Lung cancer is one of the common cancers and the leading cause of death. Tremendous caregiving burden of informal caregivers of lung cancer causes psychological disorders, such as anxiety and depression. Interventions for informal caregivers of patients with lung cancer to improve their psychological health, which ultimately leads to patients’ positive health outcomes, are crucial. A systematic review and meta-analysis was conducted to: 1) evaluate the effect of non-pharmacological interventions on the outcomes of depression and anxiety for lung cancer patients’ informal caregivers; and 2) compare the effects of interventions with differing characteristics (i.e. intervention types, mode of contact, and group versus individual delivery).
Four databases were searched to identify relevant studies. Inclusion criteria for the articles were peer-reviewed non-pharmacological intervention studies on depression and anxiety in lung cancer patients’ informal caregivers published between January 2010 and April 2022. Systematic review procedures were followed. Data analysis of related studies was conducted using the Review Manager Version 5.4 software. Intervention effect sizes and studies’ heterogeneity were calculated.
Eight studies from our search were eligible for inclusion. Regarding total effect for the caregivers’ levels of anxiety and depression, results revealed evidence for significant moderate effects of intervention on anxiety (SMD -0.44; 95% CI, -0.67, -0.21; p = 0.0002) and depression (SMD -0.46; 95% CI, -0.74, -0.18; p = 0.001). Subgroup analyses for both anxiety and depression of informal caregivers revealed moderate to high significant effects for specific intervention types (cognitive behavioral and mindfulness combined with psycho-education interventions), mode of contact (telephone-based interventions), and group versus individual delivery.
This review provides evidence that cognitive behavioral and mindfulness-based, telephone-based, individual or group-based interventions were effective for informal caregivers of lung cancer patients. Further research is needed to develop the most effective intervention contents and delivery methods across informal caregivers with larger sample size in randomized controlled trials.
Citation: Lei F, Lee E, Shin J, Lee S-Y (2023) Non-pharmacological interventions on anxiety and depression in lung cancer patients’ informal caregivers: A systematic review and meta-analysis. PLoS ONE 18(3): e0282887. https://doi.org/10.1371/journal.pone.0282887
Editor: Tim Luckett, University of Technology Sydney, AUSTRALIA
Received: May 13, 2022; Accepted: February 26, 2023; Published: March 13, 2023
Copyright: © 2023 Lei et al. This is an open access article distributed under the terms of the Creative Commons Attribution License, which permits unrestricted use, distribution, and reproduction in any medium, provided the original author and source are credited.
Data Availability: All relevant data are within the paper.
Funding: The authors received no specific funding for this work.
Competing interests: The authors have declared that no competing interests exist.
Lung cancer is the second most common cancer in both men and women and the leading cause of cancer death among both men and women, making up almost 21% of all cancer deaths . National Cancer Institute  estimates that about 236,740 new lung cancer cases will occur, and about 130,180 patients with lung cancer will die in 2022.
Treatments and care for patients with lung cancer have been advanced gradually, but many unsolved issues remain. Lung cancer patients experience significant physical and psychosocial symptoms, including pain, dyspnea, anorexia, anxiety, and depression due to cancer itself and/or its treatment. Compared to other types of cancer, lung cancer patients had a higher symptom burden, resulting in poor quality of life [2, 3]. Because of the disease trajectory of lung cancer patients, informal caregivers play a key role in caring for them . Informal caregivers can assist patients with lung cancer in managing symptoms, activities of daily living, finance, transportation, seeking information, and providing psychosocial support [4–7]. Taking care of cancer patients is a tremendous burden for informal caregivers  and the resultant burden often leads to in physical as well as psychosocial malfunction [4, 9]. In particular, psychological disorders such as anxiety and depression are prevalent and frequently occur in patients with lung cancer and their informal caregivers [4, 9]. For example, studies [5, 9] have reported that psychological symptoms including anxiety (32.6%-37%) and depression (22%-25.5%) are prevalent among the caregivers of cancer patients. Higher levels of depression and anxiety for caregivers are associated with impaired quality of life of cancer patients, younger patients, or patients’ physical function declined (p<0.05) [10, 11]. Family caregivers of cancer patients are distressed by the poor quality of their own life, disruption of their usual social activities, and the emotional and physical burden of caregiving (p<0.05) . Caregivers of cancer patients desperately need interventions to address their psychosocial problems. One study  provided evidence that 36% of caregivers of cancer patients (N = 99) reported the most difficult part of caregiving was psychosocial; 31% of caregivers responded that they need more information to help them cope emotionally.
Maintaining the psychological health of informal caregivers is all the more important because it is associated with the clinical health of cancer patients [7, 13, 14]. For example, a study of 43 lung cancer patient and caregiver dyads found that patient’s symptoms were positively correlated with the caregiver’s depression and anxiety . Another study  linked higher depression scores of the patient with caregiver depression (b = 0.72, p<0.001). For these reasons, the Clinical Practice Guidelines for Quality Palliative Care published by the National Coalition for Hospice and Palliative Care  suggest that palliative care should focus on not only physical, psychological, functional, spiritual, and practical aspects of seriously ill patients but should also be family-centered, emphasizing the importance of family caregiver assessment, support, and education.
In the past, many systematic reviews and meta-analyses [17–19] have explored the effectiveness of interventions on anxiety and depression for lung cancer patients. A number of systematic reviews and meta-analyses have examined the effects of non-pharmacological interventions on anxiety and depression for informal caregivers of people with cancer. These meta-analyses have found inconsistent results between and within different kinds of interventions. For example, a meta-analysis of meditation intervention  has shown statistically significant improvement in depression and anxiety in informal caregivers, while another of cognitive behavioral therapies  and psychosocial interventions  were less favorable. A Cochrane Systematic review and meta-analysis  found that psychosocial interventions have a significant effect on depression but insignificant effect on anxiety in caregivers of advance cancer patients. Up to date, inconsistent results of meta-analyses on non-pharmacological interventions on anxiety and depression in informal caregivers of cancer patients have been reported. Furthermore, none have examined non-pharmacological interventions on anxiety and depression for the informal caregivers of lung cancer patients. Investigating the topic further will fill the gap in the literature, also findings from this study could help to inform effective intervention strategies to mitigate the prevalent psychological problems (e.g., anxiety and depression) in informal caregivers of lung cancer patients, which will eventually help to decrease their psychological burden. This systematic review and meta-analysis is the first to appraise the effectiveness of non-pharmacological interventions to reduce anxiety and depression in informal caregivers of lung cancer patients. More specifically, a systematic review and meta-analysis was conducted to: 1) evaluate the effect of non-pharmacological interventions on the outcomes of depression and anxiety for lung cancer patients’ informal caregivers; and 2) compare the effects of interventions with differing characteristics (i.e. intervention types, mode of contact, and group versus individual delivery).
We followed the Preferred Reported Items for Systematic Reviews and Meta-Analyses (PRISMA) guidelines.
We used the following electronic databases (EMBASE, CINHAL, PsycInfo, and PubMed) and Clinical Trials.gov. The database search strategy used a combination of medical subject headings (MeSH) terms and text keywords. An example of our PubMed search strategy is in the appendix. The main keywords were informal caregivers, patients with lung cancer, and intervention. Detailed keywords for the literature search were: 1) informal caregivers: caregivers, family members, relatives, or carers; 2) patients with lung cancer: lung cancer, lung neoplasms, lung tumor or lung adenocarcinoma; 3) intervention: intervention, program, education, training, patient education, patient teaching, psychotherapy, support education, or communication; 4) depression: depression, depressive disorder, depressive symptoms, and major depressive disorder; and 5) anxiety: anxiety, anxiety disorders, and generalized anxiety disorder. We also hand-searched reference lists of full-text manuscripts and cross-referenced for potentially relevant papers.
Eligibility criteria and study selection
We included primary intervention articles published between January 2010 and April 2022 in English. Additional inclusion criteria for the articles included: 1) population: targeted population is lung cancer patients’ informal caregivers (defined as family members, friends, or anyone who assisted the patients with lung cancer without compensation); 2) intervention: peer-reviewed studies on non-pharmacological interventions (defined as health interventions that were not primarily based on medication), and 3) outcome: outcomes included depression and/or anxiety. We excluded articles that 1) included various types of cancer (including lung cancer) but did not report data pertinent to the subgroup of informal caregivers; 2) reported only intervention development processes without results; and 3) informal articles such as conference abstracts or commentary articles. The first and the second authors reviewed all abstracts from the search results and selected studies for full text review. Two authors of this study independently screened the titles and abstracts of relevant studies.
Data about the study characteristics (first author and year, country, study design, sample size), intervention type (cognitive-based, mindfulness, yoga, or meditation), mode of contact (in person or telephone-based), group versus individual delivery, and anxiety and depression outcomes were extracted from each study. The first author extracted the data and the second author verified it. No disagreement existed between the two authors regarding the data extraction results.
We used the Physiotherapy Evidence Database (PEDro) scale  to determine the quality of the intervention articles. The PEDro scale is used for randomized clinical trial (RCT) studies to determine internal validity . The scale has 11 items, the higher the score, the greater the methodological quality. We included non-RCT studies due to the limited available intervention articles, but the PEDro scale was still useful in evaluating the quality of articles.
We used the Review Manager Version 5.4 software to conduct the meta-analysis. A random-effects model was applied in the analysis since the observed estimates of intervention effect varied across studies both due to real differences in the intervention effect in each study and sampling variability . Exploratory post-hoc subgroup analyses were conducted to examine the effects of the intervention types, mode of contact, and group versus individual delivery on the anxiety and depression of lung cancer patients’ informal caregivers. Intervention effect sizes for anxiety and depression symptoms were calculated using Hedge’s g statistic and weighted by the sample size of the studies. The Hedge’s g-values were then averaged to calculate the overall effect size and converted to a z value. Hedge’s g was interpreted as 0.2 to indicate a small, 0.5 a medium, and 0.8 a large effect size . The Tau2 and I2 statistics were utilized to evaluate the included studies’ heterogeneity and reveal the variance among the studies. The I2 statistics values were categorized into no (0%–25%), low (25%–50%), moderate (50%–75%), and high (75%–100%) heterogeneity . Since the studies used different measurement scales to measure informal caregivers’ anxiety and depression levels, we used the standardized mean differences along with its 95% confidence intervals to measure the estimated effect size. Because some of studies were quasi-experimental, without control groups, data from control groups in the randomized control trial studies and pre-intervention data from quasi-experimental studies were used as comparisons in evaluating the effect of interventions. We assessed the risk of publication bias within studies according to PRISMA recommendations. Moreover, forest plots were prepared to visualize the effect size and the standardized mean difference with 95% CI. Publication bias was examined visually using funnel plots. An asymmetrical funnel plot represents a potential publication bias. The first author did the data analysis, and the second author reviewed and verified the results.
Characteristics of the studies are summarized in Tables 1 and 2. All of the 8 studies were published between 2015 to 2020 [28–35]. Five of them were conducted in the United States [28, 30–33]. Of the remaining three, one study was conducted in China  and the other two were conducted in Netherlands  and Cyprus . The sample size of included studies ranged from 9  to 120 . Four studies were randomized controlled trials [28–31] and the remaining four studies used quasi-experimental design [32–35].
Of the eight studies, four studies used cognitive-behavioral interventions or body-mind interventions [28, 29, 31, 35], two studies used mediation/mindfulness [30, 34], two studies used yoga [32, 33]. Regarding the ways in which interventions were delivered, five studies were in person interventions [29, 32–35], while three studies were telephone-based [28, 30, 31]. All the studies used couple-based interventions focusing on both patients with lung cancer and their informal caregivers. Three of the eight studies used group-based interventions [29, 34, 35], and five studies used individual-based interventions [28, 30–33]. All interventions were delivered on a regular basis and were given multiple times, for instance, weekly 60 minute telephone counseling over 6 weeks , or four 30 minute sessions over 8 weeks . All interventions had multiple components and were led by health care professionals, such as intervention manuals, telephone counseling sessions , and multidisciplinary educational sessions . Intervention effects on anxiety and depression are reported separately.
Overall, the quality of the studies was satisfactory based on the PEDro scale (Table 3). Most of the studies were randomized controlled trials, except for three studies that did not have control groups [32–34]. Two studies had an attrition rate of more than one-third [34, 35]. Therefore, those studies are of relatively lower quality than others.
Effect on the anxiety of informal caregivers for lung cancer patients
Total effect for the caregivers’ levels of anxiety.
Overall, interventions on informal caregivers of patients with lung cancer significantly decreased the caregivers’ anxiety levels in the intervention groups, as opposed to the comparison groups (p = 0.0002). The pooled summary effect of the included interventions showed that, post intervention, informal caregivers in the intervention group were 0.44 lower at risk for anxiety as contrasted with the comparison group (SMD, -0.44; 95% CI, -0.67, -0.21). However, a very small heterogeneity was noticed across the study results (Tau2 = 0.02, ChI2 = 8.14, df = 7, p = 0.32, I2 = 14%) (Fig 2).
Effect by intervention types
As against comparison groups, the cognitive-behavioral intervention, and the interventions combining mindfulness and psycho-education, significantly decreased the level of anxiety of informal caregivers for lung cancer patients (p = 0.02 and p = 0.04, respectively). Although a decrease in anxiety levels was also noticed on the yoga combined with meditation method, the decrease was not significant (p = 0.36). The pooled summary effect of the cognitive-behavioral intervention, and the mindfulness with psycho-education intervention, showed that caregivers in the intervention groups reduced their risk for anxiety by half as opposed to the comparison group post intervention (SMD, -0.45; 95% CI, -0.83, -0.07; and SMD, -0.50; 95% CI, -0.97, -0.02; respectively). The subgroup analysis showed a significant decrease in heterogeneity across the studies on the absent of heterogeneity of mindfulness with psycho-education intervention studies, and yoga with meditation intervention studies (Tau2 = 0.00, ChI2 = 0.66, df = 1, p = 0.42, I2 = 0% and Tau2 = 0.00, ChI2 = 0.99, df = 1, p = 0.32, I2 = 0%, respectively) (Fig 3).
CBI = cognitive behavioral intervention.
Effect by mode of contact.
Interventions using both in person and telephone-based contact methods significantly decreased levels of anxiety for informal caregivers (p = 0.01). The pooled summary effect of the in person and telephone-based interventions showed that caregivers in these intervention groups were 0.37 and 0.60 lower at risk for anxiety in opposition with the comparison group post intervention (SMD, -0.37; 95% CI, -0.65, -0.09; and SMD, -0.60; 95% CI, -1.05, -0.14; respectively). The subgroup analysis showed an absence of heterogeneity across the in person intervention studies (Tau2 = 0.00, ChI2 = 3.28, df = 4, p = 0.51, I2 = 0%), and an increase of heterogeneity across the telephone-based intervention studies (Tau2 = 0.09, ChI2 = 4.40, df = 2, p = 0.11, I2 = 55%) (Fig 4).
Effect by group versus individual delivery.
Individual-based interventions demonstrated significant decreasing levels of anxiety in informal caregivers (p = 0.003). Although a decreased anxiety level was also noticed in the group-based intervention method, the decrease narrowly failed to reach significance (p = 0.05). The pooled summary effect of the individual-based interventions showed that caregivers in the intervention group were about 0.51 lower at risk for anxiety than the comparison group post intervention (SMD, -0.51; 95% CI, -0.85, -0.17). The subgroup analysis showed a low heterogeneity across the group-based intervention studies (Tau2 = 0.01, ChI2 = 2.23, df = 2, p = 0.33, I2 = 10%) and individual based intervention studies (Tau2 = 0.04, ChI2 = 5.73, df = 4, p = 0.22, I2 = 30%) (Fig 5).
Effect on the depression of informal caregivers for lung cancer patients
Interventions for informal caregivers of lung cancer patients significantly decreased the caregivers’ depression levels as opposed to the comparison groups (p = 0.001). The pooled summary effect of the included interventions showed that caregivers in the intervention group were 0.46 lower at risk for depression than the comparison group post intervention (SMD, -0.46; 95% CI, -0.74, -0.18). A low heterogeneity was noticed across the study results (Tau2 = 0.05, ChI2 = 11.08, df = 7, p = 0.14, I2 = 37%) (Fig 6).
Effect by intervention types.
The cognitive-behavioral intervention, and the mindfulness with psycho-education interventions, significantly decreased depression in informal caregivers of lung cancer patients (p = 0.02). Although a decreased depression level was also noticed with the yoga combined with meditation method, the decrease was not significant (p = 0.91). The pooled summary effect of the cognitive-behavioral intervention, and the mindfulness with psycho-education interventions, showed that caregivers in the intervention groups were about 0.54 and 0.55 lower at risk for depression as opposed to the comparison group post intervention (SMD, -0.54; 95% CI, -0.98, -0.10; and SMD, -0.55; 95% CI, -1.03, -0.08; respectively). The subgroup analysis showed a significant decrease in heterogeneity across the studies and the absence of heterogeneity of mindfulness combined with psycho-education, and yoga combined with meditation intervention studies (Tau2 = 0.00, ChI2 = 0.16, df = 1, p = 0.69, I2 = 0% and Tau2 = 0.00, ChI2 = 0.70, df = 1, p = 0.40, I2 = 0%, respectively) (Fig 7).
Effect by mode of contact.
Both in-person and telephone-based interventions significantly decreased the level of depression in informal caregivers of patients with lung cancer (p = 0.01 and p = 0.04, respectively). The pooled summary effect of the in person and telephone-based interventions showed that caregivers in the intervention groups were 0.44 and 0.57 lower at risk for depression as opposed to the comparison group post intervention (SMD, -0.44; 95% CI, -0.78, -0.09; and SMD, -0.57; 95% CI, -1.11, -0.03, respectively). The subgroup analysis showed decreased heterogeneity across in-person intervention studies (Tau2 = 0.03, ChI2 = 4.81, df = 4, p = 0.31, I2 = 17%) but increased heterogeneity across the telephone-based intervention studies (Tau2 = 0.15, ChI2 = 6.20, df = 2, p = 0.05, I2 = 68%) (Fig 8).
Effect by group versus individual delivery.
Results showed that when contrasted with the comparison groups, the group-based interventions significantly decreased depression in informal caregivers for lung cancer patients (p = 0.0001). Although a decreased depression level was also noticed in the individual-based intervention method, the decrease narrowly failed to reach significance (p = 0.05). The pooled summary effect of the group-based interventions showed that caregivers in the intervention group were about 0.62 lower at risk for depression than the comparison group post intervention (SMD, -0.62; 95% CI, -0.93, -0.30). The subgroup analysis showed decreased heterogeneity across the group-based intervention studies (Tau2 = 0.00, ChI2 = 1.57, df = 2, p = 0.46, I2 = 0%) but increased across the individual-based intervention studies (Tau2 = 0.11, ChI2 = 8.21, df = 4, p = 0.08, I2 = 51%) (Fig 9).
Respective funnel plots were generated for each main outcome of interest to evaluate publication bias. The distribution of data points provided limited evidence for small study publication bias (Fig 10A and 10B).
a. Effect on the Anxiety of Informal Caregivers for Lung Cancer Patients. SE: standard error, SMD: Standardized mean difference. b. Effect on Depression in Informal Caregivers for Lung Cancer Patients. SE: standard error, SMD: Standardized mean difference.
This systematic review and meta-analysis found that non-pharmacological interventions have generally been successful in significantly decreasing anxiety and depression on caregivers of people with lung cancer. Subgroup analyses revealed that relative effectiveness on both anxiety and depression may depend on specific intervention types, mode of contact, and group versus individual delivery.
First, regarding intervention types, there have been few systematic reviews and meta-analyses on non-pharmacological interventions on anxiety and depression in informal caregivers of patient populations other than lung cancer. The findings of this review are consistent with a previous systematic review and meta-analysis, which has found significant effects on meditation intervention on informal caregivers of chronic illness patients . After 27 randomized controlled trials evaluating the association of meditation interventions at an average of eight weeks following intervention initiation in informal caregivers of chronic illness patients, a meta-analysis reported that meditation interventions were associated with significant improvement in anxiety (effect size 0.53, 95% CI 0.06 to 0.99) and in depression (effect size 0.49, 95% CI 0.24 to 0.75) . Interestingly, previous meta-analyses papers reported little significant effects of cognitive behavioral therapies on both anxiety and depression in informal caregivers of patients with cancer of various kinds beyond just lung cancer, including: informal caregivers of cancer patients and cancer survivors , psychosocial interventions with informal caregivers of cancer patients , and insignificant effects of psychosocial interventions on anxiety in caregivers of advanced cancer patients . Cognitive behavioral therapy refers to intervention strategies such as cognitive restructuring, coping skills training or stress and anxiety management . A meta-analysis  analyzed 36 studies using cognitive behavioral therapy and found a small statistically significant effect of cognitive behavioral therapy on the common psychological complaints of cancer patients’ caregivers, such as anxiety and depression (Hedge’s g = 0.08, p = 0.014). This is inconsistent with our findings in this review that cognitive behavioral interventions have small to large effects on reducing anxiety and depression in informal caregivers of lung cancer patients. Furthermore, the present findings are inconsistent with a meta-analysis that revealed significant small to moderate effects on both anxiety and depression in yoga interventions for cancer patients . More specifically, a systematic review and meta-analysis of 26 yoga interventions for cancer patients, including a majority of breast cancer patients, revealed evidence of significant small to medium effects of yoga on depression (g = -0.419, 95% CI -0.558 to -0.281) and anxiety (g = -0.347, 95% CI -0.473 to -0.221) . Different study characteristics such as cancer patients vs. caregivers, or cancer vs. lung cancer may result in different study results (e.g., intervention effectiveness).
Second, for mode of contact and group versus individual delivery, findings of this review, that in person and telephone-based interventions, and individual- and group-based interventions decreased anxiety and depression in informal caregivers of patients with lung cancer, are similar to findings from previous such meta-analyses. For example, a meta-analysis of 29 randomized trial studies with family caregivers of cancer patients reported that both face to face intervention (Hedges’ g 1.06, 95% CI 0.42 to 1.71, p<0.05) and group-based intervention (Hedges’ g 1.01, 95% CI 0.39 to 1.63, p<0.001) significantly improved coping strategies . Although this review included individual- and telephone-based interventions for informal caregivers, internet-based interventions on informal caregivers’ mental health were previously investigated as effective delivery methods. For example, a meta-analysis study  examined the impact of internet-based interventions on informal caregiver mental health outcomes. It revealed the beneficial effects of internet-based intervention programs by decreasing a mean of 0.40 (95% CI -0.58 to -0.22) for anxiety among informal caregivers of adults with cancer, dementia, or stroke . Furthermore, information platforms (e.g., smartphone applications) are considered useful in providing information in a timely manner . Thus, future research needs to explore various and innovative intervention delivery methods for the psychological health of informal caregivers of lung cancer patients.
Strengths and limitations
Despite the fact that the well-being of lung cancer patients’ informal caregivers is crucial, a few evidence-based interventions addressing anxiety and depression in such caregivers are available at present. The strengths of this systematic review and meta-analysis study are: a) providing the first evidence summary on the effectiveness of non-pharmacological interventions on anxiety and depression for lung cancer patients’ informal caregivers, b) including newly published intervention studies on these issues, and c) performing new subgroup analyses compared to previous reviews.
This systematic review and meta-analysis had limitations that we should be aware of. Firstly, only eight studies were included in this review and two or four studies were analyzed in subgroup analysis. We found significant decreases in anxiety and depression, though only two to four studies in each subgroup were included, which may limit the strength of our results. While some indicate that at least two studies are needed to conduct a meta-analysis , others suggest that meta-analyses with very small numbers of studies may underestimate heterogeneity . Because our subgroups in this meta-analysis are relatively small, heterogeneity results should be interpreted with caution. Lastly, we included studies published only in English, which may reduce the generalizability of our results to non-English speaking countries.
Psychological problems such as anxiety and depression in informal caregivers of patients with lung cancer are closely interrelated with the health outcomes of the patients [4–7]. We should attempt to improve positive health outcomes in both populations. The findings of this meta-analysis show potential beneficial effects of cognitive behavioral and mindfulness-based, telephone-based, individual- or group-based interventions on anxiety and depression in informal caregivers of patients with lung cancer. Further research is needed to develop and test in order to find the most effective intervention contents and delivery methods by comparing different psychological interventions head-to-head in trials.
- 1. National Cancer Institute. Cancer Stat Facts: Lung and bronchus cancer 2022 Available from: https://seer.cancer.gov/statfacts/html/lungb.html.
- 2. Sung MR, Patel MV, Djalalov S, et al. Evolution of symptom burden of advanced lung cancer over a decade. Clin Lung Cancer. 2017;18(3):274–80. pmid:28185791
- 3. Lyer S, Roughley A, Rider A, Taylor-Stokesau G. The symptom burden of non-small cell lung cancer in the USA: a real-world cross-sectional study. Support Care Cancer. 2014;22:181–7. pmid:24026981
- 4. Cochrane A, Reid O, Woods S, et al. Variables associated with distress amongst informal caregivers of people with lung cancer: A systematic review of the literature. Psycho-Oncology. 2021;30:1246–61. https://doi.org/10.1002/pon.5694
- 5. Skalla KA, Smith EML, Li Z, Gates C. Multidimensional needs of caregivers for patients with cancer. Clinical Journal of Oncology Nursing. 2013;17(5):500–6. pmid:23956004
- 6. Deshields T, Rihanek A, Potter P, Zhang Q, Kuhrik M, Kuhrik N, et al. Psychosocial aspects of caregiving: Perceptions of cancer patients and family caregivers. Supportive Care in Cancer. 2012;20(2):349–56. pmid:21298291
- 7. Sato T, Fujisawa D, Arai D, et al. Trends of concerns from diagnosis in patients with advanced lung cancer and their family caregivers: A 2-year longitudinal study. Palliative Medicine. 2021;35(5):943–51. pmid:33761790
- 8. Sun V, Raz DJ, Kim JY. Caring for the informal cancer caregiver. Current Opinion in Supportive and Palliative Care. 2019;13(3):238–42. pmid:31157656
- 9. He Y, Sun L-Y, Peng K-W, Luo M-J, Deng L, Tang T, et al. Sleep quality, anxiety and depression in advanced lung cancer: patients and caregivers. BMJ Supportive & Palliative Care. 2020;0:1–7. pmid:32253349
- 10. Lyons KS, Bennett JA, Nail LM, Fromme EK, Dieckmann N, Sayer AG. The role of patient pain and physical function on depressive symptoms in couples with lung cancer: a longitudinal dyadic analysis. Journal of Family Psychology. 2014;28(5):692–700. pmid:25090253
- 11. Borges EL, Franceschini J, Costa LHD, Fernandes ALG, Jamnik S, Santoro IL. Family caregiver burden: the burden of caring for lung cancer patients according to the cancer stage and patient quality of life. The Brazilian Journal of Pulmonology and international databases. 2017;43(1):18–23. https://doi.org/10.1590/S1806-37562016000000177
- 12. Fujinami R, Sun V, Zachariah F, Uman G, Grant M, Ferrell B. Family caregivers’ distress levels related to quality of life, burden, and preparedness. Psychooncology. 2015;24(1):54–62. pmid:24789500
- 13. Litzelman K, Kent EE, Molica M, Rowland JH. How does caregiver well-being relate to perceived quality of care in patients with cancer? Exploring associations and pathways. Journal of Clinical oncology. 2016;34(29):3554–61. pmid:27573657
- 14. Litzelman K, Kent EE, Rowland JH. Interrelationships between health behaviors and coping strategies among informal caregivers of cancer survivors. Health Education & Behavior. 2018;45(1):90–100. https://doi.org/10.1177/1090198117705164
- 15. Pinquart M, Duberstein PR. Optimism, pessimism, and depressive symptoms in spouses of lung cancer patients. Psychology and Health. 2005;20(5):565–78. https://doi.org/10.1080/08870440412331337101
- 16. National Consensus Project for Quality Palliative Care. Clinical practice guidelines for quality palliative care. 4th edition ed. Richmon VA: National Coalition for Hospice and Palliative Care; 2018.
- 17. Li J, Li C, Puts M, Wu Y, Lyu M, Yuan B, et al. Effectiveness of mindfulness-based interventions on anxiety, depressin, and fatigue in people with lung cancer: A systematic review and meta-analysis. International Journal of Nursing Studies. 2023;In press. https://doi.org/10.1016/j.ijnurstu.2023.104447
- 18. Zhu R, Chen H, Gao Y, Pan Z, Wang J. Effects of psychological nursing care on anxiety and depression in perioperative patients with lung cancer: A systematic review and meta-analysis. Medicine. 2022;101(29):e29914. pmid:35866819
- 19. Gravier F, Smondack P, Guillaume P, Medrinal C, Combret Y, Muir J, et al. Effects of exercise training in people with non-small cell lung cancer before lung resection: a systematic review and meta-analysis. Thorax. 2022;77(5):486–96. pmid:34429375
- 20. Dharmawardene M, Givens J, Wachholtz A, Makowski S, Tjia J. A systematic review and meta-analysis of meditative interventions for informal caregivers and health professionals. BMJ Support Palliative Care. 2016;6(2):160–9. pmid:25812579
- 21. O’Toole MS ZR, Renna ME, Mennin DS, Applebaum A. Cognitive behavioral therapies for informal caregivers of patients with cancer and cancer survivors: a systematic review and meta-analysis. Psycho-Oncology. 2017;26:428–37. pmid:27147198
- 22. Treanor CJ, Santin O, Prue G, Coleman H, Cardwell CR, O’halloran P, et al. Psychosocial interventions for informal caregivers of people living with cancer. Cochrane Database of Systematic Reviews. 2019;6:CD009912. pmid:31204791
- 23. Lee JZ, Chen H, Lee JX, Klainin-Yobas P. Effects of psychosocial interventions on psychological outcomes among caregivers of advanced cancer patients: A systematic review and meta-analysis. BMJ Support Care Cancer. 2021;29(1):7237–48. pmid:34240256
- 24. Physiotherapy Evidence Database. PEDro scale: The University of Sydney; 1999 Available from: https://pedro.org.au/english/resources/pedro-scale.
- 25. Riley RD, Higgins JP, Deeks JJ. Interpretation of random effects meta-analyses. BMJ. 2011;342:d549. pmid:21310794
- 26. Hedges L, Olkin I. Statistical methods for medta-analysis. New York: Academic Press; 1995.
- 27. Higgins JP, Thompson SG, Deeks JJ, Altman DG. Measuring inconsistency in meta-analyses. BMJ. 2003;327(7414):557–60. pmid:12958120
- 28. Badr H, Smith CB, Goldstein NE, Gomez JE, Redd WH. Dyadic psychosocial intervention for advanced lung cancer patients and their family caregivers: results of a randomized pilot trial. Cancer. 2015;121(1):150–8. pmid:25209975
- 29. Li YW, Fang MH, Quan MM, Yan ZC, Liu DY, Pan ZY. Influence of wellness education on first-line icotinib hydrochloride patients with stage IV non-small cell lung cancer and their family caregivers. Current Problems in Cancer. 2018;42:358–66. pmid:29731164
- 30. Mosher CE, Secinti E, Hirsh AT, Hanna N, Einhorn LH, Jalal SI, et al. Acceptance and Commitment Therapy for Symptom Interference in Advanced Lung Cancer and Caregiver Distress: A Pilot Randomized Trial. Journal of Pain and Symptom Management. 2019;58(4):632–44. pmid:31255586
- 31. Mosher CE, Winger JG, Hanna N, et al. Randomized Pilot Trial of a Telephone Symptom Management Intervention for Symptomatic Lung Cancer Patients and Their Family Caregivers. Journal of Pain and Symptom Management. 2016;52(4):469–82. pmid:27401514
- 32. Milbury K, Chaoul A, Engle R, Liao Z, Yang C, Carmack C, et al. Couple-based Tibetan yoga program for lung cancer patients and their caregivers. Psycho-oncology. 2015;24(1):117–20. pmid:24890852
- 33. Milbury K, Mallaiah S, Lopez G, Liao Z, Yang C, Carmack C, et al. Vivekananda Yoga Program for Patients With Advanced Lung Cancer and Their Family Caregivers. Integrative Cancer Therapies. 2015;14(5):446–51. pmid:25917816
- 34. van den Hurk DG, Schellekens MP, Molema J, Speckens AE, van der Drift MA. Mindfulness-Based Stress Reduction for lung cancer patients and their partners: Results of a mixed methods pilot study. Palliative Medicine. 2015;28(7):652–60. pmid:25701663
- 35. Choratas A, Papastavrou E, Charalambous A, Kouta C. Developing and assessing the effectiveness of a nurse-led home-based educational programme for managing breathlessness in lung cancer patients. A feasibility study. Frontiers in Oncology. 2020;10(1366):1–14. pmid:32983967
- 36. Nenova M, Morris L, Paul L, Li Y, Applebaum A, DuHamel K. Psychosocial interventions with cognitive-behavioral components for the treatment of cancer-related traumatic stress symtoms: a review of randomized controlled trials. Journal of Cognitive Psychotherapy. 2013;27:258–84. https://doi.org/10.1891/0889-83188.8.131.528
- 37. Gonzalez M, Pascoe MC, Yang G, Manincor M, Grant S, Lacey J, et al. Yoga for depression and anxiety symptoms in people with cancer. Psycho-Oncology. 2021;30:1196–208. https://doi.org/10.1002/pon.5671
- 38. Northouse LL, Katapodi MC, Song L, Zhang L, Mood DW. Interventions with family caretivers of cancer patients: Meta-analysis of randomized trials. CA: Cancer. 2010;60(5):317–39. https://doi.org/10.3322/caac.20081
- 39. Sherifali D, Ali MU, Ploeg J, Markle-Reid M, Valaitis R, Bartholomew A, et al. Impact of internet-based interventions on caregiver mental health: Systematic review and meta-analysis. Journal of Medical Internet Research. 2018;20(7):e10668. pmid:29970358
- 40. Valentine JC, Pigott TD, Rothstein HR. How many studies do you need? A primer on statistical power for meta-analysis. Journal of Educational and Behavioral Statistics. 2010;35:215–47. https://doi.org/10.3102/1076998609346961
- 41. Kontopantelis E, Springate DA, Reeves D. A re-analysis of the Cochrane library data: the dangers of unobserved heterogeneity in meta-analyses. PLoS ONE. 2013;8:e69930. pmid:23922860