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Original Article
Pulmonary rehabilitation program including respiratory conditioning
for chronic obstructive pulmonary disease (COPD): Improved
hyperinflation and expiratory flow during tidal breathing
Kaku Yoshimi1, Jun Ueki2, Kuniaki Seyama1, Makiko Takizawa3, Seiko Yamaguchi3, Eriko Kitahara4, Shinji Fukazawa5,
Yukiko Takahama5, Masako Ichikawa1, Kazuhisa Takahashi1, Yoshinosuke Fukuchi1
1Department of Respiratory Medicine, Juntendo University School of Medicine, 2-1-1 Hongo, Bunkyo-Ku, Tokyo, 113-8421, Japan;
2Juntendo University School of Health Care and Nursing, 2-5-1, Takasu, Urayasu-City, Chiba, 279-0023, Japan; Departments of 3Nursing,
4Rehabilitation, and 5Inhalation therapy, Juntendo University Hospital, 3-1-3, Hongo, Bunkyo-Ku, Tokyo 113-8431, Japan
Corresponding to: Kaku Yoshimi, MD. Department of Respiratory Medicine, Juntendo
University School of Medicine, 2-1-1 Hongo, Bunkyo-Ku, Tokyo 113-8421, Japan. Tel:
(+81) 3-5802-1063; Fax: (+81) 3-5802-1617. Email: kyoshimi@juntendo.ac.jp.
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Abstract
Background: Pulmonary rehabilitation has generally relieved symptoms, strengthened exercise endurance and
improved health-related quality of life (QOL) in patients with COPD, but recovery of pulmonary function remains
questionable. This analysis of our innovative rehabilitation program is directed at documenting changes in patients’
expiratory airflow limitation, pulmonary symptoms and QOL. This program is designed to provide “respiratory conditioning”,
a physical therapist-assisted intensive flexibility training that focuses on stretching and rib cage mobilization.
Methods: Thirty-one patients with COPD who attended rehabilitation sessions at Juntendo University Hospital from
1999 to 2006 were analyzed. Pulmonary function, expiratory flow limitation during tidal breathing, six minute walk
distance (6MWD), respiratory muscle strength, and St. George Respiratory Questionnaire (SGRQ) were measured
before and after pulmonary rehabilitation.
Results: In participants ages 68±7 years, the FEV1% predicted was 39.3±15.7%. 6MWD, SGRQ and respiratory muscle
strength were significantly improved after pulmonary rehabilitation. Although neither FEV1% predicted nor FEV1/FVC
was affected to a significant extent, indicating little effect on airflow limitation, expiratory flow limitation in supine as
well as seated during tidal breathing improved significantly. Moreover, rehabilitation significantly diminished TLC%
predicted, FRC% predicted, RV% predicted and RV/TLC values, thus indicating a reduction of hyperinflation of the
lungs at rest.
Conclusion: The present results suggest that our rehabilitation program with respiratory conditioning significantly
lowered the hyperinflation of lungs at rest as well as the expiratory flow limitation during tidal breathing. In patients
with COPD, overall pulmonary function improved, exercise endurance increased and health-related QOL was enhanced.
Key words
Expiratory flow limitation; hyperinflation; negative expiratory pressure; pulmonary rehabilitation; respiratory conditioning
J Thorac Dis 2012;4(3):259-264. DOI: 10.3978/j.issn.2072-1439.2012.03.17
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Introduction
Chronic obstructive pulmonary disease (COPD) is a
common disease in the elderly and its prevalence is increasing
worldwide. The impact of COPD on public health is
highlighted in the Global Initiative for Chronic Obstructive
Lung Disease (GOLD) Workshop Report ( 1). A nation-wide
epidemiological study indicated the great burden of COPD
in Japan, eliciting an urgent need for promoting awareness of
this disease in this country ( 2). Airflow limitation suggesting
the existence of COPD was prevalent in 10.9% of individuals
aged ≥40 years and significantly more prevalent in older subjects
(3.5% in 40-49 years old vs. 24.4% in those >70 years) ( 2). Pulmonary rehabilitation is an important nonpharmacological
treatment for COPD. Many studies have
shown that such therapy reduces dyspnea on exertion,
increases exercise capacity and improves health-related quality
of life (QOL) ( 3- 6). Progressive airflow limitation in COPD
patients results in exercise de-conditioning, immobility and
muscle wasting, relative social isolation, altered mood states,
especially depression, and body weight loss over a prolonged
period ( 1). These problems interact with each other resulting
in a vicious cycle of deterioration. In this context, pulmonary
rehabilitation is therefore considered beneficial and effective
for COPD patients, since it mitigates each of these conditions
and can interrupt deterioration process ( 1). However, whether
pulmonary rehabilitation actually improves pulmonary function,
including airflow limitation, remains controversial ( 4, 7- 9). We designed to provide a “respiratory conditioning” segment
in conjunction with exercise training and respiratory muscle
training. Respiratory conditioning maneuvers involve the
optimization of breathing patterns, physical therapist-assisted
rib cage mobilization and improvement of body flexibility. We
considered the physiotherapy working on thoracic cage would be
a critical component for successful rehabilitation program since
a static lung volume fraction and the level of functional residual
capacity (FRC) is determined by the compliance of the lung as
well as that of chest wall. We report here that our pulmonary
rehabilitation program including a “respiratory conditioning”
ameliorated pulmonary symptoms and upgraded exercise
endurance as well as QOL in patients with COPD. Furthermore,
we confirmed that both expiratory flow limitation (EFL) during
tidal breathing as well as hyperinflation of the lungs at rest
improved after completing the program. |
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Methods
Study population
We encouraged patients with stable COPD to participate in
the pulmonary rehabilitation program, who were treated in
the respiratory outpatient clinic of Juntendo University and
expected to visit regularly 2 days per week for 6 weeks during
the program. The study protocol was approved by the Ethics
Committee of the Juntendo University Hospital. From 1999
to 2006, 37 patients with stable COPD participated in our
pulmonary rehabilitation program. Each patient was diagnosed
with COPD and treated with medicines according to GOLD
guideline ( 1). They were treated with inhaled bronchodilators,
and most of them were given either short- or long-acting
anticholinergics. During pulmonary rehabilitation, all patients
were allowed to continue their pharmacological therapy. Five
patients were on supplemental oxygen therapy. Six patients were
excluded from the analysis because their pulmonary function
data after pulmonary rehabilitation were not obtainable after an
exacerbation of COPD. Accordingly, 31 patients with COPD,
including one patient with stage I (FEV 1≥80% predicted), 4
with stage II (50%≤FEV 1<80% predicted), 18 with stage III
(30%≤FEV 11<30%
predicted) according to the disease severity of GOLD criteria ( 1),
were retrospectively analyzed. All the patients were males, exsmokers
and 67±7 (mean ± SD) years old. Comprehensive multidisciplinary pulmonary rehabilitation
program
All the patients participated in the pulmonary rehabilitation
program on an outpatient basis. The comprehensive outpatient
pulmonary rehabilitation program included 2 sessions per
day (60 minutes per session), 2 days per week for 6 weeks
and was provided by a multidisciplinary team that included
various health care professionals (physician, nurse, physical
and respiratory therapist, pulmonary function laboratory
technician, pharmacist, dietitian, medical social worker, and a
provider of long-term home oxygen therapy). Treatment groups
consisted of a maximum of three patients. The program included
physiotherapy, exercise, respiratory muscle training (12 sessions,
one on one), self-management education (11 sessions, as a
group) and nutritional consultation (1 session, one on one).
The physiotherapy respiratory conditioning involves the
optimization of breathing patterns, therapist-assisted rib cage
mobilization and improvement of body flexibility. For the rib
cage mobilization of COPD patients, the physical therapist
performed continuous manual compressions of the rib cage
during exhalation (not shaking/vibrations) as well as manual
stretching and relaxation of the intercostal and pectoral muscles,
neck muscles and back muscles. Therapists also applied manual
mobilization of the spine and correction of posture during
exercise or breathing. Manual stretching of the abdominal
muscles and hamstrings and manual mobilization of the
pelvis were performed for therapist-assisted improvement of
body flexibility. During the initial three sessions, most of each
session was spent on respiratory conditioning. As the sessions
proceeded, the time used for conditioning in each session
gradually decreased, while the time used for exercise training
increased. These exercises included low-intensity endurance
and strength training of the upper and lower extremities and
respiratory muscle training. Walking (hall walk) and stationary
bike training (cycle ergometer 5 to 15 W) was extended
(symptom-limited maximum) to promote endurance of the
lower extremities. Upper and lower extremity strength training
started with free weights, then hand and ankle light weights (0.5
to 2 kg) were used. The ThresholdTM inspiratory muscle trainer
(HealthScan, Cedar Grove NJ, USA) was used for the inspiratory
muscle training at 30% of Pimax. The patients were encouraged
to exercise (for example, stretching of the intercostal and pectoral
muscles, low-intensity endurance and strength training of the
upper and lower extremities) at home between sessions while
they were on the program.
Initial assessment and outcome measures of pulmonary
rehabilitation
When each patient’s COPD was stable, ventilatory function was
assessed by spirometry (Autospirometer system 9, Minato Inc.,
Japan), and lung volumes were evaluated by body plethysmography
(Bodyplethysmograph BX-9, Minato Inc., Japan). The reference
values obtained from the Japanese population were utilized to
calculate the % predicted value ( 10). With patients in supine
as well as sitting positions, EFL during tidal breathing was
measured according to the negative expiratory pressure method
of Koulouris et al. ( 11). EFL assessment included the two indices
described by Eltayara et al. ( 12). One is a discrete variable, a
score expressing the degree of flow limitation (FL): 0= none, 1=
mild, 2= moderate, 3= severe and 4= very severe. The other is
a continuous variable, the FL (%), a percentage of flow-limited
volume to control expired tidal volume (VT). Respiratory
muscle strength was determined by the measurement of Pimax
and Pemax (Pmax Mouth Pressure Monitor, PK Morgan,
UK) according to the American Thoracic Society/European
Respiratory Society statement ( 13). Six-minute walk distance
(6MWD) was measured according to the American Thoracic
Society statement ( 14). Health-related QOL was assessed by
The St. George’s Respiratory Questionnaire (SGRQ). Statistical analysis
Data are presented as means±SD. Comparisons of the data
before and after rehabilitation were evaluated by the paired t-test
using the StatView® software program, and a value of P<0.05 was
considered to be significant. |
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Results
The outcomes of the comprehensive multidisciplinary pulmonary
rehabilitation
The baseline characteristics of the 31 COPD patients and
results after pulmonary rehabilitation are summarized in
Table 1. Attendance at the sessions was excellent with a mean
percentage of 99.5%. The pulmonary rehabilitation’s significantly
improved outcomes were recorded as the following values:
TLC% predicted (137.4±22.7 vs. 131.5±18.9, P<0.01),
FRC% predicted (148.4±31.8 vs. 140.0±26.8, P<0.01), RV%
predicted (230.3±61.4 vs. 210.3±52.8, P<0.01) and RV/TLC
(58.4±7.4 vs. 56.3±8.0, P<0.05), thus indicating the reduction
of hyperinflation in the lungs at rest. Values not significantly
improved were FEV 1, FEV 1% predicted, VC and DLco/
VA% predicted. Although obstructive ventilatory impairment
during forced-expiratory maneuver did not lessen during our
rehabilitation program, EFL during tidal breathing improved
notably to a statistically significant extent. Both FL score and FL (%)
(seated as well as supine) decreased after our pulmonary
rehabilitation, although evaluation was limited to only 19
patients of the total study population ( Table 1). The EFL
while sitting completely disappeared in 3 of 8 COPD patients
examined; even better, EFL vanished from 8 of 15 supine
patients with COPD.
| Table 1. Characteristics of the study population and outcomes of the comprehensive multidisciplinary pulmonary rehabilitation (n=31). |
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Before |
After |
P value |
| Body weight (kg) |
54.4±10.2 |
54.9±9.9 |
<0.05 |
| Pulmonary function tests (n=31) |
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| FEV1 (L) |
1.05±0.41 |
1.04±0.41 |
0.501 |
| VC (L) |
3.16±0.64 |
3.25±0.72 |
0.118 |
| FEV1 % predicted |
40.3±15.8 |
39.9±15.8 |
0.502 |
| DLco/VA % predicted |
37.2±11.6 |
37.4±10.8 |
0.880 |
| TLC % predicted |
137.4±22.7 |
131.5±18.9 |
<0.01 |
| RV % predicted |
230.3±61.4 |
210.3±52.8 |
<0.01 |
| FRC % predicted |
148.4±31.8 |
140.0±26.8 |
<0.01 |
| RV/TLC |
58.4±7.4 |
56.3±8.0 |
<0.05 |
| 6MWD |
405±92.0 |
436±83.0 |
<0.01 |
| Respiratory muscle strength (n=27)* |
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| Pimax |
–58.3±16.7 |
–69.3±18.4 |
<0.01 |
| Pemax |
149.4±40.0 |
162.1±36.5 |
<0.01 |
| SGRQ (n=24)† |
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| Total |
42.4±12.5 |
31.7±14.5 |
<0.01 |
| *Four patients were excluded for exacerbation of COPD precluding measurement of respiratory muscle strength (n=1), an episode of acute
lumbago (n=1), or a recent episode of pneumothorax (n=2) at the time when the evaluation after pulmonary rehabilitation was scheduled;
†SGRQ was not evaluated in 7 patients. |
| Table 2. Effect of the comprehensive multidisciplinary pulmonary rehabilitation program on EFL during tidal breathing (n=19). |
| |
Before |
After |
P value |
| FL score(range 0-4)* |
2.2±1.5 |
1.0±1.5 |
<0.01 |
| FL (%) (seated) |
20.9±28.1 |
10.4±20.8 |
<0.05 |
| FL (%) (supine) |
49.9±32.9 |
20.7±29.2 |
<0.01 |
| *Definition of FL category (12): 0= not flow-limited either seated or supine; 1= flow-limited <50% tidal breathing volume (VT) supine but not
flow-limited seated; 2= flow-limited >50% VT supine but not flow-limited seated; 3= flow-limited <50% VT seated but flow-limited supine; and 4=
flow-limited >50% VT seated but flow-limited supine. |
Overall, exercise endurance significantly improved after
pulmonary rehabilitation, as indicated by an increase of 6MWD
from 405±92 to 436±83 m, closely approximating that described
by Puhan et al. ( 15) as an important advance. They reported
that 6MWD should change by –35 m for patients with moderate
to severe COPD in order to represent an important effect. In
addition, respiratory muscle strength measured by Pimax and
Pemax significantly improved after pulmonary rehabilitation.
The Pimax increased from –58.3±16.7 to –69.3±18.4 cmH 2O,
and the Pemax increased from 149.4±40.0 to 162.1±36.5
cmH2O. Nutritional status also responded well to this
pulmonary rehabilitation as indicated by the patients’ increase
of body weight from 54.4±10.2 to 54.9±9.9 (P<0.05, statistically
significant although the magnitude of increment is small).
Health-related QOL improved after rehabilitation as indicated
by a decrease of the total score from 42.4±12.5 to 31.0±14.5,
which satisfied the minimal clinical importance of 4 points. |
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Discussion
Our comprehensive pulmonary rehabilitation program presented
here significantly improved hyperinflation of the lungs at rest,
EFL during tidal breathing, exercise endurance and healthrelated
QOL for patients with COPD. Although pulmonary
rehabilitation has typically benefited such patients ( 1, 3- 6, 16, 17),
few improvements in pulmonary functions have been established
( 7- 9). However, we have demonstrated for the first time that
our pulmonary rehabilitation program including respiratory
conditioning can significantly reduce EFL during tidal breathing,
which should be interpreted as particularly relevant in this
physiological setting. The factor that most differentiated our rehabilitation program
from others was the introduction of “respiratory conditioning,”
defined as a procedure for improving the flexibility of the
chest with the correction of posture and the stretching and
mobilization of the rib cage. We considered that respiratory
conditioning would contribute to expanding expiratory
flow and reducing hyperinflation of the lungs at rest. In fact,
respiratory muscle stretch gymnastics have been proposed as an
additional form of pulmonary rehabilitation for COPD patients.
The objective is to decrease chest wall stiffness by stretching
the respiratory muscles of the chest wall during breathing.
Accordingly, Minoguchi et al. ( 7) and Yamada et al. ( 8) suggested
that respiratory muscle stretching would decrease FRC while
increasing chest wall expansion and exercise capacity. However,
on their own, those patients were required to perform 5 patterns
of muscle stretching gymnastics 3 times every day for 4 weeks
to obtain any benefit. In contrast, our program incorporated
physical therapist-assisted manual stretching of the respiratory
muscles to reduce dyspnea before starting exercise training.
Moreover, the effect of this technique on chest wall compliance
did not depend on patients’ skill but rather on the knowledge of
trained therapists. Similar to the results of other studies ( 4), our pulmonary
rehabilitation program did not improve the airflow limitation
as assessed by spirometry. For the FVC maneuver, a subject
is requested to exhale with a maximal effort in order to assess
pulmonary function. However, this maneuver is quite unusual
and not experienced in daily living, hence not an actual
physiological assessment of pulmonary function. In daily living,
those patients utilize a much lower flow in tidal breathing,
and parameters obtained with the FVC maneuver cannot
reflect changes in the lower flow ranges. However, the negative
expiratory pressure method claims validity in detecting small
changes in expiratory flow during tidal breathing. EFL is as
sensitive as FEV 1% predicted, but has a stronger correlation with
the severity of dyspnea in COPD patients, therefore, is more
appropriate for evaluating effects on airflow limitation relevant
to the activities of daily life ( 12). We theorized that the improvement of EFL would contribute
to a reduction of hyperinflation in lungs at rest and other
functions. However, the improvement of EFL did not correlate
with a reduction of hyperinflation of lungs at rest, SGRQ or
6MWD (data not shown). Our study population may have been
too small to produce such data; hence, a larger study is needed to
prove the clinical implication of EFL regarding mechanistic and
physiologic significance on an outcome measure of pulmonary
rehabilitation in patients with COPD.
Hyperinflation of the lungs at rest and/or during exercise is an
important physiological feature in COPD. The narrowing of the
small airways, reduced elastic recoil pressure due to destruction
of alveoli, blood gas abnormalities, and increased chest wall
stiffness are possible mechanisms for their hyperinflation
( 16, 18, 19). In addition, the FRC increases with age mainly due
to a decrease in chest wall compliance or an increase in chest
wall stiffness, thus increasing the outward recoil force of chest
wall and the lungs ( 20). An improvement of airflow limitation
using a bronchodilator has been reported to reduce the
hyperinflation of the lungs (decreased FRC) with an increase in
IC ( 21). Albuquerque et al. ( 22) reported that not only the postbronchodilator
FEV 1 and IC but also IC/TLC values provide
useful information for estimating a COPD patient’s maximal
exercise capacity, whether severely reduced or not. In the current
study, no increase in the IC was observed, since the amount
of reduction between TLC and FRC was about the same. In
addition, IC/TLC did not increase significantly (P=0.103),
although it tended increase after the pulmonary rehabilitation.
Although it is unlikely that our pulmonary rehabilitation
program directly affected the airways or lung parenchyma,
the reduction of hyperinflation of lungs at rest at the baseline
appeared to retard the progression of dynamic hyperinflation
on effort, which would eventually raise the end-expiratory
level to the dyspnea limit ( 23). In addition, by decreasing chest
wall stiffness thereby increasing its flexibility, the reduced
hyperinflation of lungs at rest may generate greater mobility of
the diaphragm. Consequently, this effect may improve exercise
capacity. In this context, we believe that respiratory conditioning
in our pulmonary rehabilitation program can ameliorate
symptoms, raise exercise capacity and improve QOL. Our program resulted in the improvement in all domains
of health-related QOL and a reduction of 10.6 in the SGRQ
total score: that is, greater than the mean reduction of 6.11
in SGRQ total score obtained from the meta-analysis done
by Lacasse et al ( 5). Good attendance and adherence to
our rehabilitation program would have contributed for the
participants to achieve its optimal benefits. Sabit R et al. reported
that poor attendance at pulmonary rehabilitation programs
was independently associated with being a current smoker,
participating in a longer rehabilitation program, having more
numerous hospital admissions, suffering a higher degree of
breathlessness or enduring a long journey to the hospital ( 24).
Factors contributing to our high attendance rate may be the
non-smoking status (all were ex-smokers) and an appropriate
duration of pulmonary rehabilitation programs (2 sessions
per day, 2 days per week and 6 weeks duration) ( 17). Other
factors we speculate that might have played a role include: (I)
respiratory conditioning (physical therapist-assisted manual
compression and relaxation of the thoracic cage) created a
strong interaction between patient and physical therapist,
thereby decreasing anxiety about exercise training and reducing
breathlessness, (II) an early amelioration of exertional dyspnea
during the program motivated COPD patients to complete the
program, while also enhancing the efficacy of exercise training,
and (III) the reduction of hyperinflation of the lungs at rest
obtained by our rehabilitation program improved the function
and mobility of diaphragm, which in turn decreased symptoms
and increased exercise tolerance. Our study has several limitations including (I) a retrospective
analysis, (II) a small number of study subjects, and (III)
participants were very heterogeneous regarding the severity
of COPD. They therefore clearly impede us to draw a precise
conclusion. However, the present study focused for the first time
on the significance of respiratory conditioning during pulmonary
rehabilitation and reported that its beneficial effect on chest wall
kinematics are likely to improve EFL and reduce hyperinflation
of the lungs for the many victims of COPD. Further study on
the understanding of the role of respiratory conditioning during
pulmonary rehabilitation seems to be warranted.
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Acknowledgements
We appreciate the contributions of Tomomi Shida as a dietitian,
Naoki Tsukada as a physical therapist and Masako Yoshida
as a medical social worker to the comprehensive pulmonary
rehabilitation program. We also appreciate Phyllis Minick for
excellent assistance in the organization of the manuscript and the
review of English.
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Cite this article as: Yoshimi K, Ueki J, Seyama K, Takizawa M, Yamaguchi
S, Kitahara E, Fukazawa S, Takahama Y, Ichikawa M, Takahashi K, Fukuchi
Y. Pulmonary rehabilitation program including respiratory conditioning for
chronic obstructive pulmonary disease (COPD): Improved hyperinflation
and expiratory flow during tidal breathing. J Thorac Dis 2012;4(3):259-264.
doi: 10.3978/j.issn.2072-1439.2012.03.17
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