Respiratory Medicine (2015) 109, 437e442

Available online at www.sciencedirect.com

ScienceDirect

journal homepage: www.elsevier.com/locate/rmed

REVIEW

Integrating pulmonary rehabilitation into the

multidisciplinary management of lung
cancer: A review
Hiram Rivas-Perez*, Patrick Nana-Sinkam 1

Wexner Medical Center at the Ohio State University Division of Pulmonary, Allergy, Critical Care, and
Sleep Medicine, USA

Received 6 May 2014; accepted 3 January 2015

Available online 22 January 2015

KEYWORDS Summary
Cancer; Introduction: Lung cancer is the number one cause of cancer related deaths. It is increasingly
Lung; recognized that a multidisciplinary approach to the diagnosis and management of patients with
Radiation; lung cancer represents the ideal model for health care delivery. Given the high incidence of
Rehabilitation; comorbid lung disease in lung cancer patients, strategies targeted at improving or optimizing
Pulmonary; these conditions may improve outcomes. Pulmonary rehabilitation (PR) has proven to be a use-
Chemotherapy ful management strategy for patients with chronic lung diseases including chronic obstructive
pulmonary disease, interstitial lung disease and pulmonary hypertension.
Discussion: PR improves both exercise capacity and dyspnea. The effects of PR have also been
studied in patients with lung cancer prior to and following surgical resection. Investigators
have demonstrated significant improvements in six minute walk distance and lower extremity
strength. In addition, patient recovery time is shorter when inpatient pulmonary rehabilitation
is integrated prior to or following surgery. There are also positive reports regarding the bene-
fits of exercise training in lung cancer patients receiving definite chemotherapy and radio-
therapy. Pilot studies have demonstrated improvement in dyspnea scores as well as exercise
capacity objectively measured by six minute walk distance. PR also offers an educational
component in which patients have the opportunity to be educated regarding management of
their disease as well as discuss goals of care.

* Corresponding author. University of Louisville Medical Center, Division of Pulmonary, Allergy, Critical Care, and Sleep Medicine, 550 S.
Jackson St., Louisville, KY 40245, USA.
E-mail addresses: Hiram.Rivasperez@louisville.edu (H. Rivas-Perez), Patrick.Nana-Sinkam@osumc.edu (P. Nana-Sinkam).
1
Wexner Medical Center Division of Pulmonary, Allergy, Critical Care, and Sleep Medicine, 201 Davis Heart and Lung Research Institute,
473 W 12th Ave., Columbus, OH 43210, USA.

http://dx.doi.org/10.1016/j.rmed.2015.01.001
0954-6111/Published by Elsevier Ltd.
438 H. Rivas-Perez, P. Nana-Sinkam

Conclusion: PR can be included as the standard of care for patients with advanced lung cancer
with the goal of optimizing quality of life. Here, we provide a review of the current knowledge
regarding PR in the management of patients with lung cancer.
Published by Elsevier Ltd.

Contents
Introduction . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . 438
Pulmonary rehabilitation . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . 438
Lung cancer burden on quality of life and exercise capacity . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . 439
Pulmonary rehabilitation after surgery . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . 439
Pulmonary rehabilitation before surgery . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . 440
Pulmonary rehabilitation for non-surgical candidates . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . 440
Pulmonary rehabilitation and nutrition . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . 440
Education and palliative interventions . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . 441
Barriers to referral for pulmonary rehabilitation . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . 441
Conclusions . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . 441
Conflict of interest . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . 441
References . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . 441

Introduction Pulmonary rehabilitation

Lung cancer is a devastating disease that carries tremen-
dous social and economic burden. While the overall five
year survival remains poor, targeted therapeutics, early
detection and multidisciplinary approaches to diagnosis
and management are all likely to contribute to improved
outcomes. One key component to an integrated approach
to patients with lung cancer is the consideration of
smoking related comorbidities and complications related
to chemo- and radiotherapy. Pulmonary rehabilitation
(PR) has emerged as a cost effective intervention and has
been proven to improve the quality of life of patients with
chronic lung diseases, particularly Chronic Obstructive
Pulmonary Diseases (COPD). Patients who suffer from such
chronic pulmonary diseases including COPD and pulmonary
fibrosis often have diminished exercise capacity and
increased respiratory symptoms. These pulmonary dis-
eases often coexist with lung cancer. Lung cancer inci-
dence in patients with COPD is 8.5% [1] and 6e15% in
patients with interstitial lung diseases [2e4]. In addition,
patients with lung cancer are particularly susceptible to
pulmonary complications from both radiotherapy and
chemotherapy and at higher risk for post-surgical compli-
cations. The primary goal of PR is to improve pulmonary
symptoms in a multidisciplinary and personalized manner.
To date, the role of PR in the setting of lung cancer
therapy remains relatively unexplored. Here, we review
the current literature regarding the potential role for
integrating PR into the management of lung cancer with a
particular focus on the appropriate timing for such an
intervention.
Chronic respiratory conditions can lead to an increase in
ventilatory requirements with muscle fatigue and reduced
exercise capacity which may ultimately impact quality of life
[5]. PR is an evidence-based, multidisciplinary comprehensive
exercise program targeted to patients with symptomatic
chronic respiratory diseases [6]. The goal of such an exercise
program is to optimize pulmonary function and thus the pa-
tient’s ability to function despite disease. PR integrates ex-
ercise and educational interventions into an individualized
treatment program. A standard PR protocol consists of three
sessions of thirty to ninety minutes per week for 6e8 weeks
consisting of individualized aerobic exercise and strength
training. Patients enrolled in PR have access to several types of
training including: treadmill, stationary bicycle, NU-Step,
upper body resistance training and training in breathing
techniques. The benefits of exercise training in patients with
cardiopulmonary diseases such COPD have been well docu-
mented [6e8] in the literature. The Joint American College of
Chest Physicians clinical practice guidelines reviewed all
available evidence on the effects of PR in COPD. They high-
lighted statistically significant improvements in six minute
walk distance, lower and upper extremities muscle strength,
and health status measures (Health Related Quality of life, St.
George’s Respiratory Questionnaire, Short form 36 health
survey) [7]. PR also reduced COPD exacerbations and number
of hospital days [7]. PR has also been shown to improve exer-
cise capacity and quality of life in patients with restrictive lung
disease and pulmonary hypertension receiving medical ther-
apy [9,10]. PR also integrates an educational component that
includes nutrition, smoking cessation, breathing exercises,
Pulmonary rehabilitation for lung cancer 439

Table 1 Pulmonary rehabilitation for lung cancer patients undergoing surgery.

Study Type of study n Start of PR Duration Results p value
of PR
Spruit MA Non-randomized 10 3 months 8 weeks Change in 6 MW of þ145 m; þ43.2% 0.002
et al., 2006 pilot study post-op from initial
Cesario Non-randomized 26 26 days change of 6 MW þ 95.2 m 0.01
et al., 2007 pilot study
Stigt et al., 2013 Randomized 57 1 month 12 weeks 6 MW change of þ35 m <0.024
prospective post-discharge (study group) vs 59 m (control)
Arbane Randomized 53 1 day post-op 5 days 6 MW change 0.05
et al., 2011 prospective Negative 131.6 m; quadriceps strength
change 4.0 kg
Cesario Pilot Study 8 Pre-operative 4 weeks 6 MW change of þ79.0 m <0.05
et al., 2007
Bobbio Prospective 12 Pre-operative 4 weeks VO2/max (ml/kg/min) change <0.001
et al., 2008 from 13.5 to 16.3
Bagan P Prospective 20 Pre-operative 3 weeks VO2/max <0.0001
et al., 2013 Increase of 12%
Divisi et al., 2013 Prospective 27 Pre-operative 4 weeks VO(2)max increase 0.00001
of de 12.9  1.8 a 19.2  2.1 ml/kg/min
Benzo et al., 2011 Randomized 10 Pre-operative 4 weeks PR had less hospital days 0.058
prospective
*6 MW: six-minute walk; m: meters.

and psychosocial interventions. PR also provides education to
the patient regarding their current plan for medical therapy.
Interestingly, PR has not been extensively studied in the
setting of other chronic respiratory diseases. It would stand to
reason that similar to COPD, other respiratory conditions could
benefit from the improvements in both muscle strength and
health quality afforded by PR. PR can also provide patients
with an opportunity to adapt to new therapeutic strategies
such as chemotherapy, lung transplant, lung volume reduction
surgery and non-invasive ventilation [7].
Lung cancer burden on quality of life and
exercise capacity
Lung cancer is the leading cause of cancer death in the
world [11]. In the United States, the overall 5-year survival
rate of lung cancer is 16% [12]. Survival has improved with
advances in treatment modalities. Given the high incidence
of comorbid lung illness observed in lung cancer patients,
patients are particularly at risk for exercise intolerance and
impaired pulmonary function in the setting of both surgery
and chemo-radiation [13]. Performance status is an essen-
tial determining factor in therapeutic decisions and in some
cases can exclude a patient from receiving any therapy. In
addition, concomitant chronic respiratory disease contrib-
utes to a higher incidence of lung toxicity in patients
receiving chemo- or radiotherapy which may aggravate
respiratory symptoms [14].
Breathlessness affects quality of life. Minimal nursing
interventions such as relaxation and breathing exercises
have been shown to improve performance status, and
physical and emotional states [15]. Hence, PR is a good
intervention for these patients with chronic lung disease.
Evidence supporting the benefits of PR in patients with lung
cancer is limited to certain clinical settings.
Pulmonary rehabilitation after surgery
Patients undergoing lung resection surgery are prone to a
decline in exercise capacity within one month of lobectomy
with capacity eventually returning back to baseline within a
year following surgery [16,17]. PR has been studied in pa-
tients with lung cancer undergoing lung resection surgery
(Table 1). In particular, PR has been used to prevent sig-
nificant impairments in exercise capacity and respiratory
symptoms following surgery. Spruit et al. demonstrated in a
pilot study that patients had a significant improvement in
exercise capacity following an 8 week inpatient PR program
following surgery. This improvement was objectively
measured by six minute walk distance and muscle strength
[13]. There were no changes in pulmonary function test
(PFT) values such as Forced Expiratory Volume in one sec-
ond (FEV1), Forced Vital Capacity (FVC) and Diffusion Ca-
pacity of the Lung for carbon monoxide (DLCO). A study by
Cesario et al. reported similar results. In an independent
study, they enrolled patients who had undergone lung
resection surgery into an aggressive inpatient PR program.
The regimen consisted of three times a week sessions of PR
for a total of 4 weeks. They reported a statistically signif-
icant improvement in dyspnea symptoms as measured by
the Borg scale. Patients also exhibited marked improve-
ments in six minute walk distance and an increase in FEV1
and FVC [18]. Investigators have reported some disadvan-
tages to implementing PR soon after surgery. Patients
tended to report more pain when PR was started immedi-
ately after surgery. Thus, a delay of instituting PR until 3
months post-operatively has been suggested [19].
Introducing PR following surgery seems to be the most
appropriate time; however, the optimal duration of PR re-
mains unclear. PR lasting more than 2 weeks has been
shown to lead to improved outcomes [17,18]. Lastly, those
440
Table 2 Pulmonary rehabilitation for patients with locally advanced NSCLC.
Study/year Type of study n Type Initiation of PR
of cancer
Glatkki Retrospective 47 NSCLC After cancer treatment
et al., 2012 (27)
Shannon Prospective 189 NSCLC After cancer treatment
et al., 2011 (28) (n Z 113)
During cancer treatment
(n Z 76)
Pasaqua Prospective 25 NSCLC After cancer treatment
et al., 2012 (29)
*6 MW: six-minute walk; m: meters.
studies demonstrating no benefit of inpatient PR may be
attributable to the short duration of the exercise regimen
[20].
Pulmonary rehabilitation before surgery
PR has been shown to decrease post-operative complica-
tions as well as hospital length of stay in patients who un-
dergo lung resection [21]. PR increases preoperative oxygen
consumption (VO2) and six minute walk distance. These
changes contribute to prompt recovery from major thoracic
surgery. Combining PR with physiotherapy also leads to a
lower incidence of atelectasis and hospital acquired in-
fections [21]. Studies also show that patients in particular
with worse baseline pulmonary function prior to surgery
benefit from pre-operative PR [22e24]. The morbidity and
length of stay decreases when lung cancer patients undergo
PR prior to pneumonectomy or lobectomy [24]. A 4e6-week
program prepares the lung cancer and COPD patients
properly for surgery by reducing their functional limitations
[25].
It is also worth noting that similar to post-operative PR,
one of challenges during the pre-operative period is
determining the optimal initiation time and duration of PR.
Given the potential delays imposed by preoperative PR,
randomized trials addressing this question have been
limited but should be conducted [26].
Pulmonary rehabilitation for non-surgical
candidates
There is very limited data in the literature examining the
potential benefits of PR in patients with advanced lung
cancer deemed not to be surgical candidates. Chemo-
therapy and radiotherapy can lead to significant pulmonary
complications. Furthermore, fatigue, cachexia and weak-
ness, among other side effects, can also be a result of
treatment thus, significantly impacting quality of life.
Chemotherapeutic agents can also cause parenchymal lung
injury leading to significant respiratory symptoms. In-
fections and hospitalizations have also been associated
with poor performance levels during cancer treatment.
The radio-sensitization produced by chemotherapy when
given concomitantly with radiation has been shown to
improve survival in patients with unresectable disease [27];
H. Rivas-Perez, P. Nana-Sinkam
Outcomes p value
Mean increase in 6 MW, 41 m <0.001
Patients undergoing cancer treatment <0.001
and PR had larger improvements
of 6 MW (þ92.5 m vs þ64.3 m)
Mean change in six minute 0.003
walk þ 62.73 m
however, unfortunately, concurrent therapy often results in
an increase in pulmonary complications including pneu-
monitis. Hanna et al. reported a significant incidence of
pneumonitis in patients who underwent chemo-radiation
followed by Docetaxel consolidation. Most of the patients
in the Docetaxel group harbored reduced baseline pulmo-
nary function with a FEV1 less than 2 L/minute [14]. Thus,
impairment in baseline pulmonary capacity is likely to
predict an increased risk for complications produced by
chemo-radiation. PR is thought to be a useful tool one
month after lung cancer therapy (either surgery, chemo-
therapy, radiation or a combination of these interventions).
PR leads to improvements in exercise capacity. Improve-
ments in pulmonary function tests changes were indepen-
dent of presence of COPD [28].
The efficacy of PR in patients undergoing chemo-
radiation therapy has been examined in pilot studies
(Table 2) [29,30]. Exercise tolerance, as measured by the
six minute walk test, decreases significantly following
chemo-radiation for lung cancer [18]. Inpatient rehabilita-
tion has been tested in patients receiving definitive cancer
treatment who are deemed not to be adequate surgical
candidates. This program consisted of four weeks of
treadmill or exercise cycling with patients reaching 80% of
their predicted maximum exercise capacity. Investigators
reported a statistically significant improvement in the six
minute walk distance among patients that underwent
inpatient PR following radical chemo-radiation [30]. There
are also reported benefits of exercise performance when PR
is performed concomitantly with chemo-radiation [29,30].
Pulmonary rehabilitation and nutrition
Approximately 20e35% of patients with COPD, have muscle
wasting and malnutrition due to their inability to compen-
sate for energy expenditures [31]. Increments in caloric
intake during PR resulted in positive outcomes for patients
with COPD. Steiner and colleagues followed 85 patients
with COPD undergoing PR. One group received a 570 kcal
carbohydrate rich supplement diet and the other group
received a non-nutritive placebo daily for the duration of a
7 week outpatient PR. Patients with a body mass index
greater than 19 kg/m2 prior to PR that were supplemented
with 570 kcal carbohydrate diet had better exercise per-
formance [32].
Pulmonary rehabilitation for lung cancer
Most lung cancer patients suffer from similar nutritional
issues. PR offers the opportunity to educate patients about
maintaining the proper diet. A combination of increased
caloric intake, exercise and in some instances, anabolic
steroids, may produce significant weight gain [33]. At the
end of PR, patients are able continue a healthy diet and are
educated on strategies to improve their nutritional needs if
necessary.
Education and palliative interventions
Proper communication between health care providers, pa-
tients and family members leads to efficient overall care
for chronic conditions. Setting short term and long term
goals helps patients understand the disease, the treatment
and provides coping mechanisms [34]. In an attempt to
offer individualized treatment, PR also provides patients
with this kind of education. Patients are educated both
about their disease and prognosis.
Smoking cessation interventions are also another
important part of PR. Studies evaluating smoking cessation
when included in the PR regimen in patients undergoing
lung cancer surgery had no impact on outcomes. However,
in this particular study patients differed in baseline char-
acteristics and the groups were not further divided ac-
cording to those who were at higher risk for post-operative
complications (pneumonectomy versus lobectomy) [35].
Pulmonary rehabilitation personnel also provide pallia-
tive care by treating symptoms, discussing goals of care,
and providing hospice care referrals when indicated [36].
This is of particular importance given that lung cancer pa-
tients have a complicated disease course and management
which may not necessarily be efficient in terms of time
commitment to follow up appointments with primary care
physicians. PR can easily facilitate discussions regarding
goals of care.
Barriers to referral for pulmonary
rehabilitation
PR has become standard of care for patients with stable
COPD that meet criteria for referral [6]. Possible barriers to
lack of referral in patients with lung cancer include: lack of
knowledge of available PR services, patient unwillingness
to participate, lack of physician education regarding whom
to refer and lack of access to PR services [37]. In addition,
patients are often poorly informed about PR and its po-
tential benefits. This lack of education regarding the types
of exercise regimens that can produce increased strength,
longer endurance and improvement of respiratory symp-
toms remains a major barrier that contributes to poor pa-
tient enrollment to PR [38].
Conclusions
PR is a minimally invasive therapeutic intervention that
offers patients multiple tools to improve their respiratory
symptoms and quality of life. PR success for lung cancer
patients has been observed in various settings. Current
studies show that intensive inpatient rehabilitation when
441
introduced either immediately prior to or after surgery
when done for a duration of more than 4 weeks leads to
fewer post-operative complications. It also improves the
quality of life for non-surgical patients who are receiving
chemotherapy and radiotherapy. Prospective randomized
trials focusing on examining the effects of PR in the lung
cancer population with special attention to duration and
ideal time for initiation are still lacking. Currently the
EXHALE trial will look for the effects of PR versus standard
of care in patients with lung cancer [39]. If there are pos-
itive outcomes in such studies, PR should eventually
become an integral part of the standard of care for patients
with lung cancer. Nevertheless, PR should still be consid-
ered a viable option for improving exercise capacity and
quality of life in lung cancer patients.
Conflict of interest
Hiram Rivas-Perez: No conflicts to disclose.
Patrick Nana-Sinkam: Other grant monies from National
Cancer Institute on 10/2013 and 2/2011.
References
[1] De Torres JP, Marı́n JM, Casanova C, Cote C, Carrizo S,
Cordoba-Lanus E, Baz-Dávila R, Zulueta JJ, Aguirre-Jaime A,
Saetta M, Cosio MG, Celli BR. Lung cancer in patients with
chronic obstructive pulmonary disease incidence and pre-
dicting factors. Am J Respir Crit Care Med 2011 Oct 15;184(8):
913e9.
[2] Asada K, Mukai J, Ougushi F. Characteristics and management
of lung cancer in patients with idiopathic pneumonia. Jpn J
Thor Dis 1992;51:214e9.
[3] Ogura T, Kondo A, Sato A, Ando M, Tamura M. Incidence and
clinical features of lung cancer in patients with idiopathic
interstitial pneumonia. Nihon Kyobu Shikkan Gakkai Zasshi
1997;35:294e9.
[4] Takiguchi Y, Nagao K, Cho K, Kuriyama T. Coincidence of lung
cancer in patients with idiopathic pulmonary fibrosis. Respi-
ration 1993;12:120e5.
[5] Rochester CL. Exercise training in chronic obstructive pulmo-
nary disease. J Rehabil Res Dev 2003 Sep-Oct;40(5 Suppl. 2):
59e80.
[6] Nici L, Donner C, Wouters E, Zuwallack R, Ambrosino N,
Bourbeau J, Carone M, Celli B, Engelen M, Fahy B, Garvey C,
Goldstein R, Gosselink R, Lareau S, MacIntyre N, Maltais F,
Morgan M, O’Donnell D, Prefault C, Reardon J, Rochester C,
Schols A, Singh S, Troosters T. ATS/ERS pulmonary rehabili-
tation writing committee. American Thoracic Society/Eur-
opean Respiratory Society statement on pulmonary
rehabilitation. Am J Respir Crit Care Med 2006 Jun 15;173(12):
1390e413.
[7] Ries AL, Bauldoff GS, Carlin BW, Casaburi R, Emery CF,
Mahler DA, Make B, Rochester CL, Zuwallack R, Herrerias C.
Pulmonary rehabilitation: joint ACCP/AACVPR evidence-based
clinical practice guidelines. Chest 2007 May;131(5 Suppl.):
4Se42S.
[8] Bolton CE, Bevan-Smith EF, Blakey JD, Crowe P, Elkin SL,
Garrod R, Greening NJ, Heslop K, Hull JH, Man WD,
Morgan MD, Proud D, Roberts CM, Sewell L, Singh SJ,
Walker PP, Walmsley S. British Thoracic Society guideline on
pulmonary rehabilitation in adults: accredited by NICE. British
Thoracic Society pulmonary rehabilitation guideline develop-
ment group, on behalf of the British Thoracic Society
442
standards of care committee. Thorax 2013 Sep;68(Suppl. 2):
ii1e30.
[9] Salhi B, Troosters T, Behaegel M, Joos G, Derom E. Effects of
pulmonary rehabilitation in patients with restrictive lung
diseases. Chest 2010;137(2):273e9.
[10] Fox BD, Kassirer M, Weiss I, Raviv Y, Peled N, Shitrit D,
Kramer MR. Ambulatory rehabilitation improves exercise ca-
pacity in patients with pulmonary hypertension. J Card Fail
2011 Mar;17(3):196e200.
[11] Jemal A, Bray F, Center MM, et al. Global cancer statistics. CA
Cancer J Clin 2011;61:69e90.
[12] American Cancer Society. Cancer facts & figures 2010.
Atlanta: American Cancer Society; 2010. p. 15e6.
[13] Spruit MA, Janssen PP, Willemsen SC, Hochstenbag MM,
Wouters EF. Exercise capacity before and after an 8-week
multidisciplinary inpatient rehabilitation program in lung
cancer patients: a pilot study. Lung Cancer 2006 May;52(2):
257e60.
[14] Hanna N, Neubauer M, Yiannoutsos C, McGarry R, Arseneau J,
Ansari R, Reynolds C, Govindan R, Melnyk A, Fisher W,
Richards D, Bruetman D, Anderson T, Chowhan N, Nattam S,
Mantravadi P, Johnson C, Breen T, White A, Einhorn L, Hoosier
Oncology Group; US Oncology. Phase III study of cisplatin,
etoposide, and concurrent chest radiation with or without
consolidation docetaxel in patients with inoperable stage III
non-small-cell lung cancer: the hoosier oncology group and U S
oncology. J Clin Oncol 2008 Dec 10;26(35):5755e60.
[15] Bredin M, Corner J, Krishnasamy M, Plant H, Bailey C,
A’Hern R. Multicenter randomized controlled trial of nursing
intervention for breathlessness in patients with lung cancer.
BMJ 1999 Apr 3;318(7188):901e4.
[16] Brunelli A, Xiumé F, Refai M, Salati M, Marasco R, Sciarra V,
Sabbatini A. Evaluation of expiratory volume, diffusion ca-
pacity and exercise tolerance following major lung resection:
a prospective follow-up analysis. Chest 2007;131:141e7.
[17] Nagamatsu Y, Maeshiro K, Kimura NY, Nishi T, Shima I,
Yamana H, Shirouzu K. Long-term recovery of exercise ca-
pacity and pulmonary function after lobectomy. J Thorac
Cardiovasc Surg 2007;134:1273e8.
[18] Cesario A, Ferri L, Galetta D, Pasqua F, Bonassi S, Clini E,
Biscione G, Cardaci V, di Toro S, Zarzana A, Margaritora S,
Piraino A, Russo P, Sterzi S, Granone P. Post-operative respi-
ratory rehabilitation after lung resection for non-small cell
lung cancer. Lung Cancer 2007 Aug;57(2):175e80.
[19] Stigt JA, Uil SM, van Riesen SJ, Simons FJ, Denekamp M,
Shahin GM, Groen HJ. A randomized controlled trial of
postthoracotomy pulmonary rehabilitation in patients with
resectable lung cancer. J Thorac Oncol 2013 Feb;8(2):
214e21.
[20] Arbane G, Tropman D, Jackson D, Garrod R. Evaluation of an
early exercise intervention after thoracotomy for non-small
cell lung cancer (NSCLC), effects on quality of life, muscle
strength and exercise tolerance: randomised controlled trial.
Lung Cancer 2011 Feb;71(2):229e34.
[21] Nagarajan K, Bennett A, Agostini P, Naidu B. Is preoperative
physiotherapy/pulmonary rehabilitation beneficial in lung
resection patients? Interact Cardiovasc Thorac Surg 2011;13:
300e2.
[22] Cesario A, Ferri L, Galetta D, Cardaci V, Biscione G, et al. Pre-
operative pulmonary rehabilitation and surgery for lung can-
cer. Lung Cancer 2007;57:118e9.
[23] Bobbio A, Chetta A, Ampollini L, Primomo GL, Internullo E,
Carbognani P, Rusca M, Olivieri D. Preoperative pulmonary
rehabilitation in patients undergoing lung resection for non-
small cell lung cancer. Eur J Cardiothorac Surg 2008 Jan;
33(1):95e8.
[24] Bagan P, Oltean V, Ben Abdesselam A, Dakhil B, Raynaud C,
Couffinhal JC, De Crémoux H. Pulmonary rehabilitation and
H. Rivas-Perez, P. Nana-Sinkam
non-invasive ventilation before lung surgery in very high-risk
patients. Rev Mal Respir 2013 May;30(5):414e9.
[25] Divisi D, Di Francesco C, Di Leonardo G, Crisci R. Preoperative
pulmonary rehabilitation in patients with lung cancer and
chronic obstructive pulmonary disease. Eur J Cardiothorac
Surg 2013 Feb;43(2):293e6.
[26] Benzo R, Wigle D, Novotny P, Wetzstein M, Nichols F, et al.
Preoperative pulmonary rehabilitation before lung cancer
resection: results from two randomized studies. Lung Cancer
2011;74:441e5.
[27] Furuse K, Fukuoka M, Kawahara M, Nishikawa H, Takada Y,
Kudoh S, Katagami N, Ariyoshi Y. Phase III study of concurrent
versus sequential thoracic radiotherapy in combination with
mitomycin, vindesine, and cisplatin in unresectable stage III
non-small-cell lung cancer. J Clin Oncol 1999 Sep;17(9):
2692e9.
[28] Glattki GP, Manika K, Sichletidis L, Alexe G, Brenke R,
Spyratos D. Pulmonary rehabilitation in non-small cell lung
cancer patients after completion of treatment. Am J Clin
Oncol 2012 Apr;35(2):120e5.
[29] Shannon V, Maldonado J, Thurman C. Timing of pulmonary
rehabilitation (PR) relative to cancer treatments impacts PR
benefits among patients with NSCLC and moderate to severe
COPD. Chest Oct 2011;140(4). Meeting Abstracts.
[30] Pasqua F, D’Angelillo R, Mattei F, Bonassi S, Biscione GL,
Geraneo K, Cardaci V, Ferri L, Ramella S, Granone P, Sterzi S,
Crisafulli E, Clini E, Lococo F, Trodella L, Cesario A. Pulmonary
rehabilitation following radical chemo-radiation in locally
advanced non surgical NSCLC: preliminary evidences. Lung
Cancer 2012 May;76(2):258e9.
[31] Schols AMWJ, Soeters PB, Dingemans AMC, Mostert R,
Frantzen PJ, Wouters EFM. Prevalence and characteristics of
nutritional depletion in patients with stable COPD eligible for
pulmonary rehabilitation. Am Rev Respir Dis 1993;147:
1151e6.
[32] Steiner MC, Barton RL, Singh SJ, Morgan MD. Nutritional
enhancement of exercise performance in chronic obstructive
pulmonary disease: a randomized controlled trial. Thorax
2003;58:745e51.
[33] Schols AM, Slangen J, Volovics L, Wouters EF. Weight loss is a
reversible factor in the prognosis of chronic obstructive pul-
monary disease. Am J Respir Crit Care Med 1998;157:1791e7.
[34] Von Korff M, Gruman J, Schaefer J, Curry S, Wagner E.
Collaborative management of chronic illness. Ann Intern Med
1997 Dec;127(12):1097e102.
[35] Schmidt-Hansen M, Page R, Hasler E. The effect of preoper-
ative smoking cessation or preoperative pulmonary rehabili-
tation on outcomes after lung cancer surgery: a systematic
review. Clin Lung Cancer 2013 Mar;14(2):96e102.
[36] Reticker AL, Nici L, ZuWallack R. Pulmonary rehabilitation and
palliative care in COPD: two sides of the same coin? Chron
Respir Dis 2012 May;9(2):107e16.
[37] Nwosu AC, Bayly JL, Gaunt KE, Mayland CR. Lung cancer and
rehabilitationewhat are the barriers? Results of a question-
naire survey and the development of regional lung cancer
rehabilitation standards and guidelines. Support Care Cancer
2012 Dec;20(12):3247e54.
[38] Cheville AL, Dose AM, Basford JR, Rhudy LM. Insights into
the reluctance of patients with late-stage cancer to adopt
exercise as a means to reduce their symptoms and improve
their function. J Pain Symptom Manage 2012 Jul;44(1):
84e94.
[39] Quist M, Langer SW, Rorth M, Christensen KB, Adamsen L.
“EXHALE”: exercise as a strategy for rehabilitation in
advanced stage lung cancer patients: a randomized clinical
trial comparing the effects of 12 weeks supervised exercise
intervention versus usual care for advanced stage lung cancer
patients. BMC Cancer 2013 Oct 14;13:477.