Preoperative Pulmonary Rehabilitation Versus Chest Physical
Therapy in Patients Undergoing Lung Cancer Resection: A Pilot
Randomized Controlled Trial
Maria T. Morano, PhD,a,bAmanda S. Arau ´jo, PT,bFrancisco B. Nascimento, PT,b
Guilherme F. da Silva, PT,bRafael Mesquita, PT,cJuliana S. Pinto, MSc,d
Manoel O. de Moraes Filho, PhD,aEanes D. Pereira, PhDa,b
From theaUniversidade Federal do Ceara ´ (UFC), Fortaleza, Brazil;bHospital de Messejana Dr. Carlos Alberto Studart Gomes, Secretaria de
Sau ´de do Estado do Ceara ´ (SESA), Ceara ´, Brazil;cCentro de Pesquisa em Cie ˆncias da Sau ´de (CPCS), Centro de Cie ˆncias Biolo ´gicas e da Sau ´de
(CCBS), Universidade Norte do Parana ´ (UNOPAR), Londrina, Brazil; anddUniversidad de Salamanca (USAL), Salamanca, Spain.
Objective: To evaluate the effect of 4 weeks of pulmonary rehabilitation (PR) versus chest physical therapy (CPT) on the preoperative functional
capacity and postoperative respiratory morbidity of patients undergoing lung cancer resection.
Design: Randomized single-blinded study.
Setting: A teaching hospital.
Participants: Patients undergoing lung cancer resection (NZ24).
Interventions: Patients were randomly assigned to receive PR (strength and endurance training) versus CPT (breathing exercises for lung
expansion). Both groups received educational classes.
Main Outcome Measures: Functional parameters assessed before and after 4 weeks of PR or CPT (phase 1), and pulmonary complications
assessed after lung cancer resection (phase 2).
Results: Twelve patients were randomly assigned to the PR arm and 12 to the CPTarm. Three patients in the CPTarm were not submitted to lung
resection because of inoperable cancer. During phase 1 evaluation, most functional parameters in the PR group improved from baseline to 1
month: forced vital capacity (FVC) (1.47L [1.27e2.33L] vs 1.71L [1.65e2.80L], respectively; PZ.02); percentage of predicted FVC (FVC%;
62.5% [49%e71%] vs 76% [65%e79.7%], respectively; P<.05); 6-minute walk test (425.5?85.3m vs 475?86.5m, respectively; P<.05);
maximal inspiratory pressure (90?45.9cmH2O vs 117.5?36.5cmH2O, respectively; P<.05); and maximal expiratory pressure (79.7?17.1cmH2O
vs 92.9?21.4cmH2O, respectively; P<.05). During phase 2 evaluation, the PR group had a lower incidence of postoperative respiratory morbidity
(PZ.01), a shorter length of postoperative stay (12.2?3.6d vs 7.8?4.8d, respectively; PZ.04), and required a chest tube for fewer days (7.4?2.6d
vs 4.5?2.9d, respectively; PZ.03) compared with the CPT arm.
Conclusions: These findings suggest that 4 weeks of PR before lung cancer resection improves preoperative functional capacity and decreases the
postoperative respiratory morbidity.
Archives of Physical Medicine and Rehabilitation 2013;94:53-8
ª 2013 by the American Congress of Rehabilitation Medicine
The most effective treatment for lung cancer remains complete
surgical resection with curative intent.1A previous study2showed
a survival rate of 51% at 3 years for patients with a potentially
curable lung cancer. Unfortunately, only 20% to 30% of
individuals with lung cancer are found to be candidates for lung
resection, owing to the stage of their disease, a limited functional
capacity, or associated comorbidities.3,4
For patients who can undergo surgery, the risk of postoperative
pulmonary complications (PPCs) is increased.3-5Decreasing the
risk of respiratory morbidity in the postoperative period will
allow a safer recovery from surgery. Poor functional capacity is
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this article has or will confer a benefit on the authors or on any organization with which the authors
Clinical Trial Registration No.: RBR-3nm5bv.
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Archives of Physical Medicine and Rehabilitation 2013;94:53-8
associated with higher rates of PPCs, making the assessment of
functional capacity part of the decision-making process for the
surgical treatment of lung cancer.5
Preoperative pulmonary rehabilitation (PR) has been demon-
strated to significantly improve exercise capacity, dyspnea, and
health-related quality of life in patients awaiting lung volume
reduction surgery and lung transplantation.6,7The scarcity of
publications about PR before lung cancer resection is evident in
the literature; there are few studies with the aim of optimizing
preoperative lung function and global conditioning of the
patients.7-13Just 1 randomized study14has been published to date
showing the beneficial effect of a short-term preoperative PR
program on the postoperative morbidity of patients with moderate
to severe chronic obstructive pulmonary disease (COPD) under-
going lung cancer resection.
The aim of this study was to assess the impact of 4 weeks of
PR versus chest physical therapy (CPT) on the preoperative
functional capacity and postoperative respiratory morbidity of
patients undergoing lung cancer resection. We hypothesized that
the PR program would improve the preoperative functional
capacity and decrease the postoperative respiratory morbidity.
This randomized single-blinded study was conducted at a teaching
hospital in Ceara ´ (northeastern Brazil). All subjects gave their
informed written consent before participation, and the study was
previously approved by the institutional review board.
Criteria for inclusion in the study were the following: patients
had to have (1) nonesmall cell lung cancer resection by open
thoracotomy or by video-assisted thoracoscopy; and (2) previous
pulmonary disease, interstitial lung disease, or obstructive airway
disease, with impaired respiratory function by spirometry.
This randomized study tested 4 weeks (5 sessions per week) of
preoperative PR versus CPT.
The rehabilitation group used the following protocol. The
upper limb incremental test was based on a principle called the
proprioceptive neuromuscular facilitation method that uses muscle
groups in diagonal movement patterns. The upper limb performs
a diagonal movement (primitive diagonal) starting from the
opposite iliac crest (rest position) going outwards and upwards
until it reaches the maximum shoulder flexion, then it goes back to
the initial rest position. The initial load is 500g, with an increase
of 500g each minute. Patients must perform a minimum rate of 15
repetitions per minute.
Lower extremity endurance training had a target time of 30
minutes and was performed on a treadmill. In the first week, the
patients performed 10 minutes of walking on a treadmill. The
duration was built up to 30 minutes during the first 3 weeks of the
program, with increments of 10 minutes each week. In the last
week they performed 30 minutes of walking. Exercise intensity
was based on 80% of the maximum load achieved during
a treadmill incremental test.
Inspiratory muscle training (IMT) was performed using the
Threshold Inspiratory Muscle Trainer.aDaily IMT sessions of 10
to 30 minutes’ duration were performed. Patients started breathing
at a resistance that required generation of 20% of their maximal
inspiratory pressure (MIP) and kept this intensity during the first
week. The load was then increased by 5% to 10% each session, to
reach a generation of 60% of their MIP at the end of the
Flexibility, stretching, and balance exercises were included as
part of the warmup and cooldown section of each exercise session.
The protocol for the group receiving conventional CPT con-
sisted of instructions about the techniques for lung expansion:
sustained maximal inspiration, fractional inspiration with or
without a pause for inspiration hold, breathing patterns (dia-
phragmatic), pursed lips, and flow-based incentive spirometry.b
This group did not perform IMT.
All the patients participated in classes about the importance of
preoperative and postoperative care and knowledge of the surgical
process, energy conservation techniques, relaxation and stress
management techniques, focus on nutrition, and the need to seek
health services when necessary. There was no control group for
the minimum education and preoperative IMT.
Before randomization, the patients had a functional evaluation
that consisted of the following measures: spirometry, MIP,
maximal expiratory pressure (MEP), 6-minute walk test (6MWT),
and blood gas measurements. If necessary, the drug treatment was
optimized. After that, patients were randomly assigned to undergo
a preoperative PR or CPT program. The randomization was done
in “blocks” of 4, and individual allocations were placed in sealed
envelopes. An external investigator blinded to the allocation
sequence picked the envelopes.
A new functional evaluation was performed during the last
daily session of the programs. The surgery was scheduled
immediately after that last evaluation. The surgical techniques and
the teams were not selected.
Endpoints of this study were evaluated in 2 phases:
? Phase 1: The functional parameters after the completion of the
programs (spirometry, MEP, MIP, 6MWT, and blood gas
? Phase 2: Hospital length of stay and PPCsdpneumonia (new
infiltrate plus either fever [temperature >38oC] and white blood
cell count >11,000, or fever and purulent secretions), bron-
chopleural fistula, bronchospasm, severe atelectasis (confirmed
by chest radiographs, requiring chest physiotherapy or bron-
choscopy), prolonged need for chest tubes (>7d), and pro-
longed mechanical ventilation (>48h).
Postoperative outcomes were obtained from the medical
records by a physical therapist blinded to the treatment
Data analysis was performed using the SPSS for Windows
16.0.cData are expressed as mean ? SD. In all continuous vari-
ables, the distribution was assessed by means of the Kolmogorov-
Smirnov test. Normally distributed variables were compared by
paired t test and the Wilcoxon rank-sum test whenever parametric
tests were inappropriate.
Continuous variables were tested between the 2 treatment arms
(PR vs CPT) using the Student t test. Categorical variables were
tested using Fisher exact tests. Nonnormal variables were assessed
List of abbreviations:
COPD chronic obstructive pulmonary disease
CPT chest physical therapy
IMT inspiratory muscle training
MEP maximal expiratory pressure
MIP maximal inspiratory pressure
PPC postoperative pulmonary complication
PR pulmonary rehabilitation
6MWT 6-minute walk test
54 M.T. Morano et al
by Mann-Whitney U for 2 independent samples. All tests were
2-sided tests, and significance was set at P<.05.
This randomized trial study recruited 31 patients between the
period of March 2008 and March 2011 from a teaching hospital
in Ceara ´ (northeastern Brazil). After that, 7 patients were
excluded, of whom 5 patients refused participation, and 2 patients
did not meet inclusion criteria because of normal pulmo-
Twenty-four patients were randomly assigned, 12 to the PR
arm and 12 to the CPT arm. All the patients from the PR group
and the CPT group successfully completed the 5 sessions per week
during 1 month. Three patients in the CPTarm were not submitted
to lung resection because of inoperable cancer. The final analysis
Flow diagram of the randomized controlled trial of 4 weeks of PR versus CPT before lung cancer resection.
Pulmonary rehabilitation and lung cancer55
of the postoperative outcome was based on data from 21 patients
(12 from the CPT arm, 9 from the PR arm) (fig 1).
Of these 24 patients, 19 had a diagnosis of COPD,152 inter-
stitial lung disease, and 3 bronchiectasis. Twenty patients had their
resections by open thoracotomy and 1 patient by video-assisted
thoracoscopy. Patients’ characteristics and actual values of base-
line functional parameters are presented in table 1. The baseline
characteristics observed between the 2 treatment arms (PR vs
CPT) were comparable for demographic, clinical, surgical, and
functional parameters except for the measures of MIP and
MEP (table 2).
The improvement in functional parameters was evident from
baseline to 1 month for the PR group. Significant increases were
found for the following parameters: forced vital capacity both
and percentage of that predicted (59.6%?15.1% vs 74.9%?16.7%,
respectively; PZ.00), 6MWT (425.5?85.3m vs 475?86.5m,
respectively; PZ.00), MIP (90?45.9cmH2O vs 117.5?36.5cmH2O,
92.9?21.4cmH2O, respectively; PZ.00). These improvements were
not observed in the CPT group (table 3).
The main differences between patients in the PR versus CPT
groups after surgery were the following: patients in the PR group
had fewer days in the hospital (7.8?4.8d vs 12.2?3.6d; PZ.04),
fewer days needing a chest tube (4.5?2.9d vs 7.4?2.6d; PZ.03),
and a lower incidence of PPCs (16.7% vs 77.8%; PZ.01)
(table 4). An intention-to-treat analysis was done including the 3
patients in the CPT group who did not have surgery and assuming
no change for the PPCs. Results analyzed both by intention to treat
and per protocol showed that the CPT group had more post-
operative complications than the PR group.
In this exploratory randomized trial, participation in a 4-week PR
program before lung cancer resection was associated with
improvements in preoperative functional capacity, fewer PPCs,
and a shorter length of postoperative hospital stay.
The studies about the benefits of PR in patients with cancer,
particularly in the perioperative setting for lung cancer, are scarce
in the literature.4-6,16Cesario et al13have reported the beneficial
effect of a 4-week inpatient preoperative PR program in 8 patients
functionally impaired with nonesmall cell lung cancer. The
program included symptom-limited exercise and muscle electric
stimulation; after that intervention the patients improved their
pulmonary function and 6MWT and were able to undergo
The length of preoperative PR for lung cancer resection is
controversial. Three studies11,17,18
postoperative outcomes with short interventions. On the other
hand, only a few studies have suggested the benefit of a preoper-
ative PR program longer than 4 weeks, before lung cancer
resection: (1) the study by Cesario13mentioned before; (2) Bobbio
et al19in a prospective observational study observed the beneficial
reported improvement in
Patients’ characteristics and actual values of baseline
Abbreviations: F, female; FEV1, forced expiratory volume in the first
second; FVC, forced vital capacity; M, male.
weeks of PR vs CPT
Baseline characteristics of the 24 patients before 4
Previous pulmonary diseasey
Lung cancer stagey
NOTE. Values are mean ? SD, n (%), or median (25the75th percentiles).
Abbreviations: FEV1, forced expiratory volume in the first second; FVC,
forced vital capacity; PCO2, carbon dioxide partial pressure; PO2, oxygen
partial pressure; Sat O2, peripheral oxygen saturation.
* Student t test.
yFisher exact test.
zMann-Whitney U test.
56M.T. Morano et al
effect of a 4-week preoperative PR program on exercise perfor-
mance of 12 patients with COPD who were candidates for lung
cancer resection; (3) Jones et al20reported that preoperative
exercise training could improve cardiorespiratory fitness of 18
patients undergoing pulmonary resection; and (4) Spruit et al21
reported a pilot study about the improvement of exercise
capacity after an inpatient PR program during 8 weeks in 10
patients with lung cancer. In the present study, functional
parameters measured before and after 4 weeks of preoperative PR
demonstrated an improvement.
There is a major concern about the delay of curative surgery
with the period of 4 weeks of PR before lung cancer resection. In
our center, there is eagerness to proceed with surgery, so the 4
weeks we chose and the usual period of workup did not change the
The previously cited studies in the literature are all
nonrandomized studies with small sample sizes, and none of them
evaluated the incidence of PPCs.
In the present randomized study, a 4-week period of preop-
erative PR decreased the postoperative respiratory morbidity and
was associated with a shorter length of hospital stay. Only 1
previous randomized study14has been published showing the
benefits of a shorter preoperative PR program before lung cancer
resection in patients with poor lung function. In that study, Benzo
et al14showed that in patients with COPD who are candidates for
lung cancer resection, a 10-session preoperative PR program
significantly decreased the time of chest tube drainage and
lowered the incidence of patients requiring chest tubes for a pro-
longed period. The authors also conducted another trial of
a 4-week preoperative PR intervention, with poor results. Most of
the patients or providers did not agree to delay the curative
surgery for 4 weeks.
One of the postoperative outcomes of the present study was
that in the PR group, few patients developed bronchopleural
fistulas, and the number of days patients required a chest tube was
decreased, the same outcomes observed by Benzo.14The mech-
anism of the decrease in our study is unclear.
Another interesting finding of this study was that the PR group
showed a significant improvement of the respiratory pressures and
walking abilities after 1 month. We could attribute these benefits
to the rehabilitation with routine use of muscle training. This
result is in line with the study results of Hulzebos et al,17who
showed that IMT before thoracic surgery may improve preoper-
ative MIP in patients undergoing coronary artery bypass graft
surgery. The impact of preoperative IMT on the outcomes of
thoracic surgery has been previously addressed.18,22,23
The very important limitations of this study are the small sample
size and the loss of patients, which raise concerns about the
generalizability of the study. We attempted to control for the loss
of patients by using intent-to-treat analysis. The uneven random-
ization is also an issue. Although the power of the analysis was not
calculated, some of the main variables in both phase 1 and phase 2
of the study achieved statistical significance in the comparisons
between groups (PR vs CPT).
Baseline and 1-month functional parameters for the 2 study groups
NOTE. Values are mean ? SD or median (25the75th percentiles).
Abbreviations: FEV1, forced expiratory volume in the first second; FVC, forced vital capacity; PCO2, carbon dioxide partial pressure; PO2, oxygen partial
pressure; Sat O2, peripheral oxygen saturation.
* Paired t test.
Postoperative outcomes after 4 weeks of PR vs CPT
Days in hospital*
ICU stay (d)y
Days with chest tubes*
Patients with PPCsz
NOTE. Values are mean ? SD, median (25the75th percentiles), or n (%).
Abbreviation: ICU, intensive care unit.
* Student t test.
yMann-Whitney U test.
zFisher exact test.
Pulmonary rehabilitation and lung cancer57
Conclusions Download full-text
To date and to our knowledge, this is the first randomized study
showing the benefit of a 4-week PR program, administered to
patients undergoing lung cancer resection, on preoperative func-
tional capacity and postoperative morbidity. We consider this to be
an important presurgical intervention that improves the condi-
tioning status of the patients and appears to be effective at
reducing morbidity in the postoperative period. Further trials,
particularly the design of large confirmatory studies, are necessary
to corroborate these findings.
a. HealthScan Products Inc, 908 Pompton Ave, Cedar Grove,
b. NCS Indu ´stria e Come ´rcio Ltda, Rua Aeroporto 192, Cha ´caras
Marco, Barueri-SP, 06419-260, Brazil.
c. IBM North America, 590 Madison Ave, New York, NY 10022.
cancer; Postoperative complications;Rehabilitation;
Eanes D. Pereira, PhD, Rua Barbara de Alencar 1401, 60140000,
Fortaleza, Ceara ´, Brazil. E-mail address: email@example.com.
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