28.1 (7.3) 0.810
VO2max 19.8 (5.1) 20.2 (5.6) 19.2 (4.9) 19.9 (5.0) 0.737
Lymphedema
Yes 19 (20%) 5 (16%) 6 (19%) 8 (25%)
No 72 (77%) 25 (81%) 25 (81%) 22 (69%)
Missing 3 (37%) 1 (3%) 1 (3%) 2 (6%)
Ethnicity
Hispanic 30 (32%) 10 (32%) 7 (23%) 13 (41%)
Non-hispanic 63 (67%) 21 (68%) 24 (77%) 18 (56%)
Missing 1 (1%) 1 (1%)
Race
White 75 (79%) 26 (84%) 25 (81%) 24 (75%)
African American 5 (5%) – 2 (6%) 3 (9%)
Asian 1 (5%) 1 (5%) – –
Other 11 (11%) 4 (13%) 3 (10%) 4 (12%)
Missing 2 (2%) – 1 (3%) 1 (3%)
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Education
High school diploma 8 (8%) 3 (10%) 2 (6%) 3 (9%)
Technical 3 (3%) 3 (10%) – –
Some college 23 (25%) 7 (23%) 7 (23%) 9 (28%)
Bachelor’s degree 26 (28%) 10 (32%) 9 (29%) 7 (22%)
Master’s degree 28 (30%) 6 (19%) 10 (32%) 12 (38%)
Terminal degree (e.g. MD, PhD) 4 (4%) 2 (6%) 2 (6%) –
Missing 2 (2%) – 1 (3%) 1 (3%)
Employment status
Employed full time 46 (49%) 14 (45%) 15 (48%) 17 (53%)
Employed part time 8 (8%) 1 (3%) 5 (16%) 2 (6%)
Not working but seeking 2 (2%) 2 (6%) – –
Not working not seeking 1 (1%) – – 1 (3%)
Retired 22 (23%) 8 (26%) 8 (26%) 6 (19%)
Homemaker 13 (13%) 6 (19%) 3 (10%) 4 (13%)
Volunteer 1 (1%) – – 1 (3%)
Missing 1 (1%) – – 1 (3%)

Total % may not add up to 100% due to rounding. YE ¼ Yoga-based exercise group; CE ¼ Comprehensive exercise group; C ¼ Comparison group.

Table 2. Descriptive statistics for yoga group physical fitness/functioning outcomes, n ¼ 20.

Pre Post Expected Change (95%CI)*

Fitness/Functioning Pre range mean (SD) Post range mean (SD) direction p score change ES**
Weight (kg) 54.6–102.1 74.6 (14.8) 55.8–97.8 74.8 (14.8) Decrease 0.766 0.23 (1.34, 1.79) 0.02
BMI (kg/m2) 19.9–40.5 28.8 (6.5) 20.1–39.9 28.8 (6.0) Decrease 0.942 0.03 (0.79, 0.85) 0.00
Body adiposity (% body fat) 18.1–43.4 34.0 (6.8) 18.1–41.2 31.0 (6.5) Decrease 50.001 3.00 (4.50, –1.50) 0.44
Resting heart rate (bpm) 51.0–99.0 68.6 (13.0) 43.0–118.0 70.0 (17.6) Decrease 0.718 1.35 (6.36, 9.06) 0.10
Systolic blood pressure (mm Hg) 110.0–160.0 126.6 (14.8) 108.0–152.0 127.6 (13.3) Decrease 0.978 0.11 (7.87, 8.08) 0.01
Diastolic blood pressure (mm Hg) 62.0–108.0 81.4 (9.8) 60.0–108.0 79.8 (10.3) Decrease 0.551 1.95 (8.67, 4.78) 0.20
Predicted VO2max (mlO2/kg/min) 10.4–33.6 21.9 (6.1) 15.9–26.2 21.2 (3.4) Increase 0.530 0.77 (3.31, 1.77) 0.13
Arm strength (kg) 13.0–39.0 22.2 (7.0) 12.0–46.0 24.7 (7.7) Increase 0.208 2.31 (1.42, 6.03) 0.33
Shoulder strength (kg) 26.0–47.0 33.0 (5.7) 14.0–46.0 32.4 (7.7) Increase 0.651 0.78 (4.34, 2.79) 0.14
Torso strength (kg) 32.0–64.0 46.4 (8.9) 21.0–68.0 49.7 (14.2) Increase 0.515 2.53 (5.60, 10.67) 0.28
Sit to stand (repetitions) 8.0–25.0 13.7 (4.3) 11.0–27.0 15.8 (3.9) Increase 0.003 2.05 (0.79, 3.31) 0.48
Sit and reach (cm) 17.5–37.5 28.7 (6.0) 13.0–45.0 29.1 (7.8) Increase 0.313 0.85 (0.87, 2.56) 0.14
Forward reach (cm) 24.5–48.0 34.6 (5.9) 25.5–54.0 38.2 (6.7) Increase 0.011 3.59 (0.92, 6.26) 0.61
Arm range of motion
Right arm sagittal 160.0–182.0 171.4 (7.1) 160.0–196.0 177.8 (11.1) Increase 0.05 6.50 (0.22, 13.22) 0.92
Right arm lateral 146.0–190.0 167.8 (11.3) 140.0–190.0 173.4 (12.3) Increase 0.10 5.55 (1.17, 12.27) 0.49
Left arm sagittal 150.0–180.0 167.8 (8.8) 150.0–188.0 170.4 (10.1) Increase 0.293 2.90 (2.71, 8.51) 0.33
Left arm lateral 150.0–180.0 168.0 (9.0) 138.0–186.0 167.2 (13.5) Increase 0.809 0.70 (6.69, 5.29) 0.08
Arm volume
Right arm 1390–3080 1917.4 (470.9) 1360–2840 1942.2 (395.0) – 0.771 24.8 (151.2, 200.8) 0.05
Left arm 1240–3190 1915.5 (513.9) 1230–2930 1992.4 (514.1) – 0.173 76.8 (36.7, 190.5) 0.15

*95% Confidence interval of the mean change score.

**ES ¼ effect size ¼ (‘‘post’’ mean - ‘‘pre’’ mean)/standard deviation of ‘‘pre’’ score.
 DOI: 10.3109/09593985.2015.1037409 Yoga and fitness outcomes 457
Table 3. Differences between groups change score (post minus pre) ANOVA.

All (n ¼ 72) YE (n ¼ 20) CE (n ¼ 26) C (n ¼ 26) Expected

Fitness/Functioning Mean (SD) Mean (SD) Mean (SD) Mean (SD) direction p Post-hoc
Weight (kg) 0.09 (2.83) 0.23 (3.35) 0.65 (2.91) 0.20 (2.29) Decrease 0.479
BMI (kg/m2) 0.02 (1.30) 0.03 (1.75) 0.14 (1.27) 0.06 (0.91) Decrease 0.838
Body adiposity (% body fat) 2.43 (3.11) 3.00 (3.21) 2.46 (3.05) 1.97 (3.14) Decrease 0.540
Resting heart rate (bpm) 3.83 (12.33) 1.35 (16.46) 4.80 (10.32) 4.81 (10.50) Decrease 0.576
Systolic blood pressure (mm Hg) 0.43 (14.95) 0.11 (16.56) 2.46 (11.54) 3.35 (16.48) Decrease 0.394
Diastolic blood pressure (mm Hg) 0.17 (9.92) 1.95 (13.95) 2.38 ( 8.96) 1.23 (6.60) Decrease 0.292
Predicted VO2max (mlO2/kg/min) 0.87 (4.56) 0.77 (5.11) 2.01 (3.45) 1.01 (4.85) Increase 0.151
Arm strength (kg) 1.71 ( 9.91) 2.31 (7.48) 2.57 (11.95) 0.54 ( 9.65) Increase 0.747
Shoulder strength (kg) 0.03 (7.02) 0.78 (7.17) 0.96 ( 5.92) 0.38 (7.93) Increase 0.702
Torso strength (kg) 2.81 (16.58) 2.53 (14.69) 0.09 (15.41) 5.42 (18.63) Increase 0.524
Sit to stand (repetitions) 2.45 ( 3.16) 2.05 ( 2.68) 2.70 ( 3.22) 2.54 ( 3.51) Increase 0.792
Sit and reach (cm) 1.11 (3.54) 0.85 (3.56) 1.66 (3.50) 0.79 (3.64) Increase 0.649
Forward reach (cm) 0.58 (6.93) 3.59 (5.71) 1.35 (6.75) 2.44 (6.97) Increase 0.009 YE4C
Arm range of motion
Right arm sagittal 5.56 (12.55) 6.50 (14.35) 6.04 (10.78) 4.38 (12.98) Increase 0.833
Right arm lateral 4.06 (13.09) 5.55 (13.09) 3.04 (12.93) 3.85 (12.64) Increase 0.819
Left arm sagittal 5.51 (13.58) 2.90 (12.00) 9.08 (15.92) 4.23 (12.13) Increase 0.272
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Left arm lateral 0.51 (13.09) 0.70 (12.79) 0.70 (13.49) 2.50 (13.21) Increase 0.623
Arm volume
Right arm 70.2 (292.9) 24.8 (376.1) 94.0 (233.1) 82.31 (279.7) — 0.714
Left arm 46.2 (269.0) 76.8 (242.7) 16.7 (302.2) 50.96 (261.7) — 0.758

YE ¼ Yoga-based exercise group; CE ¼ Comprehensive exercise group; C ¼ Comparison group.

respectively), although the differences were not statistically movement, higher body fatness, and the lower aerobic and
significant. strength conditioning characteristic of post-treatment breast
cancer survivors.
Consistent with other studies with yoga and breast cancer
Discussion
survivors, we saw improvements in physical functioning (Bower
Overwhelming evidence continues to demonstrate the benefits of et al, 2012; Chandwani et al, 2010; Culos-Reed, Carlson, Daroux,
exercise on reducing morbidity and mortality while improving and Hately-Aldous, 2006; Littman et al, 2012; Van Puymbroeck,
individual quality of life and overall health (Blair et al, 1989; Schmid, Shinew, and Hsieh, 2011) for the YE group.
Haskell et al, 2007; Lichtenstein et al, 2006; Schmitz et al, 2010b; Participation in the trial was also associated with improvements
United States Department of Health and Human Services, 1996; in body composition (body fat loss of 3%) for the YE group, who
United States Department of Health and Human Services, 2008). of the three groups had the most favorable change in body
These benefits apply to cancer survivors as well (Beasley et al, composition. This is consistent with Littman et al. (2012) six-
2012; Doyle et al, 2006; Holmes et al, 2005; Schmitz et al, 2010b; month study where yoga participants had a significant favorable
Speck et al, 2010). Adopting and maintaining a physically active change in waist circumference compared to a wait list control.
lifestyle improves cancer survivors’ well-being (Courneya, 2003), Similar to our results, these participants also did not lose weight
and reduces their risk of: cardiovascular disease (LaCroix et al, (Littman et al, 2012). The change in body composition for our
1996); noninsulin-dependent diabetes mellitus (Helmrich, participants is important to note as obesity and obesity-associated
Ragland, Leung, and Paffenbarger, 1991); osteoporosis endocrine output has been associated with breast cancer recur-
(Devogelaer and de Deuxchaisnes, 1993); and recurrent cancers rence risk (Chen et al, 2010; Demark-Wahnefried et al, 2012;
(Friedenreich and Rohan 1995; Giovannucci et al, 1995). Gilbert and Slingerland, 2013; Morimoto et al, 2002; Simpson
However, cancer survivors tend to decrease their level of physical and Brown, 2013). Some studies suggest that the association of
activity after diagnosis and mostly never regain their former levels the physical activities’ effect on biological markers associated
after treatment (Courneya and Friedenreich, 1997; Irwin et al, with breast cancer risk may not only be the direct effect from
2003; Irwin et al, 2004). activity but also the result of a favorable effect on managing/
Thus, the need for exercise activities that engage breast reducing obesity (Ballard-Barbash et al, 2012; Irwin et al, 2005;
cancer survivors is urgent. Moreover, the design of exercise Irwin et al, 2011; McTiernan, 2008; McTiernan et al, 2003a
activities specifically modified for the often compromised 2003b; McTiernan et al, 2006). Since the weight stayed virtually
physical functioning of post-treatment breast cancer survivors the same in our YE participants (+ 0.23 kg), the loss in body fat
is critical. The specificity of the design of a program could offer probably translated to a gain in lean mass, though without better
the potential to optimize the outcomes. In addition to aerobic assessment techniques (e.g. dual-energy x-ray absorptiometry) we
and/or resistance exercise programs, yoga-based programs are cannot be certain.
starting to be used for the welfare of this population. Here we Our protocol specifically used participants’ body weight for
reported on the successful fitness and physical functioning resistance training so the YE participants also performed resist-
results of 20 post-treatment breast cancer survivors who safely ance training though probably not in the same manner as the other
completed a six-month structured Hatha yoga-based exercise trial groups. This mixed results in strength outcomes between groups
and compared their results to groups randomized to ‘conven- we observed is consistent with results from Van Puymbroeck et al.
tional’ comprehensive exercise (aerobic, resistance, flexibility) or (2011) where in 8 weeks of yoga, yoga participants increased
a comparison group who chose their form of exercise. The yoga- upper and lower body strength and flexibility while a ‘light
based program took into account the potential limitations of limb exercise’ group improved in abdominal strength. As we expected
 458 D. C. Hughes et al. Physiother Theory Pract, 2015; 31(7): 451–460

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