Longitudinal study on the impact of physical activity on the symptoms of lung cancer survivors

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1 Support Care Cancer (2015) 23: DOI /s ORIGINAL ARTICLE Longitudinal study on the impact of physical activity on the symptoms of lung cancer survivors Yi-Yun Lin 1,5 & Kun-Ming Rau 2,3 & Chia-Chin Lin 4 Received: 26 September 2014 /Accepted: 29 March 2015 /Published online: 9 April 2015 # Springer-Verlag Berlin Heidelberg 2015 Abstract Purpose To examine the effect of physical activity on the physical and psychosocial symptoms of lung cancer survivors. Methods A longitudinal design was used in this study. Participants were recruited from the chest and surgical departments of medical centers in Taiwan. The instruments used were the Godin Leisure-Time Exercise Questionnaire and the Taiwanese version of the M.D. Anderson Symptom Inventory. Results In total, 185 survivors were followed up for 6 months (response rate 66 %). Disturbed sleep was the most prevalent symptom in the participants. A generalized estimating equation (GEE) method was employed to analyze the relationships among intensity of physical activity, symptom severity, and symptom interference in the daily life of the participants. Regarding symptom severity, significant differences were observed in fatigue, drowsiness, and disturbed sleep between the participants who engaged in moderate physical activity and those who did not engage in any physical activity. Regarding symptom interference, the participants who engaged * Chia-Chin Lin clin@tmu.edu.tw School of Nursing, Shu Zen College of Medicine and Management, Kaohsiung, Taiwan Division of Hematology-Oncology, Department of Internal Medicine, Kaohsiung Chang Gung Memorial Hospital, Kaohsiung, Taiwan College of Medicine, Chang Gung University, Taoyuan, Taiwan School of Nursing, College of Nursing, Taipei Medical University, Taipei, Taiwan Graduate Institute of Nursing, College of Nursing, Taipei Medical University, Taipei, Taiwan in light physical activity experienced a significantly lower level of symptom interference than did those with a sedentary lifestyle. Conclusion This is the first study to explore the role of physical activity in alleviating symptoms in lung cancer survivors by using the GEE method. The results suggest that physical activity plays an essential role in alleviating the physical and psychological symptoms of lung cancer survivors. Keywords Physical activity. Lung cancer. Longitudinal study. Cancer symptoms Introduction Lung cancer is the most prevalent type of cancer and the leading cause of cancer deaths worldwide [1]. Cancer symptoms are multidimensional from the diagnosis to the treatment stage and influence patient survival rates [2]. Physical exercise is an element of wellness promotion that can enhance the quality of life of cancer survivors [3 6]. Cancer symptoms are significantly associated with patient survival times and are predictors of the survival times of cancer survivors [2, 7 9]. Previous studies have identified several symptoms associated with the poor performance of survivors, and these symptoms can considerably affect the quality of life of patients [5, 10, 11]. Reducing the burden of cancer-related symptoms on the functional status of a survivor should be an essential treatment goal. Physical activity has been associated with the reduction of symptom severity in cancer survivors; however, the results have been inconsistent, and the most effective dose of physical activity remains unclear [10, 12 16]. Cheville et al. [14] administered an incremental walking and strength training program to stage IV cancer survivors and found that symptoms of fatigue and sleep were alleviated.

2 3546 Support Care Cancer (2015) 23: In addition, Sprod et al. [17] examined the relationship between exercise and cancer symptoms in newly diagnosed elderly cancer patients and found that patients who exercised exhibited less fatigue and a lower symptom burden than those with a sedentary lifestyle did. Tang et al. [15] studied the effect of a home-based walking exercise intervention on cancer patients and reported that patients in the exercise group experienced major improvements in their sleep symptoms. These findings suggest that physical activity can alleviate cancer symptoms and should be studied further. The aforementioned studies have focused only on individual symptoms [14, 15, 17]; however, lung cancer patients frequently experience multiple coexisting symptoms attributable to the cancer and the side effects of treatment. The role of physical activity in overall symptom severity and in symptom interference in the daily life of lung cancer survivors has not been extensively investigated. Regular physical activity can play an essential role in alleviating the cancer symptoms of lung cancer survivors. Previous studies have evaluated the relationship between physical activity and the symptoms of other cancer types by employing a cross-sectional design [13, 16, 18, 19]. No prospective study has been conducted on the relationship between physical activity and the cancer symptoms of lung cancer survivors. This study used a longitudinal design to examine the effects of physical activity on the cancer symptoms of lung cancer survivors. Nonpharmacological interventions, such as exercise, may serve as a valuable alternative for managing cancerrelated symptoms in lung cancer survivors. Materials and methods Study population This study used a longitudinal design, and the data were collected through convenience sampling from the chest and surgical departments of medical centers in Taiwan. The inclusion criteria were a diagnosis of lung cancer by a primary physician; treatment with surgery, chemotherapy, radiation therapy, or targeted therapy; and no evidence of a recurrent or progressive disease. All patients were aged 18 years. Instruments Demographic and disease characteristics The collected demographic characteristics of the survivors included age, sex, educational level, and marital status. The collected data on disease and treatment conditions included the time since diagnosis (in months), cancer stage, and treatment modalities. Physical activity We used the Godin Leisure-Time Exercise Questionnaire (GLTEQ) developed by Godin and Shephard [20] to evaluate the physical activity behaviors of the participants. This questionnaire determines the average frequency and duration with which respondents engage in mild (with minimal effort), moderate (not exhausting), and strenuous (rapid heartbeat) exercise over a typical week in their leisure time. The GLTEQ responses exhibited test retest reliabilities of and with VO 2 max [20, 21]. Miller et al. [22]obtaineda concurrent validity coefficient of 0.45 by using a Caltrac accelerometer. The participants were categorized as Bmeeting^ or Bnot meeting^ the public health activity guidelines of the American Cancer Society and the American College of Sports Medicine. These guidelines recommend that cancer survivors engage in moderate to strenuous exercise for a minimum of approximately 150 min per week [23, 24]. Cancer symptoms We used the Taiwanese version of the 19-item M.D. Anderson Symptom Inventory (MDASI-T) translated by Lin et al. [25] to evaluate the severity of the symptoms of the participants and the degree to which these symptoms interfered with their daily life. The MDASI-T comprises 13 and 6 items regarding symptom severity and symptom interference in daily life, respectively. The first section of the MDASI-T consists of 13 single-item measures of symptom intensity: fatigue, disturbed sleep, pain, drowsiness, lack of appetite, nausea, vomiting, shortness of breath, numbness, difficulty remembering, dry mouth, distress (emotional), and sadness. Each item is rated on a scale of 0 (not present) to 10 (as bad as you can imagine). The second section of the MDASI-T assesses the extent to which symptoms interfere with general activities, mood, normal work, relations with other people, walking ability, and enjoyment of life. Each of the six interference items is rated on a scale of 0 (no interference) to 10 (interferes completely). Cleeland et al. [26] evaluated the reliability and validity of the English version of the MDASI; in addition, the reliability and validity of the MDASI-T have been established [12, 25]. Data collection The study was initiated by enrolling lung cancer survivors treated in the chest and surgical departments of medical centers in Taiwan, after ethical approval was obtained. The three assessment time points of the questionnaires were the time of enrollment and two follow-ups at intervals of 3 months. Each patient took approximately 10 min to complete the questionnaire at each assessment time point. The participants unable to complete the questionnaires independently were assisted by a

3 Support Care Cancer (2015) 23: researcher who read each question to them and recorded their answers. Statistical analyses The SPSS 17.0 software package (SPSS, Chicago, IL, USA) was used for data analysis. The effect sizes were interpreted as d=0.20 (small), d=0.50 (medium), and d=0.80 (large) by Cohen [27]; the MDASI-T in our study had a large effect size (0.80). Descriptive statistics were used to represent the demographic and disease-related characteristics, and the mean and standard deviation (SD) were used to represent the physical activity and symptoms of lung cancer survivors. A generalized estimating equation (GEE) analysis was used to account for the dependence among repeated measurements. The GEE analysis was performed to examine the relationship between physical activity and cancer symptoms. The cancer stage and treatment status were included in the analytic models as confounding variables. Results Participant characteristics The demographic and disease-related characteristics of lung cancer survivors were as previously reported [28], and the average age of the participants was (SD, 10.28) years. Approximately half of the survivors of lung cancer (49.7 %) were at stage I. Most patients (73 %) had undergone surgery, and 57.3 % of the patients were in the active treatment period. In total, 185 patients participated in this study, and 143 participants continued to participate in the study until the second assessment time point. Twenty-one participants were lost to follow-up at the second assessment time point either because of death (n=6) or personal reasons (n=15), such as emotional distress and lack of motivation. The final sample comprised 122 patients with a 66 % completion rate at the 6-month follow-up. Changes in symptoms and physical activity over the 6-month study period Table 1 shows the changes in cancer symptoms measured using the MDASI-T at the three time points. The means of symptom severity in the participants were 1.60±1.40, 1.27± 1.30, and 1.34±1.45 at the three time points. At the baseline, the three most severe symptoms experienced by the participants were disturbed sleep (2.83±3.57), dry mouth (2.39± 3.02), and pain (2.15±2.96). At the 3-month follow-up, the three most severe symptoms were disturbed sleep (2.44± 3.45), pain (1.90±2.87), and fatigue (1.76±2.55). At the 6- month follow-up, disturbed sleep (2.75±3.54) was the most severe symptom experienced by the participants, followed by dry mouth (2.72±2.72) and fatigue (2.18±2.96). Figure 1 and Table 2 list the changes in physical activity from the baseline to the two follow-up points. The results indicated that the participants exhibited average physical activity times of ±196.10, ±190.36, and ± min/week at the baseline, 3-, and 6-month assessment time points, respectively. Overall, 24.8, 14.6, and 11.9 % of the participants met the public health physical activity guidelines at the baseline, 3-, and 6-month assessment time points, respectively. Regarding the intensity of physical activity, 50.3, 36.2, and 29.2 % of the participants engaged in mild activity at the baseline, 3-, and 6-month assessment time points, respectively. Effect of physical activity on cancer symptoms Tables 3 and 4 list the effects of physical activity on the symptoms of the participants. The participants who met the physical activity guidelines had significantly lower scores on than MDASI-T than did those with a sedentary lifestyle at the baseline (p=0.017). The GEE method was used to analyze the relationships among intensity of physical activity, symptom severity, and symptom interference in the daily life of the participants. A significant difference was observed in the overall symptom severity between the participants who engaged in moderate physical activity and those who did not engage in any physical activity; the average symptom severity score of the participants who performed moderate physical activity was 0.65 points (95 % CI: 1.27 to 0.03, p=0.039) lower than that of those with a sedentary lifestyle. The symptom interference score of the participants who engaged in light physical activity was 1.15 points (95 % CI: 1.94 to 0.36, p=0.005) lower than that of those with a sedentary lifestyle. Moreover, the results pertaining to physical activity and individual symptoms indicated that the incidence of nausea and shortness of breath was 0.68 (95 % CI: 1.35 to 0.01, p=0.046) and 1.25 (95 % CI: 2.29 to 0.21, p=0.019) points lower, respectively, in the participants who engaged in physical activity than that in those with a sedentary lifestyle. The average scores of fatigue, disturbed sleep, lack of appetite, and drowsiness exhibited by the participants who engaged in moderate physical activity were lower than those exhibited by the participants with a sedentary lifestyle by 1.77, 1.31, 0.96, and 1.43 points, respectively (95 % CI: 2.82 to 0.71, p=0.001; 95 % CI: 2.59 to 0.02, p=0.046; 95 % CI: 1.96 to 0.03, p=0.058; 95 % CI: 2.40 to 0.46, p=0.004). The sadness score of the participants who engaged in strenuous physical activity was significantly lower by 0.91 points (95 % CI: 1.57 to 0.25, p=0.007)comparedwiththatofthe participants who led a sedentary lifestyle.

4 3548 Support Care Cancer (2015) 23: Table 1 Mean scores of cancer symptoms among lung cancer patients over 6 months Variable Baseline, n=185 3 Months, n=143 6 Months, n=122 Mean SD Mean SD Mean SD MDASI-T MDASI-T severity MDASI-T interference MDASI items Pain Fatigue Nausea Disturbed sleep Distress Short of breath Difficulty in remembering Poor appetite Drowsiness Dry mouth Sadness Vomiting Numbness SD standard deviation, MDASI-T the M.D. Anderson Symptom Inventory-Taiwanese version Discussion The major findings of this study are summarized as follows: First, sleep disorders are a persistent primary symptom of lung cancer survivors. Second, engaging in mild physical activity mitigates symptom interference in lung cancer patients. Third, engaging in moderate physical activity alleviates the severity of overall symptoms especially fatigue, shortness of breath, lack of appetite, drowsiness, and disturbed sleep exhibited by lung cancer survivors. Lung cancer survivors can enhance and maintain their health by engaging in physical activity, which at the appropriate intensity is essential for relieving symptoms and improving the quality of life. However, the impact of physical activity on the symptoms of lung cancer survivors remains unclear. In this study, patients diagnosed with lung cancer were observed for 6 months to evaluate the individual trends of the symptoms; the results show that sleep disorders constitute a prevalent primary symptom exhibited by % of lung cancer survivors. This prevalence rate is consistent with that reported in previous studies [29, 30]. Previous studies have also reported sleep disorders in % of survivors diagnosed with other cancer types, such as breast, prostate, and ovarian cancers [13, 19, 31]. Sleep disorders can affect the quality of life of lung cancer survivors; therefore, improving the sleep quality of lung cancer survivors is a priority in improving their quality of life. Moreover, sleep disorders in lung cancer survivors are a multidimensional problem, and additional studies that involve the use of objective evaluation tools are essential for extensively addressing all aspects of this problem. Our results show that, regarding the clinically important differences in the symptoms among lung cancer patients, the participants had a mean score of 1.6 on the MDASI-T, which is lower than the cutoff score of 4.8 established by Wang et al. [32]. Clinically important differences among lung cancer survivors have not been specifically defined for the MDASI-T. The differences in scores may occur because only outpatients whose quality of life was relatively stable [28] were investigated in our study. Therefore, in future studies, we must include inpatients to increase the generalizability of the findings. The results of this study indicate that engaging in mild physical activity mitigates symptom interference in the daily life of lung cancer survivors. Such activity also alleviates nausea and shortness of breath. One possible reason for the decreased nausea is the redirection of the attention of the participants when they engage in physical activity; however, future studies are required to examine the underlying mechanisms. Jones [33] and Riesenberg [34] have indicated alleviation in shortness of breath among their participants, asserting that engaging in physical activity strengthens the cardiopulmonary functions of lung cancer patients. The findings of the present study suggest that physical activity can be considered a cancer care intervention for lung cancer survivors; the participants significantly benefitted from engaging in mild physical activity.

5 Support Care Cancer (2015) 23: Fig. 1 Prevalence of physical activity intensity among lung cancer patients over 6 months Prevalence Baseline 3 months 6 months Regarding the effect of physical activity on the physical symptoms of cancer, the participants who regularly engaged in exercise exhibited low self-perceived symptomatic distress. This result is consistent with those obtained by Yang et al. [12], who studied breast cancer patients. In addition, participants who regularly engaged in physical activity exhibited low levels of fatigue, which is consistent with the result obtained by Karvinen et al. [35], who reported that bladder cancer survivors alleviated their low and medium levels of daily fatigue by engaging in physical activity. Furthermore, similar findings were obtained by Humpel and Iverson [19], who studied breast and prostate cancer patients. Previous studies Table 2 Mean scores of physical activity behavior among lung cancer patients over 6 months Variable Baseline, n=185 3 Months, n=143 6 Months, n=122 Mean (SD) Range Mean (SD) Range Mean (SD) Range Total PA time min/week (196.10) (190.36) (195.31) Frequency Percent (%) Frequency Percent (%) Frequency Percent (%) PA intensity Sedentary Mild activity Moderate activity Strenuous activity PA guidelines Not meeting Meeting SD standard deviation, PA physical activity

6 3550 Support Care Cancer (2015) 23: Table 3 Effects of physical activity on symptoms determined using generalized estimating equation analysis Table 4 Effects of physical activity intensity on individual symptoms determined using generalized estimating equation analysis Variable Estimate Standard error 95 % Confidence interval p value Variable Estimate Standard error 95 % Confidence interval MDASI severity Intercept to Months to Months to PA, min/week to b 6 Months PA to Months PA to MDASI interference Intercept to Months to Months to PA, min/week to b 6 Months PA to Months PA to a Reference group: baseline data b Control for cancer stage and treatment status was applied in analyses on lung cancer patients have demonstrated that exercise programs can increase cardiopulmonary function; physical activity may alleviate fatigue in lung cancer patients by improving muscular strength and endurance, peak oxygen consumption, and cardiopulmonary fitness [33, 34, 36, 37]. Engaging in moderate physical activity reduced the severity of the overall symptoms exhibited by the participants. Of these symptoms, alleviation of disturbed sleep, drowsiness, fatigue, and shortness of breath as well as the improvement of appetite were the most apparent. Disturbed sleep symptoms were alleviated in the participants who engaged in moderate physical activity, which is consistent with the results obtained by Cheville et al. [14], who devised a home-based exercise program specifically for terminal lung cancer and colorectal cancer patients; Tang et al. [15], who developed a home exercise intervention for cancer patients; and Payne et al. [16], who investigated the effect of exercise on breast cancer patients who experienced disturbed sleep. In addition, the participants in our study who engaged in moderate physical activity exhibited less fatigue than did those who did not engage in any physical activity, and this result is consistent with those of numerous breast, ovarian, prostate, and colorectal cancer studies [13, 14, 18, 19]. Furthermore, participants who engaged in moderate or strenuous physical activity exhibited improved appetites, possibly because the physical activity increased their metabolism Fatigue 6 Months to Months to 0.86 Strenuous PA to 2.05 Moderate PA to 0.71* Mild PA to Months strenuous to Months moderate to Months mild to Months strenuous to Months moderate to Months mild to 1.55 Nausea 6 Months to Months to 0.61 Strenuous PA to 0.04 Moderate PA to 0.35 Mild PA to 0.01* 6 Months strenuous to Months moderate to Months mild to Months strenuous to Months moderate to Months mild to 1.68 Disturbed sleep 6 Months to Months to 0.45 Strenuous PA to 3.36 Moderate PA to 0.02* Mild PA to Months strenuous to 1.93* 6 Months moderate to Months mild to Months strenuous to Months moderate to Months mild to 1.73 Short of breath

7 Support Care Cancer (2015) 23: Table 4 (continued) Variable Estimate Standard error 95 % Confidence interval 6 Months to Months to 0.53 Strenuous PA to 4.43 Moderate PA to 0.17* Mild PA to 0.21* 6 Months strenuous to Months moderate to Months mild to Months strenuous to Months moderate to Months mild to 2.36 Poor appetite 6 Months to Months to 0.74 Strenuous PA to 0.68* Moderate PA to 0.03* Mild PA to Months strenuous to Months moderate to Months mild to Months strenuous to Months moderate to Months mild to 1.17 Drowsiness 6 Months to Months to 0.06 Strenuous PA to 0.27 Moderate PA to 0.46* Mild PA to Months strenuous to Months moderate to Months mild to Months strenuous to Months moderate to Months mild to 2.01 a Reference group: baseline data b Reference group: no PA *p<0.05 [38]. However, the detailed mechanisms underlying this improvement remain unclear. Additional studies are required to investigate the effect of physical activity on gastrointestinal symptoms. Similarly, these results indicate that moderate physical activity can alleviate sleep disorder and fatigue symptoms in lung cancer patients; however, additional studies are required to examine the interactive mechanisms between physical activity and sleep disorders. Regarding the relationship between the intensity of physical activity and the psychological symptoms of cancer, the results indicate that feelings of sadness among the participants were alleviated after they participated in strenuous physical activity. This result is inconsistent with those obtained by Stevinson et al. [13] and Knobf et al. [10], because these two studies primarily assessed depression among survivors, whereas we used only one item to assess the psychological symptoms of the participants. In addition, in our study, engaging in physical activity did not alleviate the distress aspect of the psychological conditions of the survivors in our study, which is consistent with the results obtained by Rogers et al. [18] and Payne et al. [16]. However, some discrepancies were observed between these results and those obtained by Stevinson et al. [13], who investigated the influence of physical activity on the psychological conditions of ovarian cancer patients, because only 25 % of the participants examined in our study exhibited distress symptoms. Nevertheless, the effect of physical activity on the psychological condition of lung cancer survivors should not be overlooked. The most beneficial type of physical activity program and its optimal administration frequency for alleviating psychological symptoms among lung cancer survivors should be investigated in the future. This study has several limitations that should be addressed. First, a survival analysis of lung cancer survivors should be performed in future studies. Second, the walking exercises of the participants were assessed using a self-report measure. Future studies should incorporate objective activity measurement methods to increase the accuracy of the walking exercise assessment. Third, although a prospective design is superior to a retrospective design, it does not provide definitive information on causation. Extended research involving randomized control trials is urgently required to evaluate the effect of physical activity on lung cancer survivors. Fourth, the findings of this study cannot be generalized to all lung cancer survivors because only outpatients were examined. This study used a novel longitudinal design to specifically investigate the impact of physical activity on the symptoms of lung cancer survivors and used the GEE method to evaluate the correlation among repeated measurements. The results indicate that the symptoms of fatigue, nausea, shortness of breath, lack of appetite, drowsiness, and disturbed sleep in lung cancer survivors can be alleviated by engaging in regular mild or moderate physical activity for 6 months. The rate at

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