Effects of Inspiratory Muscle Training and Yoga.4

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Research Report

Effects of Inspiratory Muscle Training and Yoga


Breathing Exercises on Respiratory Muscle
Function in Institutionalized Frail Older
Adults: A Randomized Controlled Trial
Maria dels ngels Cebri i Iranzo, PT, PhD1,2; David Alan Arnall, PT, PhD3;
Celedonia Igual Camacho, PT, PhD1,4; Jos Manuel Toms, PhD5
ABSTRACT
Background: In older adults, respiratory function may be seriously compromised when a marked decrease of respiratory
muscle (RM) strength coexists with comorbidity and activity limitation. Respiratory muscle training has been widely
studied and recommended as a treatment option for people
who are unable to participate in whole-body exercise training
(WBET); however, the effects of inspiratory muscle training and yoga breathing exercises on RM function remain
unknown, specifically in impaired older adults.
Purpose: To evaluate the effects of inspiratory threshold training (ITT) and yoga respiratory training (YRT) on RM function
in institutionalized frail older adults.
Methods: Eighty-one residents (90% women; mean age, 85
years), who were unable to perform WBET (inability to independently walk more than 10 m), were randomly assigned to
a control group or one of the 2 experimental groups (ITT or
YRT). Experimental groups performed a supervised intervalbased training protocol, either through threshold inspiratory
muscle training device or yoga breathing exercises, which
lasted 6 weeks (5 days per week). Outcome measures were
collected at 4 time points (pretraining, intermediate, posttraining, and follow-up) and included the maximum respiratory
pressures (maximum inspiratory pressure [MIP] and maximum expiratory pressure [MEP]) and the maximum voluntary
ventilation (MVV).

Results: Seventy-one residents completed the study: control


(n = 24); ITT (n = 23); YRT (n = 24). The treatment on had
a significant effect on MIP YRT (F6,204 = 6.755, P < .001,
2 = 0.166), MEP (F6,204= 4.257, P < .001, 2 = 0.111),
and MVV (F6,204= 5.322, P < .001, 2= 0.135). Analyses
showed that the YRT group had a greater increase of RM
strength (MIP and MEP) and endurance (MVV) than control
and/or ITT groups.
Conclusion: Yoga respiratory training appears to be an effective and well-tolerated exercise regimen in frail older adults
and may therefore be a useful alternative to ITT or no training,
to improve RM function in older population, when WBET is
not possible.
Key Words: frail older adult, IMT, respiratory muscle function,
yoga
(J Geriatr Phys Ther 2014;37:65-75.)

INTRODUCTION

DOI: 10.1519/JPT.0b013e31829938bb

With aging, respiratory muscle (RM) strength decreases


over time.1 The loss of RM strength is due in large part
to geometric changes in the thoracic cage, the reduction
of costovertebral joint mobility, the degradation of neuromuscular recruitment patterns, as well as the loss of muscle
fiber-type (sarcopenia).1,2 Hence, maximum respiratory
pressures decline with aging and become critically low in
the eighth and ninth decades.3 When this decline in RM
strength is complicated by the onset of comorbidities such
as stroke, myocardial infarction, severe musculoskeletal
problems, or dementia, an older adult will often require
professional long-term care and, in most cases, institutionalization.4 The loss of RM strength (declining maximum
respiratory pressures) in addition to all of the changes due
to the presence of different diseases create a scenario of a
downward spiral, as inferred by declining mobility and the
loss of tolerance for physical activity. Respiratory muscle
can be strengthened with regular physical activity,5 and
consequently whole-body exercise training as well as activities of daily living are directly linked with the improvement
or maintenance of RM function.3,4 However, in frail older
adults who are lacking in general strength, whole-body
physical conditioning is rarely possible.6 Therefore, if older

Journal of GERIATRIC Physical Therapy

65

1Department of Physiotherapy, University of Valencia,


Valencia, Spain.
2Cardiopulmonary Rehabilitation Service, University
Hospital La Fe, Valencia, Spain.
3Physical Therapy Department, East Tennessee State
University, Johnson City, Tenessee, USA.
4Musculoskeletal Rehabilitation Service, Clinic University
Hospital of Valencia, Spain.
5Department of Behavioral Sciences Methodology,
University of Valencia, Valencia, Spain.
Preliminary results reflected in this article have been presented at the 8th World Congress on Active Aging; August
13-17, 2012; Glasgow, Scotland.
The authors declare no conflicts of interest.
Address correspondence to: Maria dels ngels Cebri i
Iranzo, PT, PhD, Department of Physiotherapy, University
of Valencia, C. Gasc Oliag, 5, 46010 Valencia, Spain
(angeles.cebria@uv.es).

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Research Report
adults are unable to undergo whole-body exercise training
(eg, walking) because of comorbid conditions, specific RM
strength training is a useful alternative training method to
prevent the clinical deterioration in this population with
disabilities who are susceptible to disease.7-10
One of the most common techniques used for RM
strengthening is respiratory threshold loading.11-12
Inspiratory threshold loading devices (eg, Threshold IMT;
Respironics HealthScan Inc, Cedar Grove, New Jersey) have
emerged as a simple, relatively and an effective method
to increase inspiratory muscle strength and endurance,
independent of breathing pattern.10 Gosselink13 noted
an additional advantagethe threshold loading device
shortens inspiratory time and increases time for exhalation
and relaxation, which could delay the onset of inspiratory
muscle fatigue. Several studies have investigated the effect
of threshold inspiratory muscle training (IMT) devices in
healthy participants14,15 and in participants with respiratory, neuromuscular, and cardiovascular diseases.16-19 A
recent meta-analysis20 concluded that people with more
advanced weakness benefit more than those with less severe
disease. However, none of these studies incorporated institutionalized frail older adults in their cohorts.
Yoga breathing exercises (Pranayama) are less
commonly used for RM strength training. Pranayama
combines the inspiration and expiration through one or
both nostrils, controls the time of the breathing cycle,
and requires an activation of chest and abdomen RMs.21
Most studies22-25 evaluate comprehensive yoga programs,
including (a) physical postures or Asanas; (b) different
methods of timed breathing or Pranayama; and (c) meditation sessions. Only 2 previous studies assessed the effect
of yoga breathing exercises on RM strength, showing a
significant increase in maximum respiratory pressures, one
in a healthy young population26 and one in a healthy older
population.27
However, there is a complete paucity of literature on
the training effects of yoga breathing exercises on RM
strength in institutionalized frail older adults. Therefore,
the purpose of the study was to evaluate the effects of
inspiratory threshold training (ITT) and yoga respiratory
training (YRT) on RM function in institutionalized frail
older adults. The hypothesis was that both RM training
programs (ITT and YRT) would improve RM strength
and endurance when compared with the control group in
institutionalized frail older population.

METHODS
Design
This was an open-label randomized controlled trial in
which 81 residents with activity limitation were allocated
into 3 balanced groups: 1 control group and 2 training
groups (ITT and YRT). The trained participants performed
66

a 6-week supervised RM training program and did not


perform other forms of exercise training. The control
group did not participate in any form of training during the
study period. This study was approved by the University
of Valencia ethics committee for human research, was performed within 2008 and 2009, and has been registered in
the ClinicalTrials.gov (NCT ID: NCT01624272).

Setting and Participants


The sample was made up of all eligible older adults from
4 nursing homes located in Valencia, Spain. The included
nursing homes met similar criteria to classify the residents
and similar professional health services. A flow diagram
(Figure 1) describes the participant eligibility and randomization of the population who met the following inclusion
criteria: (1) older than 65 years; (2) medically stable; and
(3) a Mini-Mental State Examination score of 21 points or
greater28,29 to assess the level of cognitive function (participants without moderate or severe cognitive deterioration
to assure their proper collaboration in assessment and
training processes). Exclusion criteria for the participants
were (1) ability to independently walk more than 10 m; (2)
chronic pulmonary disease; (3) any acute cardiorespiratory
episode within 2 months before the study; (4) muscular,
neurological, or neuromuscular disease that could interfere
in the proper performance of assessment and/or training protocols; (5) smoking for short term or within the
last 5 years before the study; and (6) a terminal disease
diagnosis. All participants were informed of the risks and
benefits of the study and agreed to participate by signing
a consent form.
In sum, the sample was characterized by individuals
spending a great deal of their time sitting and lying down,
though some walked short distances between rooms (bed
room, dining room, bath room, etc). None of the participants left the nursing home for walks (38% used a
wheelchair for displacements inside the nursing home, and
62% were unable to independently walk >10 m). Physical
functioning and participation in daily activities were not
therefore considered as outcomes.

Randomization and Interventions


The recruitment strategies were as follows (Figure 1): first,
the research group members (coordinators) selected the nursing homes according to their location (metropolitan area of
Valencia) and similar standards (eg, residents admission and
classification criteria, offered services, professional health
qualifications) to guarantee the same quality of care; second,
health care professionals specialized in geriatrics (a physician and a psychologist per nursing home) selected the older
people who met the inclusion criteria mentioned earlier; and
third, the same health care professionals identified diagnosed
diseases and other circumstances that would exclude the
potential participants from the study. Nursing home health
care professionals exclusively conducted the recruitment
Volume 37 Number 2 April-June 2014

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Research Report

Figure 1. Enrollment, intervention allocation, follow-up, and data analysis, according with updated guidelines for reporting parallel
group randomized trials. IMT indicates inspiratory muscle training; ITT, inspiratory threshold training; max, maximum; min,
minimum; YRT, yoga respiratory training.

process following the manual of procedures developed by the


research group, but they were not involved in any other tasks
related to the study.
Then, participants were randomly allocated to 1 of 3
groups: control (n = 27), ITT (n = 27), and YRT (n =
27). A statistician who had no contact with the participants
and/or the health care professionals who undertook the
measurements and the intervention performed the random
allocation sequence (random number generator in SPSS;
SPSS, Inc, Chicago, Illinois).

Outcomes and Follow-up


All participants were measured at 4 intervals: at baseline
(T1) and at the end of week 3 (T2), week 6 (T3), and week
9 (T4). Baseline measurements covered demographic characteristics, lung function and RM function, functional and
cognitive capacity, and diagnosed diseases. In addition,
primary outcomes (maximum inspiratory and expiratory
pressures) and secondary outcome (maximum voluntary
ventilation [MVV]) were assessed at the 4 time points by a
physical therapist not involved in any of the training protocols (ITT or YRT).
Pulmonary volumes and capacities were measured
according to the standards published by the American
Journal of GERIATRIC Physical Therapy

Thoracic Society30: Slow vital capacity, forced vital capacity, forced expiratory volume in the first second, peak
inspiratory flow, peak expiratory flow, and MVV were collected by using a Jaeger spirometer (Flow Screen; VIASYS
Healthcare GmbBH, Hoechberg, Germany). For RM function, a pressure gauge (Series 2000 Magnehelic Pressure
Gauge; Dwyer Instruments, Michigan City, Indiana) was
used to measure maximum inspiratory pressure (MIP) and
maximum expiratory pressure (MEP), in accordance with
the standards required by the American Thoracic Society.31
The reference values used to obtain the percentage of the
predicted values were those reported by Enright et al32 and
Neder et al33 for MIP-MEP and MVV, respectively.

Testing Sessions
The control group underwent no training but did undergo
pulmonary testing at all scheduled time periods (T1 through
T4). After the initial baseline testing (T1), the ITT and YRT
groups began training for two 3-week blocks of time for
5 days per week, followed by a 3-week follow-up period
(T4) in which no training took place. T4 was a testing
period to determine whether there was carry-over in the
training effects. At the end of each 3-week block (T2, T3,
T4), all participants underwent repeat pulmonary testing.
67

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Training Protocols
Inspiratory threshold training and YRT shared common
features, among them were (1) supervised on a daily basis;
(2) performed in groups of 8 to 10 residents; (3) intervalbased programs consisting of 7 cycles of 2-minute work
and 1-minute rest (this protocol is published as a practical guide for clinicians by Hill et al.10); (4) sessions took
place 5 times per week over a 6-week period, for a total
of 30 morning sessions; (5) 2-day familiarization period
at the beginning of the protocol, to reduce naivete and
increase performance compliance; and (6) safety of training
protocols was monitored, using a pulseoximeter (SmartOx
WM18000; Weinmann Medical Technology, Hamburg,
Germany), before and immediately after the training session. Participants who participated in less than 80% of the
sessions in both programs were dropped from the analyses.
In the same way as for the recruitment process, the intervention counted with a manual of procedures that guided
the physical therapists during the training sessions in the
different nursing homes.
The specific features of the ITT were as follows:
(1) The Threshold IMT device is an adjustable springloaded negative pressure breathing device in which the
person must exert a sufficient inspiratory effort to open
the valve and allow air to pass through the device to the
lungs. (2) The working range of pressures is from 7 to 41
cm H2O. (3) Participants were permitted to select their own
breathing pattern, and expiration was unloaded.10 The
interval-based program consisted of 7 cycles of 2-minute
work and 1-minute rest (intervention details are available
on request). As a starting point for the first period of training (weeks 1-3), the participants breathed against a load
30% to 50% of their own baseline MIP value (this load is
recommended by Gosselink13 and Hill et al10). During this
period, the load was progressed every 2 days, according to
the participant's tolerance. The T2 MIP value was used to
readjust the inspiratory load of each participant to ensure
that the participants were training at optimal loads for the
second period of training (weeks 4-6). Similarly, the load
was increased according to the participant's tolerance.
Two trained physical therapists supervised each session
and kept activity journals, recording the participant's
increases in inspiratory load (cm H2O) and the relative
difficulty of breathing for each session, using the 0- to
10-point Borg Scale.34
The specific features of the YRT were as follows:
(1) The weekly program of breathing exercises was developed by a master yoga instructor (Yoga Siromani) and was
easily reproducible by trained physical therapists (intervention details are available on request). (2) Increasing the
complexity of the exercises over time to encourage a training effect incorporated principles of increasing repetitions
of the exercise, increasing resistance by alternating the exercises (breathing through both nostrils or alternative-nostril
breathing) and the timing of the breathing cycle (inspiration:
68

apnea postinspiration: expiration: apnea postexpiration),


and performing an active expiration in all cases. Similarly,
2 physical therapists kept activity journals, recording the
participants breathing difficulty by using the 0- to 10-point
Borg scale.34 The yoga respiratory protocol was centered
on rhythmic slow, deep, and nostril breathing, not including Yogasanas and meditation, as described in most yoga
studies.22-25

Statistical Analyses
Data analyses were conducted by using SPSS 19. Descriptive
statistics were calculated for all variables and are reported as
mean (1 SD) for quantitative variables and percentages for
qualitative variables. Normality as well as other statistical
assumptions was tested, and outliers identified before using
data-modeling techniques. Variables were all screened for
normality and outliers by graphical and statistical means,
q-q plots, and Kolmogorov-Smirnov tests for normality,
box and whiskers graphs, and z scores (> 3) for outliers,
the methods recommended in the statistical literature.35
Inferential statistics were used to test for statistically
significant effects among the variables in the study. Baseline
levels on the variables of interest were compared across the
3 groups by means of analysis of variance (ANOVA) (for
quantitative dependent variables) or chi-square tests (for
qualitative dependent variables), depending on the nature
of the variables. ANOVA 3 (group) 4 (time) were used
to analyze the dependent variables in the randomized clinical trial. Effect size was measured with partial eta-squared
measures (2). Results were considered significant if P <
.05. Follow-up simple effects for the interactions were
performed with Bonferroni adjustments. In addition, nonparametric (Kruskal-Wallis) tests were used to compare the
number of comorbidities across groups.
No reliable estimates of expected effect sizes in the
context of frail older adults for both treatments existed.
Therefore, a priori calculation of sample size was not possible, and sample size was determined, as such groups were
always larger than those used in the previous literature on
both treatments.

RESULTS
Participants, Compliance, and Dropout
A pool of 355 residents files was screened from the database
of the 4 nursing homes (Figure 1); 81 residents were randomly placed into 1 of the 3 groups, resulting in the 3 balanced
groups of 27 participants. Ten participants were lost to
follow-up: (a) 3 residents died during the study because of
exacerbations of their chronic diseases, and 1 resident died
during hospitalization stay after a fall; (b) 2 residents were
excluded from analysis because of discontinued intervention;
(c) 1 resident dropped voluntarily out of the intervention;
and (d) 3 residents needed rest because of exacerbations of
their chronic diseases.
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Research Report
No significant difference (P .351) was found in the
total number of sessions attended by participants from
both experimental groups: ITT group, 24.8 (3.0) sessions
(95% confidence interval [CI], 23.5-26.1); YRT group,
24.9 (3.6) sessions (95% CI, 23.3-25.5).

Baseline Characteristics
No significant differences for variables between the 3 groups
were found, except for the variable height and functional
and cognitive capacity (Table 1). Regarding RM function,
the values were less than predicted in the complete sample
(MIP, 69%; MEP, 59%; MVV, 36%). In the case of the
predicted values of MVV (% predicted), however, it must be
borne in mind that only 15 of 71 cases (those younger than
80 years) took part in this analysis, and as a consequence,
there may be a large bias in this particular statistics (reference
values by Neder et al33). For this reason, this variable (MVV,
% predicted) was excluded from analyses.
Moreover, 17% of the participants were former smokers (control, n = 3; ITT, n = 7; YRT, n = 2; P = .101).
None of the participants (nonsmokers and former smokers)
were treated with oxygen to maintain their oxygen saturation (SpO2 94%) during the time the study progressed.
The high prevalence of morbidity was due to cardiovascular and degenerative skeletal diseases (Table 1). The
other frequent-diagnosed diseases were blindness, deafness, overweight, stroke, and diabetes mellitus sequelae
(spasticity, wounds, and amputations).

Effects of Training Protocols on Primary Outcomes


The mixed-factorial ANOVA on MIP, in absolute values
(Figure 2), found both a significant time effect (F3,204 = 40.449,
P < .001, 2 = 0.373) and a group effect (F2,68 = 3.465, P =
.037, 2 = 0.092). The treatment effect showed up in a significant interaction effect (F6,204 = 6.755, P < .001, 2 =
0.166). A second ANOVA on MIP, in percentage values, was
performed. The main effects results show a significant time
effect (F3,204 = 38.107, P < .001, 2 = 0.359). Group effect
was also statistically significant (F2,68 = 5.512, P = .006,
2 = 0.140). The statistically significant interaction effect
shows again the effectiveness of treatment (F6,204 = 6.774,
P < .001, 2 = 0.166), in line with the results already commented for the absolute values of MIP (Table 2).
Follow-up analyses (simple interaction effects, with
Bonferroni adjustment of error I and its CIs) showed an
increase of MIP means from baseline testing in the 3 groups
(Table 2). However, the YRT group showed a significantly
greater increase of inspiratory muscle strength than control
and ITT groups. After 6 weeks of training and 3 weeks
of nonintervention, the MIP in the YRT group was significantly larger than in the other 2 groups, while ITT and
control did not significantly differ.
For the MEP, in absolute values (Figure 3), the results
of main effects showed a significant time effect (F3, 204 =
53.903, P < .001, 2 = 0.442), as well as a group effect
Journal of GERIATRIC Physical Therapy

Figure 2. Maximum inspiratory pressure absolute values


(cm H2O) for each group and time point: means and
standard errors bars (SD). ITT indicates inspiratory
threshold training; YRT, yoga respiratory training.

(F2,68 = 5.112, P = .009, 2 = 0.131). The statistically significant interaction effect demonstrated the effectiveness of
treatment (F6,204= 4.257, P < .001, 2 = 0.111). Another
ANOVA on MEP, in percentage values, was estimated. The
main effects were both significant: a time effect (F3,204 =
54.228, P < .001, 2 = 0.444) and a group effect (F2,68=
6.701, P = .002, 2 = 0.165). The interaction effect was
also statistically significant (F6,204 = 5.048, P < .001, 2 =
0.129), in line with the results already commented for the
MEP absolute values. Interactions simple effects (Table 2)
showed equal means (P > .05) of MEP in the first assessment and significant differences from the intermediate

Figure 3. Maximum expiratory pressure absolute values


(cm H2O) for each group and time point: means and
standard errors bars (SD). ITT indicates inspiratory
threshold training; YRT, yoga respiratory training.
69

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Research Report
Table 1. Baseline Characteristics for Each Group: Mean (SD) and 95% Confidence Intervals Shown in Parentheses
Characteristics

Control (n = 24)

ITT (n = 23)

YRT (n = 24)

.12

Demographics
Sex, men/women
Age, y

3/21

4/19

0/24

5.9 (5.1)

83.6 (8.2)

84.0 (6.8)

(83.8-88.1)

(80.1-87.1)

(81.2-86.9)

.46
Weight, kg

65.0 (11.7)

65.9 (14.1)

65.2 (12.8)

(60.1-70.0)

(59.8-72.0)

(59.8-70.6)

.97
Height, cm

149.1 (7.1)

155.5 (7.2)

151.4 (4.9)

(146.1-152.1)

(152.4-158.6)

(149.3-153.5)

29.2 (4.8)

27.2 (5.8)

28.5 (4.8)

(27.2-31.3)

(24.7-29.7)

(26.4-30.5)

.04
Body mass index, kg/m2

.39
Pulmonary function
Vital capacity, L

1.58 (0.49)

1.78 (0.53)

1.86 (0.44)

(1.37-1.79)

(1.56-2.02)

(1.67-2.04)

78 (18)

80 (21)

91 (22)

(70-87)

(70-89)

(80-101)

.14
Vital capacity, % predicted

.12
FVC, L

1.47 (0.44)

1.67 (0.52)

1.75 (0.41)

(1.29-1.66)

(1.44-1.89)

(1.58-1.92)

.10
FVC, % predicted

73 (19)

74 (19)

86 (21)

(64-82)

(65-83)

(76-95)

1.19 (0.38)

1.28 (0.44)

1.41 (0.38)

(1.02-1.35)

(1.09-1.47)

(1.25-1.57)

.08
FEV1, L

FEV1, % predicted

FEV1/FVC, %

Peak inspiratory flow, L/s

.16
81 (25)

77 (24)

94 (26)

(70-93)

(66-88)

(82-100)

.09
80 (10)

77 (11)

80 (9)

(76-85)

(72-82)

(76-83)

.43
1.97 (0.88)

1.79 (0.60)

2.19 (0.45)

(1.60-2.34)

(1.53-2.05)

(2.00-2.40)

2.77 (1.11)

3.11 (1.37)

3.39 (1.16)

(2.30-3.24)

(2.52-3.70)

(2.89-3.88)

73.8 (18.5)

60.2 (24.6)

75.0 (20.0)

(65.9-81.6)

(49.6-70.9)

(66.6-83.5)

.12
Peak expiratory flow, L/s

.22
Functional and cognitive capacity
Barthel Index (range, 0-100)a

.04
Mini-Mental State Examination (range, 0-30)b

23.0 (3.8)

23.8 (3.6)

26.8 (2.4)

(21.4-24.6)

(22.3-25.4)

(25.8-27.8)

Respiratory (yes)

29.2

34.8

25

.76

Cardiovascular (yes)

79.2

65.2

62.5

.41

<.001

Diagnosed diseases,c

Endocrine (yes)

33.3

34.8

33.3

.99

Neurological (yes)

29.2

47.8

20.8

.13

Skeletal (yes)

79.2

60.9

54.2

.17
.24

Other diseases (yes)


Comorbidity

70.8

87

87.5

3.2 (0.9)

3.3 (1.1)

2.8 (1.0)

(2.8-3.6)

(2.8-3.8)

(2.4-3.2)

.20d

Abbreviations: CI, confidence interval; FEV1, forced expiratory volume in the first second; FVC, forced vital capacity; ITT, inspiratory threshold training; YRT, yoga respiratory training; % predicted,
percentage of the reference value.
aValues are given as Mean (SD) and 95% Confiedence Intervals Shown in parentheses.43,44
bLower score means more cognitive impairment.29
cDiagnosed diseases (DD) section shows the percentages of DD presence and the means of DD number (comorbidity).
dThis significance test is a H-Kruskal-Wallis test to compare the 3 groups analyzed.

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36.3 (14.3)
(30.11-42.5)
37.6 (15.7)
(30.8-44.4)

37.3 (20.2)
(28.8-45.8)

34.8 (22.0)
(25.5-44.1)

Week 6 (T3)

Week 9 (T4)

76 (35)
(62-91)

83 (36)
(67-98)

77 (41)
(60-94)

Week 3 (T2)

Week 6 (T3)

Week 9 (T4)

61.3 (27.4)
(49.7-72.8)

67.3 (27.6)
(55.6-79)

62.3 (34.9)
(47.6-77.0)

Week 3 (T2)

Week 6 (T3)

Week 9 (T4)

54 (21)
(44.6-62.4)

63 (22)
(54-72)

Week 0 (T1)

Week 3 (T2)

MEP, % predicteda

52.1 (24.0)
(42.0-62.2)

Week 0 (T1)

MEP, cm H2O

68 (33)
(54-81)

Week 0 (T1)

70 (27)
(58-82)

57 (25)
(45.8-67.6)

75.0 (27.9)
(62.9-87.1)

74.8 (26.9)
(63.1-86.0)

70.9 (25.7)
(59.7-82.0)

57.6 (23.1)
(47.6-67.6)

81 (37)
(65-97)

79 (34)
(64-93)

69 (27)
(57-81)

64 (26)
(53-76)

32.0 (12.3)
(26.6-37.3)

34.8 (21.2)
(25.8-43.8)

Week 3 (T2)

MIP, % predicteda

29.6 (10.8)
(24.9-34.2)

ITT (n = 23)

30.8 (19.7)
(22.5-39.1)

Control (n = 24)

Week 0 (T1)

MIP, cm H2O

Variables by Time Points

Unadjusted Mean Outcomes, (SD) and (95% CI)

90 (32)
(76-103)

67 (28)
(55.7-78.8)

96.0 (30.6)
(83.1-101.3)

92.9 (30.6)
(80.0-102)

86.3 (30.1)
(73.6-98.9)

64.4 (26.2)
(53.3-75.4)

117 (44)
(96-115)

115 (43)
(97-115)

105 (45)
(86-110)

75 (32)
(62-89)

51.3
(18.5) (43.4-57.1)

50.4 (18.1)
(42.8-58.0)

45.8 (19.5)
(37.6-54.1)

33.3 (14.2)
(27.3-39.3)

YRT (n = 24)

ITT vs Control

>.05

4.01
(30.89 to 22.86)

7.02
(12.64 to 26.77)

3.20
(14.49 to 20.90)

12.71
(9.72 to 35.13)

7.49
(12.88 to 27.87)

9.62
(10.30 to 29.54)

5.53
(11.99 to 23.04)

>.05

>.05

>.05

>.05

>.05

>.05

>.05

>.05

7.64
(33.81 to 18.53)

4.42
(24.62 to 33.45)

>.05

>.05

>.05

>.05

>.05

3.18
(25.02 to 18.66)

2.82
(10.77 to 16.41)

0.99
(13.70 to 11.72)

2.84
(15.86 to 10.19)

1.27
(12.28 to 9.74)

Mean Differences
(95% CI)

Table 2. Effects of Control, Inspiratory Threshold Training, and Yoga Respiratory Training Groups
YRT vs Control

27.64
(8.19 to 47.09)

13.73
(3.78 to 31.23)

33.75
(11.57 to 55.93)

25.65
(5.47 to 45.78)

25.00
(5.29 to 44.71)

12.29
(5.03 to 29.62)

40.05
(11.33 to 68.78)

32.28
(5.69 to 58.86)

28.13
(2.24 to 54.01)

7.94
(13.67 to 29.55)

16.46
(3.01 to 29.90)

13.13
(0.55 to 25.70)

11.04
(1.85 to 23.93)

2.5
(8.39 to 13.39)

Mean Differences
(95% CI)

.003

>.05

.001

.01

.01

>.05

.003

.01

.03

>.05

.01

.04

>.05

>.05

ITT vs YRT

(continues)

.04

>.05

21.04
(43.47 to 1.38)

20.62
(40.27 to 0.96)

>.05

18.13
(38.51 to 2.24)

>.05

>.05

15.380
(35.30 to 4.54)

10.52
(28.22 to 7.17)

>.05

.01

35.64
(64.67 to 6.61)
6.77
(24.28 to 10.75)

.004

.004

>.05

.05

.02

.03

>.05

36.29
(63.17 to 9.42)

35.77
(61.93 to 9.60)

11.12
(32.97 to 10.72)

13.64
(27.23 to 0.05)

14.11
(26.82 to 1.40)

13.88
(26.90 to 0.85)

3.77
(14.78 to 7.24)

Mean Differences
(95% CI)

Research Report

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72

Abbreviations: ITT, inspiratory threshold training; MEP, maximum expiratory pressure; MIP, maximum inspiratory pressure; MVV, maximum voluntary ventilation; YRT, yoga respiratory training; % predicted, percentage of the reference value.
aPercentage of the reference value.32

>.05
6.86
(18.11 to 4.39)
.01
13.55
(2.43 to 24.68)
>.05
6.69
(4.55 to 17.94)
32.5 (16.4)
(25.6-39.4)
Week 9 (T4)

39.2 (14.5)
(33.0-45.5)

46.1 (16.2)
(39.2-53.0)

>.05
7.90
(18.77 to 2.98)
>.05
9.74
(1.02 to 20.49)
>.05
1.84
(9.03 to 12.71)
33.3 (13.6)
(27.6-39.1)
Week 6 (T3)

35.2 (14.9)
(28.7-41.6)

43.1 (16.8)
(36.0-50.2)

>.05
5.67
(15.48 to 4.13)
>.05
7.58
(2.12 to 17.28)
>.05
1.91
(7.90 to 11.71)
32.8 (14.8)
(26.5-39.0)
Week 3 (T2)

34.7 (10.9)
(30.0-39.4)

40.3 (14.9)
(34.0-46.6)

>.05
0.38
(9.43 to 8.66)
>.05
2.69
(6.26 to 11.63)
>.05
2.30
(6.74 to 11.35)
30.4 (14.4)
(24.3-36.5)
Week 0 (T1)

MVV, L/min

63 (26)
(52-74)
Week 9 (T4)

75 (33)
(61-89)

32.7 (10.8)
(28.0-37.4)

33.1 (12.4)
(27.9-38.3)

.02
25.78 (47.62 to
3.95)
<.001
37.72 (16.12 to
59.32)
>.05
11.94
(9.90 to 33.78)
101 (32) (87-107)

.03
23.30
(44.50 to 2.10)
.004
28.58
(7.60 to 49.55)
>.05
5.28
(15.93 to 26.48)
69 (27)
(59-79)
Week 6 (T3)

74 (31)
(61-88)

98 (33)
(84-111)

Mean Differences
(95% CI)
Mean Differences
(95% CI)
Variables by Time Points

Control (n = 24)

ITT (n = 23)

ITT vs Control
Unadjusted Mean Outcomes, (SD) and (95% CI)

Table 2. Effects of Control, Inspiratory Threshold Training, and Yoga Respiratory Training Groups (Continued)

YRT vs Control

P
Mean Differences
(95% CI)
YRT (n = 24)

ITT vs YRT

Research Report

Figure 4. Training data for the inspiratory threshold-training


group over the 6 weeks of training. Note that the increases
in the training load are expressed both as percentages of
baseline maximum inspiratory pressure and as the absolute week pressure (range, 7-41 cm H2O).

assessment. However, as the MEP absolute values only


showed significant differences between control and YRT
groups, the percentage values showed significant differences between control and ITT groups versus the YRT group.
In general, the analyses of both primary outcomes demonstrated that YRT was superior to the other 2 groups. In
addition to all the evidence already presented, the training
load in cm H2O and percentage of baseline MIP were
measured in the ITT group, each training session during the
6 weeks of the study. Training loads in cm H2O (Figure 4)
significantly improved during the training sessions (F5,100 =
72.022, P < .001, 2 = 0.783). Similarly, the percentage of
baseline MIP also significantly increased over the 6 weeks
(F5,100 = 67.193, P < .001, 2 = 0.771).

Effect of Training Protocols on Secondary Outcome


Further analyses were calculated on MVV, in absolute
values (Figure 5). A mixed-factorial ANOVA on MVV
found a significant main effect of time (F3,204 = 23.374, P
< .001, 2 = 0.256) and effect of group (F2,68 = 2.325,
P = .106, 2 = 0.064). Again, the result of the interaction was statistically significant for the absolute values of
the dependent variable MVV (F6,204 = 5.322, P < .001,
2 = 0.135), thus giving support to a treatment effect.
Regarding the simple effects to assess the statistical significance of differences within each time point, a greater
increase in the YRT group appeared, but unlike the trend
of the MIP and MEP, this is not significant for T2 and T3.
In the follow-up, there was only a significant difference
between the YRT group and the control group (P = .012).
Finally, a mixed-factorial ANOVA on perceived
breathing difficulty by Borg Scale CR10 was performed.
No significant time effect (F5,205 = 1.210, P = .306,
2 = 0.029) and group effect (F1,41= 1.203, P = .279,
2 = 0.029) were found. The result of the interaction was
Volume 37 Number 2 April-June 2014

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Research Report

Figure 5. Maximum voluntary ventilation absolute values


(L/min) for each group and time point: means and standard errors bars (SD). ITT indicates inspiratory threshold
training; YRT, yoga respiratory training.

not statistically significant (F5,205= 1.015, P = .387, 2 =


0.024). The Borg Scale's mean for total sessions for ITT
group was 3.2 (0.8) (95% CI, 2.9-3.5) and for YRT group
was 3.5 (0.6) (95% CI, 3.2-3.8). Mean difference was not
statistically significant (t25 = 1.53, P = .13) (Table 3).

DISCUSSION
This is the first randomized controlled trial that evaluates
the effects of both ITT and YRT performed in institutionalized older adults with significant activity limitation and
Table 3. Perceived Breathing Difficulty (Borg Scale [0-10]) by
Participants of the 2 Trained Groupsa
Time
Week 1

Week 2

Week 3

Week 4

Week 5

Week 6

Total sessions

ITT Group
(n = 23)

YRT Group
(n = 24)

P
.15

3.2 (0.9)

4.0 (1.3)

(2.8-3.6)

(3.5-4.6)

3.3 (0.8)

3.6 (1.0)

(3.0-3.7)

(3.2-4)

3.7 (2.5)

3.6 (1.3)

(2.6-4.8)

(3.1-4.2)

3.4 (2.9)

3.2 (0.8)

(2.1-4.8)

(2.8-3.5)

3.0 (0.6)

3.5 (0.6)

(2.7-3.2)

(3.2-3.7)

3.1 (0.8)

3.3 (0.6)

(2.7-3.4)

(3.0-3.5)

3.2 (0.8)

3.5 (0.6)

(2.9-3.5)

(3.2-3.8)

Abbreviations: inspiratory threshold training (ITT); yoga respiratory training (YRT)


aValues are given as mean (SD) (95% confidence interval.

Journal of GERIATRIC Physical Therapy

.45

.85

.66

.70

.18

.13

RM weakness. The general hypothesis was that both RM


training programs (ITT and YRT) would improve RM
strength and endurance when compared with the control
group in the population under scrutiny. This hypothesis
was only partially supported by the data, as YRT was
effective when compared with gains in the control group,
but ITT improvements were not statistically different from
those in the control group.
Most randomized controlled trials to evaluate IMT
effects on RM functioning7,8,20 have found significant
effects on the primary outcomes in this study. Contrary
to these established effects, this study has not found these
effects. The majority of studies tested the effects of IMT
on other populations, especially in people with chronic
obstructive pulmonary disease. Our results are counterintuitive, since the meta-analyses by Ltters et al7 concluded
that IMT increases the MIP and MVV in people with
chronic obstructive pulmonary disease, especially those
with muscle weakness. Therefore, in the current sample
of the frail older adults with muscular weakness, it was
expected to have a significant benefit. With respect to an
older population, there were only 3 RCT studies available
for comparison: Belman and Gaesser,36 Watsford and
Murphy,9 and Fonseca et al.37 Unfortunately, 2 studies9,36
did not use the Threshold IMT device, used a lower age
range, the exercise capacity was normal, and the participants were community-dwelling. The study of Fonseca
et al37 also had several differences with the present study:
lower mean age, the older adults had an adequate exercise
capacity, and the dependent variables were not related
to measures of RM strength, but measures of functional
autonomy. In addition, the absence of experimental effect
of the ITT could also be due to the characteristics of training protocol applied in this study. Hill et al10 recommended
an ITT protocol of 3 sessions per week during 8 weeks,
whereas our study's protocol had 5 sessions per week
over 6 weeks. However, the total number of sessions in
our study exceeds the protocol of Hill et al.10 The control
group featured greater MIP improvements than the ITT
group over the first 3 checkpoints, and this could be due
to the training load being too low during the first 4 weeks
of study. Nevertheless, the lowest training load in our
study was more than the 30% suggested by Hill et al.10
However, the effect of the training load on effectiveness
of ITT protocol should be further investigated. No previous study with the same population and training protocol
has been performed that permits strict comparison with
this study. Therefore, the extreme debilitation of the older
adults and the institutionalization4 seems a potential explanation for the statistically nonsignificant effects of the ITT
in this study. Furthermore, the trend of increasing MIP and
MEP at T3 and T4 seems to point out that a longer training
duration could confirm or rule out the effect of the ITT in
the frail older adults. Finally, the improvement found in
MVV from weeks 6 to 9, after training was stopped, could
73

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Research Report
be due to the training physiological mechanism of adaptation (eg, supercompensation principle) and could indicate a
possible training effect.38
Regarding the YRT and its effectiveness, current results
presented strong evidence for its positive effects on RM
strength (MIP and MEP) and endurance (MVV). Despite
there being a recent study,27 which confirms the improvement of respiratory function (MIP and MEP) in healthy older
adults, this is the only randomized controlled trial available
in the literature with frail older adults. This supports the
effectiveness of YRT and could suggest that a new study is
needed to evaluate the effectiveness of a longer ITT protocol
in the frail older adults with comorbidity and activity limitation. Finally, this difference between the effects of the ITT
and YRT did not result in significant differences related to
the level of compliance between the 2 training protocols in
the institutionalized older population with disabilities. We
could speculate about the gain in the YRT group. First, the
results of the YRT group could be explained by the greater
expansion of the chest to a larger total lung capacity,13 giving the older adults the opportunity to have a more optimal
muscle length-tension relationship, such that their muscles
could generate a greater power after training than they could
generate before training. An improved length-tension relationship would provide them with greater power to do the
MEP maneuver.13,39,40 Second, the yoga breathing exercises
could train the brain to have better motor unit recruitment,
thus giving the participants a more optimal recruitment pattern to generate greater power output.

learning effect in the first few weeks of training, despite the


familiarization sessions at the beginning of the protocol, could
be attributable to an improved neuromuscular recruitment
pattern rather than RM conditioning.41,42 Future research
should measure RM performance and other outcomes related
to quality of life after allowing time for learning and train to
different intensities, at least 8 weeks.

Strengths and Limitations

ACKNOWLEDGMENTS

To our knowledge, the singular novelty of this study is the


comparison of 2 breathing techniques (the more conventional and recommended IMT technique and the unusual
and less-known yoga breathing exercises) in institutionalized older adults with significant activity limitation and
muscle weakness that has been insufficiently studied to
date. Another novelty is to study the improvement of RM
strength and endurance with yoga breathing exercises in a
randomized controlled trial. Also, the importance of this
evidence lies in the following aspects: (a) the mean age of
the sample (85 (7) years), since previous research has examined older adults in an age range between 60 and 75 years;
(b) the measuring at 4 time points of the main dependent
variables (MIP, MEP, and MVV), unlike previous research
in which only pre- and postintervention were tested; and (c)
finally, our sample size is greater than the average sample
size, between 4 and 15 participants per group in previous
randomized controlled trial studies.9,14,15,22,36,37
A number of limitations of this study are as follows: (a)
our protocol lasted for 6 weeks, while Hill et al10 has recently
recommended a protocol lasting 8 weeks or more; (b) the
possibility that the results could depend on the functional
and cognitive differential capacities; (c) a learning effect could
be present across groups, including controls. The potential
74

Clinical Implications
The significant increase in the proportion of old people in
the population, the increase of life expectancy, the progressive functional decline, the demand for long-term specialized care, and the prevalence of decreased RM strength lead
us to recommend yoga breathing exercises as a measure to
improve and maintain RM function in the population with
activity limitation. Apart from the direct benefits of yoga
on the RM strength, this technique may be recommended
on secondary reasons, such as ease of implementation, it is
extremely inexpensive, and may be used in nonambulatory
population.

CONCLUSIONS
In this randomized controlled trial, YRT appears as an
effective and well-tolerated exercise regimen in frail older
adults and may therefore be a useful alternative to ITT or
no training, to improve RM function in the older population with general muscle weakness, when whole-body
exercise training is not possible.

The authors thank all the residents, the yoga instructor (Lesia
Kowalyk), the physical therapists who participated in the
training protocols (Jos Moret Vilar, Juan Francisco Donoso
Hurtado, Pablo Martn Snchez, Clara Guzmn Sospedra,
and Estefana Jimnez Picazo), and the nursing homes health
care professionals responsible for the recruitment.

REFERENCES
1. Tolep K, Kelsen SG. Effect of aging on respiratory skeletal muscles. Clin
Chest Med. 1993;14(3):363-378.
2. Janssens JP, Pache JC, Nicod LP. Physiological changes in respiratory
function associated with ageing. Eur Respir J. 1999;13(1):197-205.
3. Watsford ML, Murphy AJ, Pine MJ. The effects of ageing on respiratory
muscle function and performance in older adults. J Sci Med Sport.
2007;10(1):36-44.
4. Simes RP, Castello V, Auad MA, Dionsio J, Mazzonetto M. Prevalence of
reduced respiratory muscle strength in institutionalized elderly people. Sao
Paulo Med J. 2009;127(2):78-83.
5. Summerhill EM, Angov N, Garber C, McCool FD. Respiratory muscle
strength in the physically active elderly. Lung. 2007;185(6):315-320.
6. Janssen I, Heymsfield SB, Ross R. Low relative skeletal muscle mass
(sarcopenia) in older persons is associated with functional impairment and
physical disability. J Am Geriatr Soc. 2002;50(5):889-896.
7. Ltters F, van Tol B, Kwakkel G, Gosselink R. Effects of controlled inspiratory
muscle training in patients with COPD: a meta-analysis. Eur Respir J.
2002;20(3):570-576.
8. Geddes EL, OBrien K, Reid WD, Brooks D, Crowe J. Inspiratory muscle
training in adults with chronic obstructive pulmonary disease: an update of
a systematic review. Respir Med. 2008;102(12):1715-1729.
9. Watsford ML, Murphy AJ. The effects of respiratory-muscle training on
exercise in older women. J Aging Phys Activ. 2008;16(3):245-260.
Volume 37 Number 2 April-June 2014

Copyright 2014 The Academy of Geriatric Physical Therapy of the American Physical Therapy Association. Unauthorized reproduction of this article is prohibited.

JPT200190.indd 74

3/14/14 11:17 PM

Research Report
10. Hill K, Cecins NM, Eastwood PR, Jenkins SC. Inspiratory muscle training for
patients with chronic obstructive pulmonary disease: a practical guide for
clinicians. Arch Phys Med Rehabil. 2010;91(9):1466-1470.
11. Clanton TL, Dixon G, Drake J, Gadek JE. Inspiratory muscle conditioning
using a threshold-loading device. Chest. 1985;87(1):62-66.
12. Martyn JB, Moreno RH, Par PD, Pardy RL. Measurement of inspiratory
muscle performance with incremental threshold loading. Am Rev Respir
Dis. 1987;135(4):919-923.
13. Gosselink R. Breathing techniques in patients with chronic obstructive
pulmonary disease (COPD). Chron Respir Dis. 2004;1(3):163-172.
14. OKroy JA, Coast JR. Effects of flow and resistive training on respiratory
muscle endurance and strength. Respiration. 1993;60(5):279-283.
15. Enright SJ, Unnithan VB, Heward C, Withnall L, Davies DH. Effect of
high-intensity inspiratory muscle training on lung volumes, diaphragm
thickness, and exercise capacity in participants who are healthy. Phys Ther.
2006;86(3):345-354.
16. Larson JL, Kim MJ, Sharp JT, Larson DA. Inspiratory muscle training with
a pressure threshold breathing device in patients with chronic obstructive
pulmonary disease. Am Rev Respir Dis. 1988;138(3):689-696.
17. Larson JL, Covey MK, Corbridge S. Inspiratory muscle strength in chronic
obstructive pulmonary disease. AACN Clin Issues. 2002;13(2):320-332.
18. Gross D, Ladd HW, Riley EJ, Macklem PT, Grassino A. The effect of training
on strength and endurance of the diaphragm in quadriplegia. Am J Med.
1980;68(1):27-35.
19. Evans S, Watson L, Hawkins M, Cowley AJ, Johnston ID, Kinnear WJ.
Respiratory muscle strength in chronic heart failure. Thorax. 1995;50(6):
625-628.
20. Gosselink R, De Vos J, van den Heuvel SP, Segers J, Decramer M,
Kwakkel G. Impact of inspiratory muscle training in patients with COPD:
what is the evidence? Eur Respir J. 2011;37(2):416-425.
21. Iyengar BKS. Luz sobre el Pranayama. 3rd ed. Barcelona, Spain: Editorial
Kairs; 2005.
22. Donesky-Cuenco D, Nguyen HQ, Paul S, Carrieri-Kohlman V. Yoga therapy
decreases dyspnea related distress and improves functional performance
in people with chronic obstructive pulmonary disease: a pilot study. J Altern
Complement Med. 2009;15(3):225-234.
23. Jain SC, Rai L, Valecha A, Jha UK, Bhatnagar SO, Ram K. Effect of yoga
training on exercise tolerance in adolescents with childhood asthma.
J Asthma. 1991;28(6):437-442.
24. Danucalov MA, Simes RS, Kozasa EH, Leite JR. Cardiorespiratory and
metabolic changes during yoga sessions: the effects of respiratory exercises and
meditation practices. Appl Psychophysiol Biofeedback. 2008;33(2):77-81.
25. Madanmohan SK, Mahadevan SB, Balakrishnan S, Gopalakrishnan M,
Prakash ES. Effect of six weeks yoga training on weight loss following step
test, respiratory pressures, handgrip strength and handgrip endurance in
young health subjects. Indian J Physiol Pharmacol. 2008;52(2):164-170.
26. Madanmohan, Udupa K, Bhavanani AB, Vijayalakshmi P, Surendiran A.
Effect of slow and fast pranayams on reaction time and cardiorespiratory
variables. Indian J Physiol Pharmacol. 2005;49: 313-318.

Journal of GERIATRIC Physical Therapy

27. Santaella DF, Devesa CR, Rojo MR, et al. Yoga respiratory training
improves respiratory function and cardiac sympathovagal balance in
elderly subjects: a randomised controlled trial. BMJ Open. 2011;24(1):
e000085.
28. Folstein MF, Folstein SE, McHungh PR, Fanjiang G. MMSE. Mini-mental
State Examination. Users guide. Lutz, FL: PAR Phycological Assessment
Resources, Inc; 2001.
29. Lobo A, Saz P, Marcos G. Adaptacin del Examen Cognoscitivo Mini-Mental.
Madrid, Spain: Tea Ediciones; 2002.
30. Miller MR, Hankinson J, Brusasco V, Burgos F, Casaburi R, Coates A, et al.
Standardisation of spirometry. Eur Respir J. 2005;26, 319-38.
31. American Thoracic Society/European Respiratory Society. ATS/ERS Statement
on respiratory muscle testing. Am J Respir Crit Care Med. 2002;166:518624.
32. Enright PL, Kronmal RA, Manolio TA, Schenker MB, Hyatt RE. Respiratory
muscle strength in the elderly: correlates and reference values. Am J Respir
Crit Care Med. 1994;149(2 Pt 1):430-438.
33. Neder JA, Andreoni S, Lerario MC, Nery LE. Reference values for lung
function tests. II. Maximal respiratory pressures and voluntary ventilation.
Braz J Med Biol Res. 1999;32(6):719-727.
34. Borg G. The Borg CR-10 Scale Folder. A Method for Measuring Intensity of
Experience. Hasselby, Sweden: Borg Perception; 2004.
35. Tabachnick BG, Fidell LS. Using Multivariate Statistics. 5th ed. Boston, MA:
Pearson International Edition; 2007.
36. Belman MJ, Gaesser GA. Ventilatory muscle training in the elderly. J Appl
Physiol. 1988;64(3):899-905.
37. Fonseca MA, Cader SA, Dantas EH, Bacelar SC, Silva EB, Leal SM.
Respiratory muscle training programs: impact on the functional autonomy
of the elderly. Rev Assoc Med Bras. 2010;56(6):642-648.
38. Lpez Chicharro J, Fernndez Vaquero A. Fisiologa del ejercicio. 3rd ed.
Madrid, Spain: Mdica Panamericana; 2006.
39. Barros GF, Santos Cda S, Granado FB, Costa PT, Lmaco RP, Gardenghi G.
Respiratory muscle training in patients submitted to coronary arterial bypass
graft. Rev Bras Cir Cardiovasc. 2010;25(4):483-490.
40. Liaw MY, Wang YH, Tsai YC, et al. Inspiratory muscle training in
bronchiectasis patients: a prospective randomized controlled study. Clin
Rehabil. 2011;25(6):524-536.
41. Eastwood PR, Hillman DR, Morton AR, Finucane KE. The effects of learning
on ventilatory responses to inspiratory threshold loading. Am J Respir Crit
Care Med. 1998;158(4):1190-1196.
42. Enrigth SJ, Unnithan VB. Effect of inspiratory muscle training intensities
on pulmonary function and work capacity in people who are healthy: a
randomized controlled trial. Phys Ther. 2011;91(6):894-905.
43. Stone SP, Ali B, Auberleek I, Thompsell A, Young A. The Barthel index in
clinical practice: use on a rehabilitation ward for elderly people. J R Coll
Physicians Lond. 1994;28(5):419-423.
44. Zijp EM, van den Bosch JS, van Hezik S. Geriatric rehabilitation in a nursing
home and the Barthel Index as a parameter. Ned Tijdschr Geneeskd.
1995;139(20):1037-1041.

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