Online Exclusive Article

Effect of Exercise Interventions on Quality of Life in Patients With Lung Cancer: A Systematic Review of Randomized Controlled Trials

Rui-Chen Ma

Ying-Ying Yin

Xin Liu

Ya-Qing Wang

Jiao Xie
lung cancer, exercise, quality of life, systematic review
ONF 2020, 47(3), E58-E72. DOI: 10.1188/20.ONF.E58-E72

Problem Identification: Improving quality of life (QOL) is a key issue for patients with lung cancer. Exercise interventions could positively affect patients’ QOL; however, there is no clear-cut understanding of the role of exercise in improving QOL in patients with lung cancer.

Literature Search: The PubMed®, Embase®, Cochrane Library, and Web of Science electronic databases were searched from inception to September 6, 2019.

Data Evaluation: 16 randomized controlled trials met the inclusion criteria. A qualitative synthesis method was used to identify the effect of exercise interventions on QOL in patients with lung cancer.

Synthesis: This review indicates that exercise interventions may have beneficial effects on the QOL of patients with lung cancer. The effectiveness seems to be affected by the duration of the intervention, as well as exercise frequency, intensity, and adherence.

Implications for Practice: Exercise interventions can be integrated into management plans for patients with lung cancer to improve their QOL. Healthcare providers should consider developing optimal exercise prescriptions to maximize the results for this population.

Jump to a section

    Lung cancer remains the leading cause of cancer morbidity and mortality worldwide and represents close to one in five cancer deaths (Bray et al., 2018; Siegel et al., 2020). Compared with patients with other types of cancer, patients with lung cancer have been reported to experience more disease burden and symptom distress, as well as have poorer physical functioning and health-related quality of life (QOL) (Henshall et al., 2019; Hung et al., 2011; Ostroff et al., 2011; Paramanandam & Dunn, 2015). With the improvement of various treatment methods, the survival rate of individuals with lung cancer has steadily improved. QOL is increasingly recognized as an important topic for such populations, and QOL has gradually become an integral end point in clinical trials.

    QOL is a multidimensional concept that reflects the patient-perceived evaluation of one’s health, including the physical, emotional, and social dimensions, and symptoms related to disease or treatment (Fiteni et al., 2016). Patients with lung cancer experience numerous adverse outcomes related to disease or treatment, including dyspnea, cough, pain, and fatigue, all of which are a major detriment to their QOL. Following a diagnosis of lung cancer, which is a traumatic stressor, patients often show negative emotions, such as anxiety and depression, because of the anticipation of negative outcomes and the fear of death, which have a significant impact on patients’ QOL and even disease progression (Pompili et al., 2013). Studies have also revealed that, following lung resection surgery, QOL can further decline significantly because of postoperative complications and functional disability (Balduyck et al., 2007; Handy et al., 2002; Pompili, 2015; Yip et al., 2018). In addition, the QOL of patients with advanced lung cancer is significantly reduced because of high tumor burden, as well as side effects and toxicities of chemotherapy or radiation therapy, such as nausea and vomiting (Akin et al., 2010). Considering that QOL is an important measure of cancer survivorship because it provides prognostic and predictive information, and given patients’ subjective experiences with therapeutic and lifestyle interventions, it is necessary to explore interventions that can effectively improve the QOL of patients with lung cancer (Mishra et al., 2012).

    The benefits of exercise on QOL are gaining widespread attention because they have the potential to improve physical and psychological functioning, thereby improving QOL. Exercise is a well-planned physical activity, including aerobic, resistance, or endurance exercise, all of which aim to improve physical fitness (Paramanandam & Dunn, 2015). Exercise is recognized as a core component of pulmonary rehabilitation to manage symptoms in individuals with chronic respiratory diseases. In addition, increasing evidence supports exercise training as an important component in oncology rehabilitation, and exercise interventions seem to be safe and well tolerated by patients with cancer (Heywood et al., 2017). Physical activity guidelines have noted that patients with cancer are supposed to participate in exercises as actively as their physical conditions permit (Carlson et al., 2010). To effectively perform exercise training to improve aerobic capacity and muscle strength, the total training load must exceed the load encountered in daily life, progress as improvement occurs, and reflect the specific requirements of the individual (Spruit et al., 2013).

    Published reviews assessing the effectiveness of exercise on clinical outcomes among patients with lung cancer were limited because they did not focus on QOL outcomes (Cavalheri & Granger, 2017; Henshall et al., 2019; Li et al., 2019), reached conflicting QOL results because of the small sample size (Cavalheri et al., 2014; Li et al., 2017; Sommer et al., 2018), or used a limited randomized design (Granger et al., 2011; Ni et al., 2017; Pouwels et al., 2015; Sebio García et al., 2016). Meta-analyses have shown that exercise interventions can improve QOL in individuals with cancer (Buffart et al., 2017; Gerritsen & Vincent, 2016; Sweegers et al., 2018). However, most of the included studies have focused on patients with breast cancer and other cancer types, with low representation of patients with lung cancer. Compared with other cancers, patients with lung cancer experience greater symptom distress and have distinct characteristics, such as being older, having more comorbidities, and having poorer prognosis (Henshall et al., 2019). Therefore, it is necessary to be cautious in generalizing the results to this population. To the authors’ knowledge, the effect of exercise interventions on the QOL of patients with lung cancer has not yet been thoroughly analyzed. The focus of this article was to conduct a comprehensive evaluation of existing randomized controlled trials (RCTs) and investigate the effect of an exercise intervention on QOL outcomes in patients with lung cancer.

    Methods

    The systematic review was conducted and reported according to the PRISMA (Preferred Reporting Items for Systematic Reviews and Meta-Analyses) guidelines (Moher et al., 2009).

    Search Strategy

    A comprehensive literature search of PubMed®, Web of Science, Cochrane Library, and Embase® was performed to identify relevant studies. All databases were searched from inception to September 6, 2019, using the following MeSH (Medical Subject Headings) terms and keywords: quality of life and lung cancer and randomly, with exercise intervention terms such as exercise, physical activity, breathing exercises, yoga, tai chi, and qi gong. The search strategies were customized for each database, and the authors also checked the references of relevant reviews in detail and included studies manually to ensure that no studies were missing.

    Selection Criteria

    All included studies in the review met the criteria described according to PICOS (participants, intervention, comparison, outcome, and study design). Specifically, the criteria were as follows:

    •  Participants: participants diagnosed with lung cancer, including those at any age and at any stage of the disease; participants from the entire spectrum of cancer treatment were considered for review.

    •  Intervention: exercise training program, which was defined as a regimen of physical activities (such as resistance exercise and aerobic exercise, either alone or as a part of comprehensive pulmonary rehabilitation program, which also included components of breathing exercises, education, and psychological care)

    •  Comparison: no formal exercise interventions

    •  Outcome: QOL as an outcome and measured using validated scales

    •  Study design: RCTs

    The exclusion criteria were as follows: mixed cancer population; protocols, conference summaries, theses, and letters; full-text articles not published in a peer-reviewed journal; study written in a language other than English; and the intervention group only performed breathing exercises, such as inspiratory muscle training alone. When there may have been an overlap in patient cohorts with another study, the earliest published article was included. Two reviewers (M.R.C. and Y.Y.Y.) selected the studies independently by viewing the titles and abstracts and conducted a full-text review to identify potential relevant articles. If there was an inconsistency, consensus was reached through discussion with another reviewer (L.X.).

    Data Extraction

    Data from the included studies were extracted using the predesigned data extraction forms. The following characteristics were extracted: authors, countries, and sample sizes; the timing and duration of the intervention and exercise frequency and type; and controls, assessment tools, and results. A meta-analysis was not feasible because of the heterogeneity of disease stages, exercise programs, and QOL measurement tools. Therefore, the authors conducted a systematic review of outcomes.

    Risk-of-Bias Assessment

    The Cochrane Collaboration risk-of-bias tool (Higgins & Green, 2008) was used to determine if the included studies had bias risk, including selection bias, performance bias, detection bias, attrition bias, reporting bias, and other bias. Each potential source of bias was graded as high, low, or unclear. Two authors (M.R.C. and Y.Y.Y.) evaluated the included studies independently, and different opinions were discussed with another author (W.Y.Q.). The authors included trials of all qualities and did not exclude poor-quality studies because of the small number of studies found.

    Results

    Study Selection

    The flowchart of the trial retrieval process is shown in Figure 1. A total of 928 records were identified, and 498 records remained after duplicate checking. After the titles and abstracts were screened, 428 additional records were excluded. The remaining 70 records were assessed by browsing the full texts, and most of the studies were excluded because they did not contain QOL outcomes or did not have an RCT design. Eventually, 16 studies were retained and included in qualitative synthesis (Arbane et al., 2011, 2014; Cavalheri et al., 2017; Dhillon et al., 2017; Edbrooke et al., 2019; Edvardsen et al., 2015; Egegaard et al., 2019; Granger et al., 2013; Henke et al., 2014; Hwang et al., 2012; Jastrzębski et al., 2015; Lai et al., 2017; Messaggi-Sartor et al., 2019; Morano et al., 2014; Sebio García et al., 2017; Stigt et al., 2013).

    Study Characteristics

    Participants: The included studies were conducted worldwide, were published between 2011 and 2019, and included a total of 758 patients from 10 countries: Australia (n = 4), China (n = 2), Spain (n = 2), United Kingdom (n = 2), Brazil (n = 1), Denmark (n = 1), Germany (n = 1), New Zealand (n = 1), Norway (n = 1), and Poland (n = 1). The median sample size was 33 (range = 15–131), and 379 participants were allocated to an intervention program. Seven studies specifically targeted participants following surgery (Arbane et al., 2011, 2014; Cavalheri et al., 2017; Edvardsen et al., 2015; Granger et al., 2013; Messaggi-Sartor et al., 2019; Stigt et al., 2013), three studies targeted preoperative participants (Lai et al., 2017; Morano et al., 2014; Sebio García et al., 2017), and six studies targeted participants in the advanced stage of lung cancer (Dhillon et al., 2017; Edbrooke et al., 2019; Egegaard et al., 2019; Henke et al., 2014; Hwang et al., 2012; Jastrzębski et al., 2015).

    Intervention: The most common exercises included aerobic exercise, resistance exercise, and breathing exercise. The prescribed exercise programs ranged from one to seven days a week and lasted for 5–60 minutes per session. The duration of the intervention ranged from 1 week (Lai et al., 2017) to 20 weeks (Edvardsen et al., 2015), with a median of 8 weeks. The data available for participants’ adherence to the prescribed exercise programs ranged from 44%–88%. The exercise sessions were conducted in different venues: inpatient, outpatient, home-based, or mixed. Two studies provided an inpatient exercise program (Henke et al., 2014; Lai et al., 2017), 10 studies provided an outpatient hospital-based exercise program (Cavalheri et al., 2017; Dhillon et al., 2017; Edvardsen et al., 2015; Egegaard et al., 2019; Hwang et al., 2012; Jastrzębski et al., 2015; Messaggi-Sartor et al., 2019; Morano et al., 2014; Sebio García et al., 2017; Stigt et al., 2013), 1 study provided a home-based exercise program (Edbrooke et al., 2019), and 3 studies provided a mixed exercise program (Arbane et al., 2011, 2014; Granger et al., 2013). Physiotherapists were employed to assist and supervise participants in the studies conducted in hospital settings, and patients who exercised at home were instructed but not closely supervised.

    Regarding control or comparison groups, 13 studies used usual cancer care or no intervention, whereas three studies used chest physical therapy, respiratory management, or conventional physiotherapy. Adherence rates were examined in nine studies (Cavalheri et al., 2017; Dhillon et al., 2017; Edbrooke et al., 2019; Edvardsen et al., 2015; Egegaard et al., 2019; Granger et al., 2013; Hwang et al., 2012; Messaggi-Sartor et al., 2019; Stigt et al., 2013), ranging from 44% (Cavalheri et al., 2017) to 88% (Edvardsen et al., 2015; Egegaard et al., 2019). Only one home-based exercise study reported that adherence data were assessed from patient self-report (exercise diary and weekly telephone call) (Edbrooke et al., 2019), and in the remaining studies, physiotherapists supervised inpatient or outpatient hospital-based exercise programs and assessed adherence. Participants in four studies were provided a pedometer or another activity tracker to collect activity data objectively and to facilitate greater adherence to the exercise program (Arbane et al., 2014; Cavalheri et al., 2017; Dhillon et al., 2017; Egegaard et al., 2019). More characteristics of the included studies are shown in Table 1.

    Quality Assessment

    The risk-of-bias assessment of the included studies is provided in Table 2. The randomization of patients was conducted in all studies, but the randomization process was unclear in four studies because there was insufficient information to assess it. Twelve studies performed allocation concealment prior to the assignment of patients with lung cancer. Four studies had insufficient information to assess this criterion. Because of the nature of the interventions, the blinding of patients and personnel is hardly possible. Eight studies blinded outcome assessors, whereas others were either unclear or high-risk regarding this criterion. Intention-to-treat analyses were conducted in six of the included studies, which indicated a low risk of attrition bias.

    QOL Outcomes

    QOL was the primary outcome in two studies (Arbane et al., 2011; Stigt et al., 2013). All studies used validated instruments to measure QOL; however, different tools were used. Specifically, five different tools were adopted: the European Organisation for the Research and Treatment of Cancer Quality-of-Life Questionnaire–Core 30 (EORTC QLQ-C30; n = 2), the EORTC QLQ-C30 and Lung scale (EORTC QLQ-C30-LC13; n = 8), the SF-36® general health survey (n = 11), the Functional Assessment of Cancer Therapy–Lung scale (FACT-L; n = 3), and St. George’s Respiratory Questionnaire (SGRQ; n = 1). Eight studies included only one tool, and eight included more than one tool to measure QOL.

    QOL Results

    The authors divided the studies included in this review into three distinct subgroups according to the timing of the intervention delivery: patients who were preoperative, patients who were postoperative, and patients with advanced disease. Three studies investigated preoperative exercise programs; two studies (Morano et al., 2014; Sebio García et al., 2017) found that exercise intervention improved QOL, and no significant differences were observed in another study (Lai et al., 2017). Seven studies investigated postoperative exercise programs. Two studies showed that exercise could improve QOL (Edvardsen et al., 2015; Granger et al., 2013), and one study showed that exercise had a significant benefit on QOL in a subgroup of patients with airflow obstruction (Arbane et al., 2014). However, the remaining four studies found no improvements in QOL (Arbane et al., 2011; Cavalheri et al., 2017; Messaggi-Sartor et al., 2019; Stigt et al., 2013). Six studies examined the effectiveness of exercise programs on QOL in patients with advanced disease. Three studies (Edbrooke et al., 2019; Henke et al., 2014; Hwang et al., 2012) reported a significant effect of exercise on QOL compared with that of patients in the control groups, one study (Jastrzębski et al., 2015) showed a borderline statistically significant improvement in QOL, and the remaining two studies reported no significant differences between groups (Dhillon et al., 2017; Egegaard et al., 2019).

    Discussion

    To the authors’ knowledge, the current systematic review is the first to focus on exercise interventions with an RCT design looking specifically at QOL outcomes of patients with lung cancer. A total of 16 RCTs involving 758 participants were systematically reviewed, and there are conflicting results with respect to the effectiveness of exercise interventions on QOL for individuals with lung cancer. Seven studies observed significant effects on global or other domains of QOL, and there was evidence of improvement in the palliation of symptoms, such as dyspnea, fatigue, pain, and improvement in physical and psychological functioning. Seven studies reported no significant effect on QOL, one study showed a borderline statistically significant improvement of QOL, and one study obtained a partial significant effect only for participants with airflow obstruction. In addition, in most of the included studies, exercise interventions significantly improved other health outcomes, such as exercise capacity and muscle strength.

    It has been reported that preoperative QOL, particularly physical functioning, is associated with overall survival rate and cancer-related survival rate in early stages of non-small cell lung cancer (Pompili et al., 2013). In the preoperative subgroup, one study failed to find any significant improvement in QOL after the intervention (Lai et al., 2017). The authors found that, when analyzing the data in this study, the duration of the exercise intervention was significantly shorter: only one week. It is recommended that interventions designed to enhance cardiopulmonary function in chronic respiratory disease should generally last for 8–12 weeks, with a longer duration of intervention resulting in a better effect (Sebio García et al., 2016). Therefore, perhaps a dose–effect relationship may explain why this study failed to observe an improvement in QOL. However, considering the short time period from the diagnosis to surgery, there is evidence that two to four weeks of preoperative exercise is also feasible, but its benefits still need further confirmation (Spruit et al., 2013). The results of the remaining two studies reported that exercise interventions produced a greater improvement in QOL physical component summary scores.

    Patients undergoing lung resection usually experience various pulmonary complications, which further deteriorate their QOL (Amar et al., 2010; Balduyck et al., 2007). Compared with preoperative exercise interventions, studies investigating postoperative exercise interventions have a much longer time period. However, only two of the seven studies observed a statistical improvement in QOL in the exercise group. Arbane et al. (2011, 2014) conducted two studies showing that unsupervised home-based exercise programs did not improve QOL. Of note, a previous review has indicated that, among patients with cancer, unsupervised home-based training does not seem to have the same QOL or physical benefits observed with supervised programs (Buffart et al., 2017). Unsupervised exercise programs may cause many patients to fail to reach the prescribed exercise dose, which may be one reason for the lack of changes in QOL. In addition, these two studies (Arbane et al., 2011, 2014) did not report adherence data concerning home exercise; therefore, it is unclear how much exercise the exercise group actually performed. Another important finding is that the intervention group had varying degrees of adherence to exercise. Two studies with high adherence (mean = 80%) (Edvardsen et al., 2015; Granger et al., 2013) reported that QOL after the intervention was significantly different between the groups, whereas the other two studies with low adherence (mean = 48%) (Cavalheri et al., 2017; Stigt et al., 2013) found no differences. These findings are in line with those of a previous review showing that adherence to exercise interventions is important because it affects study outcomes (Cacciata et al., 2019). Consequently, high adherence to exercise may be a key strategy to improve QOL. Some wearable activity-monitoring devices, such as the Fitbit® tracker, can be used in future research to measure exercise dose and adherence, which are more objective than patient self-reported data. The Fitbit itself also provides activity feedback, which may motivate patients to pay attention to their activity levels and increase their physical activity (Polgreen et al., 2018).

    Given that lung cancer is often diagnosed as advanced and that patients usually do not meet the surgical criteria, interventions aimed at reducing symptom distress, and particularly those aimed at improving QOL, are particularly important for patients (Henke et al., 2014). Previous reviews have reported that the implementation of exercise interventions appears to have significant between- and/or within-group improvements in QOL, physical function, and psychosocial function in patients with advanced cancer (Heywood et al., 2018). The authors speculate that one reason why exercise interventions have positive effects on the QOL of patients with advanced lung cancer can be explained by the significantly negative effect of radiation therapy and chemotherapy on fatigue, but exercise has a positive effect on this factor (Lee et al., 2008; Mustian et al., 2017). In addition, another possible reason is that the initial QOL of patients with advanced lung cancer is low, so there is enough room for improvement and it is easier to benefit from exercise (i.e., floor effect). In the inoperable lung cancer subgroup, four studies reported that exercise made a significant difference in QOL, although one of the studies did not reach statistical significance (Jastrzębski et al., 2015). In the remaining two studies in which no improvement in QOL was observed, one was a feasibility study (Egegaard et al., 2019). Of note, feasibility or pilot studies may limit generalizability because the authors of at least one included study reported that their study was not sufficiently powered to detect changes in QOL (Messaggi-Sartor et al., 2019). The authors of the other study reported that the intervention intensity (mainly walking) may not be sufficient to observe differences between the groups (Dhillon et al., 2017). In terms of intervention intensity, the majority of studies included in this review were performed at a moderate to high intensity, which is consistent with a current guideline that recommends that patients with cancer engage in 150 minutes of moderate-intensity exercise or 75 minutes of high-intensity exercise per week (Schmitz et al., 2010). Therefore, a more intensive exercise program may be required to improve QOL. In addition, the authors found that the exercise frequency in this study was low—specifically, only once a week. As far as the authors know, there are no formal guidelines for optimal exercise frequency for patients with lung cancer. However, it has been shown that individuals with cancer should exercise regularly (i.e., at least three times a week and preferably five times a week) to improve QOL and QOL-related factors (Gerritsen & Vincent, 2016).

    The exercise interventions varied by the type of treatment (surgery or chemotherapy), the timing of exercise commencement (e.g., before or after surgery), the different duration of exercise interventions, the characteristics of exercise interventions (type, frequency, intensity), and the different settings of exercise delivery (i.e., inpatient or outpatient). These variations make it challenging to translate these findings into a definite conclusion on the effect of exercise interventions on QOL. Concerning the intervention contents, aerobic exercise, resistance exercise, and breathing exercises were the most common types among the included studies. Aerobic exercise training by bicycle or walking is the most common form of exercise in pulmonary rehabilitation and is also the first choice for improving cardiorespiratory fitness and body composition (Paramanandam & Dunn, 2015). Compared with aerobic exercise, resistance exercise improves muscle mass and strength and demands a lower level of oxygen consumption and evokes less dyspnea, which is an attractive option for patients with advanced pulmonary disease (Spruit et al., 2013). Inspiratory muscle training, which is commonly used in breathing exercises, can improve the respiratory muscle strength and endurance of patients, thereby reducing dyspnea and increasing exercise capacity. There is no report that one specific type of exercise has more advantages than another; therefore, to obtain the benefits of different types of exercise, a combination of exercises is a better choice for patients with lung cancer. In addition, the authors suggest that future studies should not only focus on the comparison between exercise interventions and a passive control group (e.g., usual care) but also compare exercise interventions with different kinds of active controls (e.g., another exercise intervention) to identify the best training method for patients to improve outcome variables.

    Most studies included in this review specifically excluded patients with risk factors for adverse events, such as hypoxia, cardiovascular diseases, or musculoskeletal diseases. The frequent exclusion of patients with these comorbidities from exercise interventions may be because of concerns about exercise safety and feasibility. In the 16 studies reviewed, 379 patients with lung cancer participated in the exercise intervention program, and 12 patients experienced an adverse event. The most serious adverse event was a patient who had a hip fracture during training (Edvardsen et al., 2015); the rest were minor adverse events, such as knee pain. Generally, exercise interventions seem to be safe and feasible for patients with lung cancer under the supervision of qualified healthcare providers with expertise in exercise delivery, which has been verified in other reviews on this topic (Henshall et al., 2019; Schmitz et al., 2010). In addition, the included studies showed that the issues affecting the uptake rate for exercise were mainly related to traffic problems near the program location. A review by Dalal et al. (2010) showed that the adherence rates of home-based cardiac rehabilitation programs are better than those of center-based programs. With the development of mobile technologies in healthcare delivery, mobile health (mHealth) technology is an effective and feasible approach to remote monitoring and rehabilitation for patients with lung cancer, which can supplement traditional healthcare center–based oncology rehabilitation programs (Ji et al., 2019; Park et al., 2019). The mHealth-based exercise program seems to be an attractive alternative for individuals who are unwilling or unable to exercise in an outpatient setting and who are also a logical choice under the limitations of the clinical environment in some areas.

    Limitations

    The advantage of the review is that the authors only included RCTs, which represent the gold standard in evaluating the most convincing evidence. However, this review still has some limitations. Because of the high heterogeneity among the included studies, it was difficult to conduct forest plots to draw quantitative conclusions and to determine whether there was publishing bias. Although the review included 16 RCTs, the sample sizes in most included studies are still relatively small, which leads to the risk of studies being underpowered, resulting in less reliable results. Patients commenced exercise interventions with different initial QOL values; therefore, there may be a ceiling or floor phenomenon that may influence the effects of an intervention, so these results must be interpreted cautiously. No studies were conducted in the United States or Canada, which revealed a lack of research evidence on exercise interventions conducted in North America and the QOL of patients with lung cancer in this setting. There is a need for well-designed research in this setting to enhance the generalizability of findings.

    Implications for Nursing

    QOL is a multifactorial concept, including the impact of disease, side effects of treatment, physical functions, and psychosocial functions (Akin et al., 2010). The concept of QOL is particularly prominent in nursing because nurses have a unique focus on holistic care, focus on patients’ QOL and survival, and play important roles in maintaining the QOL of patients with cancer (Yarbro et al., 2010). Increasing attention to QOL outcomes of patients with lung cancer could facilitate communication among patients, nurses, and other healthcare providers and enable nurses to develop innovative interventions to improve QOL in this target population (Zeng et al., 2011). Oncology nurses should educate patients with lung cancer and their families about current evidence on the use of exercise as a potential intervention to improve QOL and consider including exercise as a part of standard care for lung cancer treatment.

    The effect of exercise on QOL in individuals with lung cancer appears to be highly influenced by the features of the exercise prescription (e.g., the duration, frequency, and intensity of the intervention) and adherence. These findings highlight several factors that should be taken into account to maximize the results. Oncology nurses are encouraged to cooperate with physical therapists to develop tailored exercise programs to meet patients’ abilities and interests and to address exercise safety depending on their status. For example, short high-intensity exercise workouts with a supervised component should be conducted at least three times a week for patients with lung cancer and better physical status. For patients in poor physical condition, tolerable training should be selected to further reduce any risks related to exercise. In addition, nurses need to be knowledgeable about referral resources in their community and refer their patients to appropriate programs, such as Livestrong at the YMCA in the United States, which can provide high-quality exercise programs to various cancer survivor groups (Schumacher & McNiel, 2018).

    Conclusion

    This review shows that exercise interventions may be helpful in improving the QOL of patients with lung cancer. The authors found that the effect of exercise on QOL seems to be affected by the duration of the intervention, as well as exercise frequency, intensity, and adherence. It is still premature to draw a firm conclusion because of the heterogeneity among the included studies. In addition, perhaps the QOL of patients with lung cancer also depends on the prognosis during the disease trajectory. Larger and well-designed RCTs with QOL as a primary outcome are needed to explore the true effect of exercise on QOL in this target population.

    The authors gratefully acknowledge the School of Nursing at Jilin University for its valuable support.

    About the Author(s)

    Rui-Chen Ma, MD, MSc, Ying-Ying Yin, MD, MSc, Xin Liu, MD, MSc, and Ya-Qing Wang, MD, MSc, are graduate students and Jiao Xie, MD, PhD, is an associate professor, all in the School of Nursing at Jilin University in China. Ma and Xie contributed to the conceptualization and design. Ma and Yin completed the data collection and contributed to the manuscript preparation. Liu and Wang provided analysis. Xie can be reached at 1761458270@qq.com, with copy to ONFEditor@ons.org. (Submitted October 2019. Accepted January 21, 2020.)

     

    References

    Akin, S., Can, G., Aydiner, A., Ozdilli, K., & Durna, Z. (2010). Quality of life, symptom experience and distress of lung cancer patients undergoing chemotherapy. European Journal of Oncology Nursing, 14(5), 400–409. https://doi.org/10.1016/j.ejon.2010.01.003

    Amar, D., Munoz, D., Shi, W., Zhang, H., & Thaler, H.T. (2010). A clinical prediction rule for pulmonary complications after thoracic surgery for primary lung cancer. Anesthesia and Analgesia, 110(5), 1343–1348. https://doi.org/10.1213/ANE.0b013e3181bf5c99

    Arbane, G., Douiri, A., Hart, N., Hopkinson, N.S., Singh, S., Speed, C., . . . Garrod, R. (2014). Effect of postoperative physical training on activity after curative surgery for non-small cell lung cancer: A multicentre randomised controlled trial. Physiotherapy, 100(2), 100–107. https://doi.org/10.1016/j.physio.2013.12.002

    Arbane, G., Tropman, D., Jackson, D., & Garrod, R. (2011). 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, 71(2), 229–234. https://doi.org/10.1016/j.lungcan.2010.04.025

    Balduyck, B., Hendriks, J., Lauwers, P., & Van Schil, P. (2007). Quality of life evolution after lung cancer surgery: A prospective study in 100 patients. Lung Cancer, 56(3), 423–431. https://doi.org/10.1016/j.lungcan.2007.01.013

    Bray, F., Ferlay, J., Soerjomataram, I., Siegel, R.L., Torre, L.A., & Jemal, A. (2018). Global cancer statistics 2018: GLOBOCAN estimates of incidence and mortality worldwide for 36 cancers in 185 countries. CA: A Cancer Journal for Clinicians, 68(6), 394–424. https://doi.org/10.3322/caac.21492

    Buffart, L.M., Kalter, J., Sweegers, M.G., Courneya, K.S., Newton, R.U., Aaronson, N.K., . . . Brug, J. (2017). Effects and moderators of exercise on quality of life and physical function in patients with cancer: An individual patient data meta-analysis of 34 RCTs. Cancer Treatment Reviews, 52, 91–104. https://doi.org/10.1016/j.ctrv.2016.11.010

    Cacciata, M., Stromberg, A., Lee, J.A., Sorkin, D., Lombardo, D., Clancy, S., . . . Evangelista, L.S. (2019). Effect of exergaming on health-related quality of life in older adults: A systematic review. International Journal of Nursing Studies, 93, 30–40. https://doi.org/10.1016/j.ijnurstu.2019.01.010

    Carlson, S.A., Fulton, J.E., Schoenborn, C.A., & Loustalot, F. (2010). Trend and prevalence estimates based on the 2008 Physical Activity Guidelines for Americans. American Journal of Preventive Medicine, 39(4), 305–313. https://doi.org/10.1016/j.amepre.2010.06.006

    Cavalheri, V., & Granger, C. (2017). Preoperative exercise training for patients with non-small cell lung cancer. Cochrane Database of Systematic Reviews, 6, CD012020. https://doi.org/10.1002/14651858.CD012020.pub2

    Cavalheri, V., Jenkins, S., Cecins, N., Gain, K., Phillips, M.J., Sanders, L.H., & Hill, K. (2017). Exercise training for people following curative intent treatment for non-small cell lung cancer: A randomized controlled trial. Brazilian Journal of Physical Therapy, 21(1), 58–68. https://doi.org/10.1016/j.bjpt.2016.12.005

    Cavalheri, V., Tahirah, F., Nonoyama, M., Jenkins, S., & Hill, K. (2014). Exercise training for people following lung resection for non-small cell lung cancer—A Cochrane systematic review. Cancer Treatment Reviews, 40(4), 585–594. https://doi.org/10.1016/j.ctrv.2013.11.001

    Dalal, H.M., Zawada, A., Jolly, K., Moxham, T., & Taylor, R.S. (2010). Home based versus centre based cardiac rehabilitation: Cochrane systematic review and meta-analysis. BMJ, 340, b5631. https://doi.org/10.1136/bmj.b5631

    Dhillon, H.M., Bell, M.L., van der Ploeg, H.P., Turner, J.D., Kabourakis, M., Spencer, L., . . . Vardy, J.L. (2017). Impact of physical activity on fatigue and quality of life in people with advanced lung cancer: A randomized controlled trial. Annals of Oncology, 28(8), 1889–1897. https://doi.org/10.1093/annonc/mdx205

    Edbrooke, L., Aranda, S., Granger, C.L., McDonald, C.F., Krishnasamy, M., Mileshkin, L., . . . Denehy, L. (2019). Multidisciplinary home-based rehabilitation in inoperable lung cancer: A randomised controlled trial. Thorax, 74(8), 787–796. https://doi.org/10.1136/thoraxjnl-2018-212996

    Edvardsen, E., Skjonsberg, O.H., Holme, I., Nordsletten, L., Borchsenius, F., & Anderssen, S.A. (2015). High-intensity training following lung cancer surgery: A randomised controlled trial. Thorax, 70(3), 244–250. https://doi.org/10.1136/thoraxjnl-2014-205944

    Egegaard, T., Rohold, J., Lillelund, C., Persson, G., & Quist, M. (2019). Pre-radiotherapy daily exercise training in non-small cell lung cancer: A feasibility study. Reports of Practical Oncology and Radiotherapy, 24(4), 375–382. https://doi.org/10.1016/j.rpor.2019.06.003

    Fiteni, F., Anota, A., Westeel, V., & Bonnetain, F. (2016). Methodology of health-related quality of life analysis in phase III advanced non-small-cell lung cancer clinical trials: A critical review. BMC Cancer, 16, 122. https://doi.org/10.1186/s12885-016-2152-1

    Gerritsen, J.K.W., & Vincent, A.J.P.E. (2016). Exercise improves quality of life in patients with cancer: A systematic review and meta-analysis of randomised controlled trials. British Journal of Sports Medicine, 50(13), 796–803. https://doi.org/10.1136/bjsports-2015-094787

    Granger, C.L., Chao, C., McDonald, C.F., Berney, S., & Denehy, L. (2013). Safety and feasibility of an exercise intervention for patients following lung resection: A pilot randomized controlled trial. Integrative Cancer Therapies, 12(3), 213–224. https://doi.org/10.1177/1534735412450461

    Granger, C.L., McDonald, C.F., Berney, S., Chao, C., & Denehy, L. (2011). Exercise intervention to improve exercise capacity and health related quality of life for patients with non-small cell lung cancer: A systematic review. Lung Cancer, 72(2), 139–153. https://doi.org/10.1016/j.lungcan.2011.01.006

    Handy, J.R., Jr., Asaph, J.W., Skokan, L., Reed, C.E., Koh, S., Brooks, G., . . . Silvestri, G.A. (2002). What happens to patients undergoing lung cancer surgery? Outcomes and quality of life before and after surgery. Chest, 122(1), 21–30. https://doi.org/10.1378/chest.122.1.21

    Henke, C.C., Cabri, J., Fricke, L., Pankow, W., Kandilakis, G., Feyer, P.C., & de Wit, M. (2014). Strength and endurance training in the treatment of lung cancer patients in stages IIIA/IIIB/IV. Supportive Care in Cancer, 22(1), 95–101. https://doi.org/10.1007/s00520-013-1925-1

    Henshall, C.L., Allin, L., & Aveyard, H. (2019). A systematic review and narrative synthesis to explore the effectiveness of exercise-based interventions in improving fatigue, dyspnea, and depression in lung cancer survivors. Cancer Nursing, 42(4), 295–306. https://doi.org/10.1097/ncc.0000000000000605

    Heywood, R., McCarthy, A.L., & Skinner, T.L. (2017). Safety and feasibility of exercise interventions in patients with advanced cancer: A systematic review. Supportive Care in Cancer, 25(10), 3031–3050. https://doi.org/10.1007/s00520-017-3827-0

    Heywood, R., McCarthy, A.L., & Skinner, T.L. (2018). Efficacy of exercise interventions in patients with advanced cancer: A systematic review. Archives of Physical Medicine and Rehabilitation, 99(12), 2595–2620. https://doi.org/10.1016/j.apmr.2018.04.008

    Higgins, J.P.T., & Green, S. (2008). Cochrane handbook for systematic reviews of interventions. Wiley. https://doi.org/10.1002/9780470712184

    Hung, R., Krebs, P., Coups, E.J., Feinstein, M.B., Park, B.J., Burkhalter, J., & Ostroff, J.S. (2011). Fatigue and functional impairment in early-stage non-small cell lung cancer survivors. Journal of Pain and Symptom Management, 41(2), 426–435. https://doi.org/10.1016/j.jpainsymman.2010.05.017

    Hwang, C.L., Yu, C.J., Shih, J.Y., Yang, P.C., & Wu, Y.T. (2012). Effects of exercise training on exercise capacity in patients with non-small cell lung cancer receiving targeted therapy. Supportive Care in Cancer, 20(12), 3169–3177. https://doi.org/10.1007/s00520-012-1452-5

    Jastrzębski, D., Maksymiak, M., Kostorz, S., Bezubka, B., Osmanska, I., Młynczak, T., . . . Kozielski, J. (2015). Pulmonary rehabilitation in advanced lung cancer patients during chemotherapy. In M. Pokorski (Ed.), Respiratory health. Advances in experimental medicine and biology (vol. 861, pp. 57–64). Springer. https://doi.org/10.1007/5584_2015_134

    Ji, W., Kwon, H., Lee, S., Kim, S., Hong, J.S., Park, Y.R., . . . Choi, C.M. (2019). Mobile health management platform-based pulmonary rehabilitation for patients with non-small cell lung cancer: Prospective clinical trial. JMIR mHealth and uHealth, 7(6), e12645. https://doi.org/10.2196/12645

    Lai, Y., Huang, J., Yang, M., Su, J., Liu, J., & Che, G. (2017). Seven-day intensive preoperative rehabilitation for elderly patients with lung cancer: A randomized controlled trial. Journal of Surgical Research, 209, 30–36. https://doi.org/10.1016/j.jss.2016.09.033

    Lee, Y.H., Tsai, Y.F., Lai, Y.H., & Tsai, C.M. (2008). Fatigue experience and coping strategies in Taiwanese lung cancer patients receiving chemotherapy. Journal of Clinical Nursing, 17(7), 876–883. https://doi.org/10.1111/j.1365-2702.2007.02021.x

    Li, J., Guo, N.N., Jin, H.R., Yu, H., Wang, P., & Xu, G.G. (2017). Effects of exercise training on patients with lung cancer who underwent lung resection: A meta-analysis. World Journal of Surgical Oncology, 15(1), 158. https://doi.org/10.1186/s12957-017-1233-1

    Li, X., Li, S., Yan, S., Wang, Y., Wang, X., Sihoe, A.D.L., . . . Wu, N. (2019). Impact of preoperative exercise therapy on surgical outcomes in lung cancer patients with or without COPD: A systematic review and meta-analysis. Cancer Management and Research, 11, 1765–1777. https://doi.org/10.2147/cmar.S186432

    Messaggi-Sartor, M., Marco, E., Martínez-Téllez, E., Rodriguez-Fuster, A., Palomares, C., Chiarella, S., . . . Güell, M.R. (2019). Combined aerobic exercise and high-intensity respiratory muscle training in patients surgically treated for non-small cell lung cancer: A pilot randomized clinical trial. European Journal of Physical and Rehabilitation Medicine, 55(1), 113–122. https://doi.org/10.23736/s1973-9087.18.05156-0

    Mishra, S.I., Scherer, R.W., Snyder, C., Geigle, P.M., Berlanstein, D.R., & Topaloglu, O. (2012). Exercise interventions on health-related quality of life for people with cancer during active treatment. Cochrane Database of Systematic Reviews, 8, CD008465. https://doi.org/10.1002/14651858.CD008465.pub2

    Moher, D., Liberati, A., Tetzlaff, J., & Altman, D.G. (2009). Preferred reporting items for systematic reviews and meta-analyses: The PRISMA statement. BMJ, 339, b2535. https://doi.org/10.1136/bmj.b2535

    Morano, M.T.A.P., Mesquita, R., Da Silva, G.P.F., Araújo, A.S., Pinto, J.M.D.S., Neto, A.G., . . . Pereira, E.D.B. (2014). Comparison of the effects of pulmonary rehabilitation with chest physical therapy on the levels of fibrinogen and albumin in patients with lung cancer awaiting lung resection: A randomized clinical trial. BMC Pulmonary Medicine, 14, 121. https://doi.org/10.1186/1471-2466-14-121

    Mustian, K.M., Alfano, C.M., Heckler, C., Kleckner, A.S., Kleckner, I.R., Leach, C.R., . . . Miller, S.M. (2017). Comparison of pharmaceutical, psychological, and exercise treatments for cancer-related fatigue: A meta-analysis. JAMA Oncology, 3(7), 961–968. https://doi.org/10.1001/jamaoncol.2016.6914

    Ni, H.J., Pudasaini, B., Yuan, X.T., Li, H.F., Shi, L., & Yuan, P. (2017). Exercise training for patients pre- and postsurgically treated for non-small cell lung cancer: A systematic review and meta-analysis. Integrative Cancer Therapies, 16(1), 63–73. https://doi.org/10.1177/1534735416645180

    Ostroff, J.S., Krebs, P., Coups, E.J., Burkhalter, J.E., Feinstein, M.B., Steingart, R.M., . . . Park, B.J. (2011). Health-related quality of life among early-stage, non-small cell, lung cancer survivors. Lung Cancer, 71(1), 103–108. https://doi.org/10.1016/j.lungcan.2010.04.011

    Paramanandam, V.S., & Dunn, V. (2015). Exercise for the management of cancer-related fatigue in lung cancer: A systematic review. European Journal of Cancer Care, 24(1), 4–14. https://doi.org/10.1111/ecc.12198

    Park, S., Kim, J.Y., Lee, J.C., Kim, H.R., Song, S., Kwon, H., . . . Choi, C.M. (2019). Mobile phone app-based pulmonary rehabilitation for chemotherapy-treated patients with advanced lung cancer: Pilot study. JMIR mHealth and uHealth, 7(2), e11094. https://doi.org/10.2196/11094

    Polgreen, L.A., Anthony, C., Carr, L., Simmering, J.E., Evans, N.J., Foster, E.D., . . . Polgreen, P.M. (2018). The effect of automated text messaging and goal setting on pedometer adherence and physical activity in patients with diabetes: A randomized controlled trial. PLOS ONE, 13(5), e0195797. https://doi.org/10.1371/journal.pone.0195797

    Pompili, C. (2015). Quality of life after lung resection for lung cancer. Journal of Thoracic Disease, 7(Suppl. 2), S138–S144. https://doi.org/10.3978/j.issn.2072-1439.2015.04.40

    Pompili, C., Salati, M., Refai, M., Berardi, R., Onofri, A., Mazzanti, P., & Brunelli, A. (2013). Preoperative quality of life predicts survival following pulmonary resection in stage I non-small-cell lung cancer. European Journal of Cardio-Thoracic Surgery, 43(5), 905–910. https://doi.org/10.1093/ejcts/ezs532

    Pouwels, S., Fiddelaers, J., Teijink, J.A., ter Woorst, J.F., Siebenga, J., & Smeenk, F.W.J.M. (2015). Preoperative exercise therapy in lung surgery patients: A systematic review. Respiratory Medicine, 109(12), 1495–1504. https://doi.org/10.1016/j.rmed.2015.08.009

    Schmitz, K.H., Courneya, K.S., Matthews, C., Demark-Wahnefried, W., Galvão, D.A., Pinto, B.M., . . . Schwartz, A.L. (2010). American College of Sports Medicine roundtable on exercise guidelines for cancer survivors. Medicine and Science in Sports and Exercise, 42(7), 1409–1426. https://doi.org/10.1249/MSS.0b013e3181e0c112

    Schumacher, M.M., & McNiel, P. (2018). The impact of Livestrong® at the YMCA for cancer survivors. Oncology Nursing Forum, 45(6), 717–725. https://doi.org/10.1188/18.ONF.717-725

    Sebio García, R., Yáñez-Brage, M.I., Giménez Moolhuyzen, E., Granger, C.L., & Denehy, L. (2016). Functional and postoperative outcomes after preoperative exercise training in patients with lung cancer: A systematic review and meta-analysis. Interactive CardioVascular and Thoracic Surgery, 23(3), 486–497. https://doi.org/10.1093/icvts/ivw152

    Sebio García, R., Yáñez-Brage, M.I., Giménez Moolhuyzen, E., Salorio Riobo, M., Lista Paz, A., & Borro Mate, J.M. (2017). Preoperative exercise training prevents functional decline after lung resection surgery: A randomized, single-blind controlled trial. Clinical Rehabilitation, 31(8), 1057–1067. https://doi.org/10.1177/0269215516684179

    Siegel, R.L., Miller, K.D., & Jemal, A. (2020). Cancer statistics, 2020. CA: A Cancer Journal for Clinicians, 70(1), 7-30. https://doi.org/10.3322/caac.21590

    Sommer, M.S., Staerkind, M.E.B., Christensen, J., Vibe-Petersen, J., Larsen, K.R., Holst Pedersen, J., & Langberg, H. (2018). Effect of postsurgical rehabilitation programmes in patients operated for lung cancer: A systematic review and meta-analysis. Journal of Rehabilitation Medicine, 50(3), 236–245. https://doi.org/10.2340/16501977-2292

    Spruit, M.A., Singh, S.J., Garvey, C., ZuWallack, R., Nici, L., Rochester, C., . . . Wouters, E.F. (2013). An official American Thoracic Society/European Respiratory Society statement: Key concepts and advances in pulmonary rehabilitation. American Journal of Respiratory and Critical Care Medicine, 188(8), e13–e64. https://doi.org/10.1164/rccm.201309-1634ST

    Stigt, J.A., Uil, S.M., van Riesen, S.J.H., Simons, F.J.N.A., Denekamp, M., Shahin, G.M., & Groen, H.J. (2013). A randomized controlled trial of postthoracotomy pulmonary rehabilitation in patients with resectable lung cancer. Journal of Thoracic Oncology, 8(2), 214–221. https://doi.org/10.1097/JTO.0b013e318279d52a

    Sweegers, M.G., Altenburg, T.M., Chinapaw, M.J., Kalter, J., Verdonck-de Leeuw, I.M., Courneya, K.S., . . . Buffart, L.M. (2018). Which exercise prescriptions improve quality of life and physical function in patients with cancer during and following treatment? A systematic review and meta-analysis of randomised controlled trials. British Journal of Sports Medicine, 52(8), 505–513. https://doi.org/10.1136/bjsports-2017-097891

    Yarbro, C.H., Wujcik, D., & Goble, B.H. (2010). Quality of life as an outcome of cancer care. In Cancer nursing: Principles and practice (7th ed., pp. 201–218). Jones and Bartlett.

    Yip, R., Taioli, E., Schwartz, R., Li, K., Becker, B.J., Tam, K., . . . Henschke, C.I. (2018). A review of quality of life measures used in surgical outcomes for stage I lung cancers. Cancer Investigation, 36(5), 296–308. https://doi.org/10.1080/07357907.2018.1474892

    Zeng, Y.C., Ching, S.S.Y., & Loke, A.Y. (2011). Quality of life in cervical cancer survivors: A review of the literature and directions for future research. Oncology Nursing Forum, 38(2), E107–E117. https://doi.org/10.1188/11.ONF.E107-E117