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Efficacy and mechanisms of four-week MBSR on psychological distress in lung cancer patients: a single-center, single-blind, longitudinal, randomized controlled trial

Open AccessPublished:October 12, 2022DOI:https://doi.org/10.1016/j.apjon.2022.100151

      Abstract

      Objective

      This study aimed to evaluate the efficacy of a four-week MBSR program on psychological distress in patients with lung cancer and elucidate its mechanisms.

      Methods

      This single-center, single-blinded, longitudinal, randomized controlled trial was conducted on 175 lung cancer patients randomly allocated to a four-week MBSR or a waiting-list group. The efficacy and mechanisms of the four-week MBSR program were evaluated by outcome measures at pre-intervention (T0), the immediate post-intervention (T1), 1 month (T2), and 3 months (T3). We analyzed the collected data using the per-protocol set (PP) principle, independent sample t-test, repeated measure analysis of variance (ANOVA), and structural equation modeling.

      Results

      The four-week MBSR program significantly alleviated psychological distress (F=15.05, P<0.001), decreased perceived stigma (F=8.260, P=0.005), and improved social support (F=16.465, P<0.001), and enhanced mindfulness (F=17.207, P<0.001) compared with usual care at T1, T2, and T3. All variables significantly changed over time except for copying style (P=0.250). The changes in social support, mindfulness, and perceived stigma mediated the efficacy of the four-week MBSR program on psychological distress (β=-0.292, P=0.005; β=-0.358, P=0.005).

      Conclusions

      This study shows the benefits of the MBSR program for psychological distress, social support, mindfulness, and perceived stigma in lung cancer patients. Also, it elucidates the mechanisms by which the MBSR program alleviate psychological distress by improving social support, enhancing mindfulness, and decreasing perceived stigma. The findings provide insights into applying the MBSR program to reduce psychological distress among lung cancer patients.

      Keywords

      • 1.
        The MBSR program alleviates the psychological distress of lung cancer patients.
      • 2.
        The MBSR program showed promise in improving lung cancer patients’ social support, enhancing mindfulness, and reducing perceived stigma.
      • 3.
        The MBSR program supports interventional efficacy on lung cancer patients’ psychological distress by affecting social support, mindfulness, and perceived stigma

      Introduction

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      Therefore, based on currently available evidence, we hypothesized that (a) a four-week MBSR program could alleviate psychological distress in lung cancer patients, and (b) by affecting social support, coping style, self-esteem, mindfulness, perceived stress, perceived stigma, and illness perception.

      Methods

      Study design

      The present study was a single-center, single-blinded, longitudinal, randomized, controlled, parallel trial, including a four-week MBSR program group and a waiting-list group. We recruited eligible participants from a hospital in southwest China between 1 January and 30 September 2021.

      Data collection

      We designed a face-to-face questionnaire survey to collect data, administered by a trained research nurse at three time points (depicted in Figure 1): baseline (T0), the immediate post-intervention (T1), 1-month post-intervention (T2), and 3 months post-intervention (T3).
      Figure 1
      Figure 1The Consolidated Standards for Reporting Trials (CONSORT) flow diagram of participant recruitment

      Sample size

      We estimated the sample size using psychological distress as the main effect indicator for this study. According to our previous meta-analysis[
      • Tian X.
      • Yi L.J.
      • Liang C.S.S.
      • Gu L.
      • Peng C.
      • Chen G.H.
      • et al.
      The impact of mindfulness-based stress reduction (MBSR) on psychological outcomes and quality of life in lung cancer patients: a meta-analysis.
      ], the MBSR program was associated with an effect size of 0.418 which was estimated based on the pooled result of psychological distress. Therefore, we estimated a theoretical sample size of 75 cases to ensure a statistical power of 80.0%. After considering a 20% dropout rate, 90 patients were calculated and then randomized to the four-week MBSR or the waiting-list group. We used the G*Power software (version 3.1) to estimate the sample size.

      Participant criteria

      We selected potential participants according to the following inclusion criteria: (a) cytological or histological diagnosis of lung cancer; (b) age ≥18 years; (c) patients with proven clinically significant psychological distress or at high risk of suffering from psychological distress; (d) known their diagnosis and were willing to participate in this study; and (e) able to read, write, and speak Chinese.
      Exclusion criteria included: (a) a concurrent diagnosis of other cancers or psychiatric disorders; (b) a history of suicide attempts; (c) participation in any other psychosocial interventions within 3 months before enrollment, (d) prior experience with mindfulness-based interventions (MBIs), and (e) physical or cognitive (<26 on the Mini-Mental State Examination [MMSE]) impairments hampering participation in the four-week MBSR program or completion of questionnaires. Dropout criteria included: (a) unable to complete the intervention; and (b) loss to follow-up.

      Recruitment

      The trained research nurses enrolled participants from the respiratory and medical oncology inpatient departments of a general hospital in southwest China at patient visits. Trained research nurses assessed their eligibility, introduced the purpose of the study, and explained research content to potential participants and ensured that participants voluntarily participated in this study.

      Randomization, allocation concealment, and blinding

      After signing a written informed consent, eligible participants formally participated in this study. We first conducted a baseline survey of all participants in this study. Then, we randomly assigned participants to a four-week MBSR or waiting-list group using random numbers generated by SPSS software version 22.0. An independent research nurse used sealed and opaque envelopes for assignments. We invited independent psychologists qualified in the MBSR program to conducted a four-week MBSR program for participants in the experimental group. Since all participants have been informed of the detailed processes of this study, it is not possible to blind participants. However, outcome assessments were blinded because independent staff analyzed all outcomes.

      Interventions

      Experimental group

      Participants in the experimental group received both usual care and a four-week MBSR program. In this study, we selected a four-week MBSR program as an intervention according to our meta-analysis[
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      ] because lung cancer patients usually have a relatively short median survival time and fast deterioration in physical health[
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      ]. During this four-week MBSR program, all participants in the experimental group practiced MBSR under the guidance and supervision of a psychologists qualified as mindfulness trainer. The details of this four-week program were as follows: 10-minute explanation and meditation in the first week, 10-minute walking meditation in the second week, 10-minute breathing meditation in the third week, and 20-minute experience sharing in the fourth week. Details of each session in this four-week MBSR programme are summarized in Table S1. Participants were supervised to daily practice at home by psychologists twice weekly using telephone or WeChat (a popular social media in China).

      Waiting-list group

      Participants in the waiting list group first received usual care, including dietary instruction, health education, rehabilitation excise, emotional counseling, and medication instruction. Following the conclusion of this study, these participants were invited to voluntarily receive a four-week MBSR program and were provided with videos and materials for the intervention.

      Demographics

      At baseline, we used a self-designed data collection sheet to collect the demographic and clinical characteristics, including demographic information (gender, age, education level, occupation, marital status, residence, medical insurance, yearly income, family history of lung cancer, and smoking history) and clinical characteristics (TNM tumor stage, metastases, comorbidities, and pain degree).

      Outcome measures

      Psychological distress

      We used the distress thermometer (DT) to measure psychological distress on an 11-point thermometer scale from 0 to 10 in this study, and 0 and 10 indicate no distress and extreme distress, respectively[
      • Riba M.B.
      • Donovan K.A.
      • Andersen B.
      • Braun I.
      • Breitbart W.S.
      • Brewer B.W.
      • et al.
      Distress Management, Version 3.2019, NCCN Clinical Practice Guidelines in Oncology.
      ]. The reliability and validity of DT across different settings have been extensively tested[
      • Hong J.
      • Wei Z.
      • Wang W.
      Preoperative psychological distress, coping and quality of life in Chinese patients with newly diagnosed gastric cancer.
      ]. Previous empirical studies indicated a score of ≥4 effectively confirms clinically significant psychological distress[
      • Hong J.
      • Wei Z.
      • Wang W.
      Preoperative psychological distress, coping and quality of life in Chinese patients with newly diagnosed gastric cancer.
      ,
      • Donovan K.A.
      • Grassi L.
      • McGinty H.L.
      • Jacobsen P.B.
      Validation of the distress thermometer worldwide: state of the science.
      ]. A score of 4 was also demonstrated as the cut-off value for defining clinically significant psychological distress in Chinese cancer populations[
      • Hong J.
      • Wei Z.
      • Wang W.
      Preoperative psychological distress, coping and quality of life in Chinese patients with newly diagnosed gastric cancer.
      ]. Meanwhile, we used the predictive algorithm, which was previously developed by our team[
      • Tian X.
      • Jin Y.
      • Tang L.
      • Pi Y.-P.
      • Chen W.-Q.
      • Jimenez-Herrera M.F.
      Predicting the Risk of Psychological Distress among Lung Cancer Patients: Development and Validation of a Predictive Algorithm Based on Sociodemographic and Clinical Factors.
      ], to identify those patients at high risk of psychological distress. In this predictive algorithm, a score of ≥66 indicates that patients have a high risk of suffering from psychological distress. We selected lung cancer patients who scored ≥4 in DT or ≥66 in the predictive algorithm to participate in this study.

      Social support

      The 12-item Multidimensional Scale of Perceived Social Support (MSPSS) was used to measure social support from three aspects, including family, friends, and significant others, on a 7-point Likert scale (1 indicates very strongly disagree but 7 represents very strongly agree)[
      • Zimet G.D.
      • Powell S.S.
      • Farley G.K.
      • Werkman S.
      • Berkoff K.A.
      Psychometric characteristics of the Multidimensional Scale of Perceived Social Support.
      ]. A previous study tested the psychological properties of MSPSS and reported coefficient alpha values of subscales ranging from 0.81 to 0.98[
      • Zimet G.D.
      • Powell S.S.
      • Farley G.K.
      • Werkman S.
      • Berkoff K.A.
      Psychometric characteristics of the Multidimensional Scale of Perceived Social Support.
      ]. The Chinese version had a reliability of 0.90[
      • Yang J.
      • Li S.
      • Zheng Y.
      Predictors of depression in Chinese community-dwelling people with type 2 diabetes.
      ]. We used the Chinese version in this study, which had an overall Cronbach’s alpha coefficient of 0.818, 0.785, 0.835, and 0.701 at T0, T1, T2, and T3, respectively, to measure social support.

      Coping style

      The 20-items Medical Coping Modes Questionnaire (MCMQ) was used to evaluate the coping styles, including confrontation, avoidance, and giving up coping, on a linear 4-point Likert scale from 1 to 3[
      • Feifel H.
      • Strack S.
      Coping with conflict situations: middle-aged and elderly men.
      ]. Shen, et al.[
      • Shen X.H.
      • Jiang J.Q.
      Report on application of Chinese version of MCMQ in 701 patients.
      ] validated the Chinese version of the MCMQ, reporting a Cronbach’s alpha coefficient of more than 0.60 for three subscales. We used the Chinese version in this study, which had an overall Cronbach’s alpha of 0.561, 0.542, 0.753, and 0.537 at T0, T1, T2, and T3, respectively, to measure coping style.

      Self-esteem

      The 10-item Rosenberg Self-Esteem Scale (RSES) was developed to measure global self-esteem, having a Cronbach’s alpha of 0.88[
      • Rosenberg M.
      • Schooler C.
      • Schoenbach C.
      Self-Esteem and Adolescent Problems: Modeling Reciprocal Effects.
      ]. A higher score indicated a higher level of self‐esteem[
      • Rosenberg M.
      • Schooler C.
      • Schoenbach C.
      Self-Esteem and Adolescent Problems: Modeling Reciprocal Effects.
      ]. The Chinese version of the RSES has been validated by [
      • Wu Y.
      • Zuo B.
      • Wen F.
      • Yan L.
      Rosenberg Self-Esteem Scale: Method Effects, Factorial Structure and Scale Invariance Across Migrant Child and Urban Child Populations in China.
      ] and has been extensively used in China[
      • Cai Z.
      • Gui Y.
      • Wang D.
      • Yang H.
      • Mao P.
      • Wang Z.
      Body Image Dissatisfaction and Impulse Buying: A Moderated Mediation Model.
      ,
      • Qian Y.
      • Yu X.
      • Liu F.
      Comparison of Two Approaches to Enhance Self-Esteem and Self-Acceptance in Chinese College Students: Psychoeducational Lecture vs. Group Intervention.
      ,
      • Xiao X.
      • Zheng X.
      The Effect of Parental Phubbing on Depression in Chinese Junior High School Students: The Mediating Roles of Basic Psychological Needs Satisfaction and Self-Esteem.
      ]. We used the Chinese version in this study, which had an overall Cronbach’s alpha coefficient of 0.809, 0.774, 0.750, and 0.775 at T0, T1, T2, and T3, respectively, to measure self-esteem.

      Mindfulness

      The 39-item Five Facet Mindfulness Questionnaire (FFMQ) was first developed by [
      • Baer R.A.
      • Smith G.T.
      • Hopkins J.
      • Krietemeyer J.
      • Toney L.
      Using self-report assessment methods to explore facets of mindfulness.
      ] to assess mindfulness from five facets on a 5-point Likert scale: observing, describing, acting with awareness, non-judging, and non-reacting[
      • Baer R.A.
      • Smith G.T.
      • Hopkins J.
      • Krietemeyer J.
      • Toney L.
      Using self-report assessment methods to explore facets of mindfulness.
      ]. The original FFMQ has been translated into Chinese[
      • Deng Y.-Q.
      • Liu X.-H.
      • Rodriguez M.A.
      • Xia C.-Y.
      The Five Facet Mindfulness Questionnaire: Psychometric Properties of the Chinese Version.
      ] with good psychometric properties. In addition, a recent study continued to confirm the psychometric properties of the Chinese version in cancer patients using a Bayesian structural equation modeling approach[
      • Fong T.C.T.
      • Wan A.H.Y.
      • Wong V.P.Y.
      • Ho R.T.H.
      Psychometric properties of the Chinese version of Five Facet Mindfulness Questionnaire-short form in cancer patients: a Bayesian structural equation modeling approach.
      ]. We used the Chinese version in this study, which had an overall Cronbach’s alpha coefficient of 0.644, 0.704, 0.731, and 0.749 at T0, T1, T2, and T3, respectively, to measure mindfulness.

      Perceived stress

      The 10-item Perceived Stress Scale (PSS) was used to measure perceived stress on a linear 5-point Likert scale from 0 to 4[
      • Cohen S.
      • Kamarck T.
      • Mermelstein R.
      A global measure of perceived stress.
      ]. A higher score represents a greater stress level. The 10-item Chinese version has been validated and got a Cronbach’s alpha of 0.619[
      • Yuan L.X.
      • Lin N.
      Research on factor structure of perceived stress scale in Chinese college students (in Chinese).
      ]. We used the Chinese version in this study, which had an overall Cronbach’s alpha coefficient of 0.614, 0.608, 0.699, and 0.682 at T0, T1, T2, and T3, respectively, to measure perceived stress.

      Perceived stigma

      The 31-item Cataldo lung cancer stigma scale (CLCSS) was used to measure perceived stigma, categorized into stigma and shame, social isolation, discrimination, and smoking, on a linear 0- to 4-point[
      • Cataldo J.K.
      • Slaughter R.
      • Jahan T.M.
      • Pongquan V.L.
      • Hwang W.J.
      Measuring stigma in people with lung cancer: psychometric testing of the cataldo lung cancer stigma scale.
      ]. A higher score indicates a higher level of perceived stigma. Yu et al.[
      • Yu Y.
      • Wang L.
      • Zhang M.
      • Du Y.H.
      • Bai Y.
      • Liu J.E.
      Psychometric evaluation of the Chinese version of the Cataldo Lung Cancer Stigma Scale (CLCSS).
      ] translated the original version to Chinese and reported an overall Cronbach alpha of 0.932. In addition, 4 subscales had a Cronbach alpha of 0.799, 0.922, 0.863, and 0.803, respectively. This study used the Chinese version of the CLCSS, which had an overall Cronbach’s alpha coefficient of 0.863, 0.717, 0.709, and 0.730 at T0, T1, T2, and T3, respectively, to measure perceived stigma.

      Illness perception

      Weinman et al.[
      • Weinman J.
      • Petrie K.J.
      • Moss-Morris R.
      The Illness Perception Questionnaire: a new method for assessing illness perceptions.
      ] first developed the Brief Illness Perception Questionnaire (B-IPQ) to measure illness’s emotional and cognitive representations on a continuous linear 0 to 10 point. A higher score represents a more negative illness perception. Broadbent et al.[
      • Broadbent E.
      • Petrie K.J.
      • Main J.
      • Weinman J.
      The brief illness perception questionnaire.
      ] have shown a good test-retest reliability and predictive and discriminant validity of the B-IPQ. Xue et al.[

      Xue F, Lin Y. Brief illness perception questionnaire: Chinese version. Available at: www.uib.no/ipq/pdf/B-IPQ-Chinese.pdf.

      ] translated the original version to Chinese, and it has been widely used in China[
      • Zhang N.
      • Fielding R.
      • Soong I.
      • Chan K.K.
      • Lee C.
      • Ng A.
      • et al.
      Psychometric assessment of the Chinese version of the brief illness perception questionnaire in breast cancer survivors.
      ,
      • Schaefert R.
      • Höner C.
      • Salm F.
      • Wirsching M.
      • Leonhart R.
      • Yang J.
      • et al.
      Psychological and behavioral variables associated with the somatic symptom severity of general hospital outpatients in China.
      ]. We used the Chinese version in this study, which had an overall Cronbach’s alpha coefficient of 0.657, 0.676, 0.643, and 0.630 at T0, T1, T2, and T3, respectively, to measure illness perception.

      Statistical analysis

      We used descriptive statistics to present participants’ demographics. The Kolmogorov-Smirnov tests showed that, in addition to age and risk scores in the prediction algorithm, the distribution of scores for psychological distress, social support, coping style, self-esteem, mindfulness, perceived stress, perceived stigma, and illness perception was abnormal at most time points. However, we preferred to use mean ± standard deviation (SD) for all continuous variables because (a) parametric tests are more powerful than non-parametric tests, (b) the results of the Kolmogorov-Smirnov test are not necessarily true, especially for relatively large sample size[
      • Steinskog D.J.
      • Tjøstheim D.B.
      • Kvamstø N.G.
      A Cautionary Note on the Use of the Kolmogorov–Smirnov Test for Normality.
      ], and (c) according to kurtosis and skewness values, our data followed a normal distribution[
      • Kim H.-Y.
      Statistical notes for clinical researchers: assessing normal distribution (2) using skewness and kurtosis.
      ]. Therefore, we used the Chi-square test and independent-sample t-test to compare the variables between the two groups. However, repeated measure analysis of variance (ANOVA) was used to analyze changes or differences of variables between the groups (experimental vs. waiting-list groups), within-group (time), and interaction (group*time) effects.
      Furthermore, we used structural equation modeling to elucidate the mediating role of significant variables that showed significant differences in the efficacy of a four-week MBSR program on psychological distress between the two groups after intervention We first defined the interventions used in the experimental and waiting-list groups as dummy variables using 1 (experimental group) and 0 (waiting-list group), respectively. In addition, we adjusted all variables obtained from post-intervention using the baseline value[
      • Shenk C.E.
      • Putnam F.W.
      • Rausch J.R.
      • Peugh J.L.
      • Noll J.G.
      A longitudinal study of several potential mediators of the relationship between child maltreatment and posttraumatic stress disorder symptoms.
      ].
      We employed IBM Statistical Package for Social Sciences (SPSS) version 22.0 and Amos version 21.0 for statistical analysis.

      Ethical consideration

      This study strictly followed the statement of the Declaration of Helsinki. The ethical institutional board of the hospital approved this trial (approval number: CZLS2021183-A), and we also registered the study protocol at the Chinese Clinical Trials Registry (Approval identifier: ChiCTR2100041899). Before participating in this study, all eligible participants signed informed consent and were freely allowed to withdraw from this study.

      Results

      Recruitment

      As depicted in the CONSORT flow chart (see Figure 1), 299 lung cancer patients were eligible for evaluation, but 190 patients who were eligible agreed to participate in this study. Of the 190 patients, 95 were randomly assigned to the experimental or waiting-list groups. However, 12 and 3 patients received no interventions in the experimental and waiting-list groups. One hundred seventy-five patients completed the study and underwent T1 and T2 assessments; however, at the T3 assessment, 5 and 3 patients were missed from the experimental and waiting-list groups, respectively. There was no statistically significant difference in the lost participants between the two groups at T3 (P=0.480).

      Participants’ characteristics

      The mean age of the participants in the experimental and waiting-list groups was 58.98 (SD=9.72) and 59.90 (SD=8.72), respectively, without significant difference (P=0.507). Of the 175 patients analyzed, most patients were male (61.7%) and lived in the urban areas (58.9%). Most patients were married (97.1%) and had low education (85.7% with a middle-high school education or less). Most of the patients paid medical costs using resident basic health insurance (97.7%) and had no family history of lung cancer (96.0%). Still, most patients were pain free (68.0%), had no comorbidity (76.6%), and were at stage III or IV. There remaining demographic and clinical data of the two groups were no significantly different (P>0.05), as presented in Table 1.
      Table 1Demographic and clinical characteristics of the patients (N= 175).
      VariableExperimental (n=83)Control (n=92)t/χ2P-value
      Gender0.059*0.809
       Male5256
       Female3136
      Age, years58.98±9.7259.90±8.720.664#0.507
      Education3.086*0.214
       Primary school or below1526
       Middle and high school5752
       College and above1114
      Occupation6.726*0.081
       No work4238
       Working817
       Retire3037
      Marital status1.128*0.569
       Single10
       Married8090
       Divorced/widowed22
      Residence0.938*0.333
       City5251
       Rural areas3141
      Medical insurance1.248*0.264
       Self-payment31
       Residents’ basic health insurance8091
      Yearly income, yuan5.080*0.166
       <2000039
       20001-500002517
       50001-1000003846
       >1000001720
      Family history of LC1.040*0.308
       Yes25
       No8187
      Smoking history0.217*0.641
       Yes3940
       No4452
      TNM tumor stage3.055*0.383
       I1015
       II2215
       III1820
       IV3342
      Metastases1.361*0.506
       Yes4848
       No3543
      Comorbidities2.525*0.112
       Yes1526
       No6866
      Pain degree4.102*0.251
       No pain5465
       Mild1513
       Moderate139
       Severe15
      LC, lung cancer; TNM, tumor-node-metastasis. *χ2, #t.

      The effect of the intervention on outcomes

      The scores of seven variables between the two groups were not significantly different (P>0.05) at the baseline except for the score in the mindfulness, which was significantly higher in patients in the waiting-list group than patients in the four-week MBSR program group (t=4.746, P<0.001). After the intervention, as shown in Figures 2 and 3, apart from the coping style (F=1.386, P=0.250), the remaining variables changed significantly over time (P<0.05). As presented in Table 2, the four-week MBSR program significantly alleviated psychological distress (F=15.051, P<0.001), improved social support (F=16.465, P<0.001), enhanced mindfulness (F=17.207, P<0.001), and reduced perceived stigma (F=8.260, P=0.005) at immediate post-intervention, 1-month postintervention, and 3 months post-intervention. In addition, the difference in interventional effects between the two groups was also statistically significant over time (P<0.05).
      Figure 2
      Figure 2The changes of scores in psychological distress, social support, coping style, and self-esteem before and after intervention between the two group
      Figure 3
      Figure 3The change of scores in mindfulness, perceived stress, perceived stigma, and illness perception before and after intervention between the two groups
      Table 2A comparison of the outcome variables between the two groups before and after the intervention.
      VariableT0 (mean ± SD)T1 (mean ± SD)T2 (mean ± SD)T3 (mean ± SD)F1 (P)F2 (P)F3 (P)
      Experimental (n=83)Control (n=92)Experimental (n=83)Control (n=92)Experimental (n=92)Control (n=83)Experimental (n=78)Control (n=89)
      Risk score67.84±24.4266.39±29.90n.a.n.a.n.a.n.a.n.a.n.a.n.a.n.a.n.a.
      t=-0.350n.a.n.a.n.a.n.a.n.a.n.a.n.a.n.a.n.a.
      P=0.727n.a.n.a.n.a.n.a.n.a.n.a.n.a.n.a.n.a.
      Psychological distress2.70 ± 2.132.45 ± 2.211.16 ± 1.571.78 ± 1.741.07 ± 1.532.27 ± 1.270.43 ± 1.082.26 ± 1.2556.245 (<0.001)15.051 (<0.001)37.762 (<0.001)
      t=-0.617t=-2.519t=-6.278t=-9.580
      P=0.537P=0.012P=<0.001P=<0.001
      Social support57.31±7.1755.66±12.3264.02±7.3458.80±9.3864.48±8.3557.73±9.5065.30±6.4258.81±9.1133.911 (<0.001)16.465 (<0.001)8.598 (<0.001)
      t=-0.170t=-3.752t=-4.865t=-4.769
      P=0.865P<0.001P<0.001P<0.001
      Coping style50.77±4.8949.54±4.5049.10±3.5150.48±4.9349.47±3.7350.02±5.2349.56±5.2551.60±4.151.386 (0.250)1.515 (0.220)4.995 (0.005)
      t=-1.702t=-1.486t=-0.203t=-2.372
      P=0.091P=0.137P=0.839P=0.018
      Self-esteem27.72±4.0428.17±5.0029.59±4.3427.67±4.0029.00±4.5327.44±3.9128.30±4.7027.14±4.194.894 (0.006)2.425 (0.121)9.181 (<0.001)
      t=-0.754t=-3.018t=-2.765t=-2.419
      P=0.451P=0.003P=0.006P=0.016
      Mindfulness104.57±10.87111.97±9.03117.54±9.78110.88±7.71118.30±10.05110.59±6.98120.90±11.20110.31±6.6043.216 (<0.001)17.207 (<0.001)64.963 (<0.001)
      t=-4.746t=-4.540t=-5.138t=-6.568
      P<0.001P<0.001P<0.001P<0.001
      Perceived stress20.95±4.6420.48±4.6518.35±3.8619.97±2.9519.23±3.6219.55±3.0617.49±3.6119.26±3.0317.365 (<0.001)3.755 (0.054)5.405 (0.002)
      t=-1.099t=3.106t=-1.206t=3.498
      P=0.272P=0.002P=0.228P=0.001
      Perceived stigma75.83±15.1475.22±16.0663.57±8.2767.79±8.8762.55±7.5159.50±7.7068.58±9.1086.42 ± 9.1087.520 (<0.001)8.260 (0.005)12.988 (<0.001)
      t=-0.571t=-4.309t=-2.436t=6.995
      P=0.568P=<0.001P=0.016P=<0.001
      Illness perception48.19±7.8146.98±4.6343.20±7.0045.00±7.6943.00±7.4945.62±12.1742.21±7.2045.13 ± 12.2015.240 (<0.001)2.365 (0.126)4.760 (0.009)
      t=-0.782t=1.571t=-1.080t=-1.539
      P=0.434P=0.118P=0.280P=0.124
      T0, baseline; T1, the immediate post intervention; T2, 1-month post-intervention; T3, 3 months post intervention; F1, time effect; F2, group effect; F3, group*time effect; SD, standard deviation.

      Results of the mediating analysis

      We only included three variables in the mediation analysis, including social support, mindfulness, and perceived stigma, according to pre-designed criteria. After structural equation modeling and appropriate adjustment of the pathways between variables according to the modification index and empirical evidence, the model fitted our data better (χ2/df=3.451, CFI=0.893, TLI=0.855, RMSEA=0.122 [95% CI: 0.108-0.136]).
      Overall, the effects of the four-week MBSR program on psychological distress at T1, T2, and T3 was -0.274, -0.292, and -0.358, respectively. At the immediate post-intervention (T1), the four-week MBSR program alleviated psychological distress directly (β=-0.274, P=0.005), not mediated by other variables. The effect of the four-week MBSR program on mindfulness at T1 and T2 continued to help alleviate psychological distress at T2 (β=-0.049). The effects of the four-week MBSR program on social support and mindfulness at T1 and T2 also continued to alleviate psychological distress at T3 by reducing perceived stigma at T2 and T3 (β=-0.039). The effect of the four-week MBSR program on perceived stigma at T1, T2, and T3 also influenced psychological distress at T3 (β=-0.081). Moreover, there was a continuous effect between psychological distress from T1 to T3 (β=0.886 from T1 to T2, β=0.816 from T2 to T3), indicating that the four-week MBSR program had a persistent effect on psychological distress (β=-0.198). The results of mediation analysis are summarized in Table 3, and the mechanism pathways are depicted in Figure 4.
      Table 3Path coefficient of variables in intervention mechanism analysis.
      PathwayΒ95% CIP
      Total effects-0.924
      Psychological distress (T1)-0.274-0.461 to -0.1440.005
      Psychological distress (T2)-0.292-0.434 to -0.7150.005
      Psychological distress (T3)-0.358-0.530 to -0.2370.005
      Direct effects-0.274-0.461 to -0.1440.005
      Psychological distress (T1)-0.274
      Indirect effects-0.650
      Psychological distress (T2)-0.292-0.434 to -0.1750.005
       Intervention → Psychological distress (T1) → Psychological distress (T2)-0.274*0.886 = -0.243
       Intervention → Mindfulness (T1) → Mindfulness (T2) →Psychological distress (T2)-0.141*0.415*0.844 = -0.049
      Psychological distress (T3)-0.358-0.401 to -0.2360.005
       Intervention → Psychological distress (T1) → Psychological distress (T2) → Psychological distress (T3)-0.274*0.886*0.816 = -0.198
       Intervention → Mindfulness (T1) → Mindfulness (T2) → Perceived stigma (T3) → Psychological distress (T3)-0.129*0.415*0.844**0.160 = -0.007
       Intervention → Mindfulness (T1) → Mindfulness (T2) → Psychological distress (T2) → Psychological distress (T3)-0.141*0.415*0.844*0.816 = -0.040
       Intervention → Perceived stigma (T1) → Perceived stigma (T2) →Perceived stigma (T3) → Psychological distress (T3)-0.403*0.768*1.639*0.160 = -0.081
       Intervention → Social support (T1) → Social support (T2) → Psychological distress (T3)-0.132*0.264*0.827* = -0.029
       Intervention → Social support (T1) → Social support (T2) → Perceived stigma (T2) → Perceived stigma (T3) → Psychological distress (T3)-0.052*0.264*0.827*1.639*0.160 = -0.003
      T1, immediate post-intervention; T2, 1-month post-intervention; T3, 3 months post-intervention; β, standardized regression coefficients; CI, confidence interval.
      Figure 4
      Figure 4Mechanism model of the four-week MBSR program to alleviate psychological distress in lung cancer patients. MBSR, mindfulness-based stress reduction.

      Discussion

      In this study, we aimed to validate the interventional effects of a four-week MBSR program on psychological distress in lung cancer patients, and to further elucidate the psychosocial mechanisms by which the program alleviates psychological distress. Our findings suggest that the four-week MBSR program, as an effective psychological intervention, significantly alleviates the psychological distress. The four-week MBSR program also improved patients’ social support considerably, enhanced mindfulness, and reduced perceived stigma. Furthermore, the results of the structural equation modeling suggest that the four-week MBSR program can exert an interventional effect by directly targeting psychological distress. Meanwhile, the four-week MBSR program supports continuous interventional effects on psychological distress by indirectly affecting social support, mindfulness, and perceived stigma.
      MBSR has been extensively used in cancer settings[
      • Cillessen L.
      • Johannsen M.
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      ,
      • Lee C.E.
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      Effects of a Mindfulness-Based Stress Reduction Program on the Physical and Psychological Status and Quality of Life in Patients With Metastatic Breast Cancer.
      ]. Currently, many meta-analyses[
      • Huang H.P.
      • He M.
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      A meta-analysis of the benefits of mindfulness-based stress reduction (MBSR) on psychological function among breast cancer (BC) survivors.
      ,
      • Cillessen L.
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      ,
      • Xunlin N.G.
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      • Klainin-Yobas P.
      The effectiveness of mindfulness-based interventions among cancer patients and survivors: a systematic review and meta-analysis.
      ,
      • Zhang Q.
      • Zhao H.
      • Zheng Y.
      Effectiveness of mindfulness-based stress reduction (MBSR) on symptom variables and health-related quality of life in breast cancer patients-a systematic review and meta-analysis.
      ,
      • Haller H.
      • Winkler M.M.
      • Klose P.
      • Dobos G.
      • Kümmel S.
      • Cramer H.
      Mindfulness-based interventions for women with breast cancer: an updated systematic review and meta-analysis.
      ] have demonstrated the benefits of MBSR program in improving the psychological well-being of cancer patients. Furthermore, our recent meta-analysis confirmed that the MBSR program significantly diluted negative psychological states and enhanced positive psychological states. In this study, we further validated the beneficial role of the MBSR program in alleviating psychological distress in lung cancer patients. Although it remains not entirely unclear why and how the MBSR program improves psychological wellbeing, previous studies[

      Kabat-Zinn J, Santorelli S. Mindfulness-Based Stress Reduction Professional Training-Scientific Papers from the Stress Reduction Clinic. Boston: Center for Mindfulness in Medicine. Health Care, and Society, UMMS 2002.

      ,
      • Kabat-Zinn J.
      • Lipworth L.
      • Burney R.
      The clinical use of mindfulness meditation for the self-regulation of chronic pain.
      ,

      Kabat-Zinn J. Mindfulness-based interventions in context: past, present, and future. 2003.

      ] suggest that the practice of mindfulness instructs participants to deliberately focus on the present moment and monitor the unfolding of experiences all the time without passing judgment. As a result, participants experience profound benefits through the mind-body connection. Thus, it is plausible that lung cancer patients experience significant alleviation in psychological distress, improvement in social support, enhancement in mindfulness, and reduction in perceived stigma following a four-week MBSR program.
      This study also showed that the MBSR program had a retained effect on psychological distress after ending the intervention through indirect effects of social support, mindfulness, and perceived stigma. Both mindfulness[
      • Kabat-Zinn J.
      Mindfulness-based interventions in context: past, present, and future.
      ] and social support[
      • Teixeira R.J.
      • Pereira M.G.
      Psychological morbidity, burden, and the mediating effect of social support in adult children caregivers of oncological patients undergoing chemotherapy.
      ] are positive sources for copying with negative psychological states, and our previous studies have demonstrated the inverse association between mindfulness and social support and psychological distress[
      • Tian X.
      • Jin Y.
      • Chen H.
      • Tang L.
      • Jiménez-Herrera M.F.
      Relationships among Social Support, Coping Style, Perceived Stress, and Psychological Distress in Chinese Lung Cancer Patients.
      ,
      • Tian X.
      • Jin Y.
      • Chen H.
      • Tang L.
      • Jiménez-Herrera M.F.
      The positive effect of social support on psychological distress among Chinese lung cancer patients: The mediating role of self-esteem.
      ,
      • Tian X.
      • Tang L.
      • Yi L.J.
      • Qin X.P.
      • Chen G.H.
      • Jiménez-Herrera M.F.
      Mindfulness Affects the Level of Psychological Distress in Patients With Lung Cancer via Illness Perception and Perceived Stress: A Cross-Sectional Survey Study.
      ]. In contrast, stigma, a negative emotional experience that includes isolation, rejection, degradation, and criticism due to undesirable conditions[
      • Cataldo J.K.
      • Slaughter R.
      • Jahan T.M.
      • Pongquan V.L.
      • Hwang W.J.
      Measuring stigma in people with lung cancer: psychometric testing of the cataldo lung cancer stigma scale.
      ], has been demonstrated to be a predictor of psychological distress in lung cancer patients[
      • Rose S.
      • Boyes A.
      • Kelly B.
      • Cox M.
      • Palazzi K.
      • Paul C.
      Lung cancer stigma is a predictor for psychological distress: A longitudinal study.
      ]. In general, psychosomatic balance plays a vital role in regulating the psychological well-being of cancer patients[
      • Bãrbuş E.
      • Peştean C.
      • Larg M.I.
      • Piciu D.
      Quality of life in thyroid cancer patients: a literature review.
      ]. Therefore, patients would suffer from significant physical and psychological problems when specific events (e.g., cancer diagnosis) destroyed psychosomatic balance[
      • Zhang Q.
      • Zhao H.
      • Zheng Y.
      Effectiveness of mindfulness-based stress reduction (MBSR) on symptom variables and health-related quality of life in breast cancer patients-a systematic review and meta-analysis.
      ].
      According to the Mindful Coping Model[
      • Garland E.
      • Gaylord S.
      • Park J.
      The role of mindfulness in positive reappraisal.
      ], we can easily explain why MBSR program can consistently affect psychological distress through social support, mindfulness, and perceived stigma. Specifically, the destructive effects of internal and external stressors (e.g., cancer diagnosis, anti-cancer treatment, and symptom burden) can cause psychological distress in patients; however, the implementation of an MBSR program can initiate psychological adjustment to trigger or enhance the protective effects of positive sources (improvement in social support, enhancement in mindfulness) and weaken the harmful effects of negative sources (reduction in perceived stigma)[
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      Interventions to improve psychosocial well-being in female BRCA-mutation carriers following risk-reducing surgery.
      ], and may then significantly dilute the destructive impacts of stressors (alleviation in psychological distress)[
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      ].

      Strengths and Limitations

      Overall, our study obtained these valuable findings due to several strengths. First, we enrolled both patients with clinically significant psychological distress and those at high risk of psychological distress by applying both DT and the risk prediction algorithm we developed, which significantly expanded the applicability of our findings in clinical practice. Second, we estimated the theoretical sample size from our meta-analysis, which ensured the statistical power of our results. Third, we explored the intervention mechanisms of the four-week MBSR program by determining the role of significant variables after the intervention, which benefited more simply revealing the active ingredients of the four-week MBSR program. Fourth, all potential mediating variables included in the intervention mechanism analysis have been previously investigated for their role in the development of psychological distress, increasing the reliability of theoretical evidence. Finally, our study was also rated as high in methodological quality because it met the six Cochrane collaboration criteria for high-quality trials[
      • Higgins J.P.T.
      • Altman D.G.
      • Gøtzsche P.C.
      • Jüni P.
      • Moher D.
      • Oxman A.D.
      • et al.
      The Cochrane Collaboration's tool for assessing risk of bias in randomised trials.
      ], except that blinding participants due to the nature of the psychological intervention.
      We cannot deny the fact that our study has several limitations. First and foremost, we used self-reported instruments to collect data, which may affect the accuracy of the results. Therefore, more objective tools need to be developed to measure these variables. Second, we recruited potentially eligible participants from only one hospital in southwest China due to the limited time. Therefore, we unable to eliminate the adverse impact of selection bias and time constraints on our findings. As a result, adequately powered studies with more extended intervention and follow-up duration are warranted to demonstrate our findings. Third, we selected only those variables tested in our previous studies to explore possible mechanisms of the MBSR program on psychological distress. However, we did not consider those factors that we did not investigate previously. Therefore, more intervention mechanisms analysis is needed to fully reveal the nature of MBSR program in alleviating psychological distress in lung cancer patients. Fourth, we used a four-week MBSR program with abbreviated sessions instead of a standard eight-week MBSR program in this study, which may have underestimated the intervention effect of the MBSR program due to inadequate duration of intervention. Therefore, future studies should further balance the interventional effects and applicability of the MBSR program in lung cancer patients. More importantly, it is necessary to further investigate the interventional effects of the enhanced protocol with adequate sessions in future studies. Fifth, the mechanism model fitted our data relatively when we explored the intervention mechanism of the MBSR program to alleviate psychological distress, which limited the generalization of our results. Therefore, considering that limited participants were enrolled in our study, we suggest future studies with larger sample sizes to further elucidate the intervention mechanism of the MBSR program in alleviating psychological distress. Sixth, we chose brief versions of the scales to ensure the quality of the data collection process in this study; however, the average time for a patient to complete all scales was still up to 45 minutes. Although no patients were excluded for failing to complete scales, we could not eliminate the psychological burden caused by the need to complete multiple scales. Finally, in this study, we did not consider the impacts of sleep, fatigue, and exercise on the psychological status of lung cancer patients. Therefore, we suggest future studies to address this limitation.

      Conclusions

      In summary, the present study validated the intervention effect of the MBSR program in alleviating psychological distress, and provided relatively robust and reliable evidence for clinical practitioners to integrate the MBSR program into usual care to improve psychological well-being of lung cancer patients. Meanwhile, this study also suggested the positive effects of MBSR program on social support, mindfulness, and perceived stigma, which provided a reference for the application of MBSR program to improve clinical outcomes. Furthermore, this study revealed the direct impact of the MBSR program on short-term psychological distress. Additionally, it indicated the continuous effect of the MBSR program on psychological distress through social support, mindfulness, and perceived stigma.

      Authors’ contributions

      Conceived and designed the analysis: Xu Tian, Gui-Hua Chen, María F. Jiménez Herrera.
      Collected the data: Xu Tian, Zhong-Li Liao, Ling Tang.
      Contributed data or analysis tools: Xu Tian, María F. Jiménez Herrera.
      Performed the analysis: Xu Tian, Zhong-Li Liao, Li-Juan Yi.
      Wrote the paper: Xu Tian, Zhong-Li Liao, Gui-Hua Chen, María F. Jiménez Herrera.

      Funding

      This study was supported by the Chongqing Natural Science Foundation (project number: cstc2020jcyj-msxmX0212), the Basic Science and Frontier Technology Research Project of Chongqing (project number: cstc2048jcyjAX0775), and the Medical Research Project which was jointly approved by the Chongqing Science and Technology Bureau and Health Commission of Chongqing Municipal City (project number: 2022MSXM067).

      Declaration of competing interest

      None declared.

      Ethics statement

      This study was approved by the Clinical Research Ethics Board of the Chongqing University Cancer Hospital (Approval No. CZLS2021183-A).

      Author Agreement Statement

      We the undersigned declare that this manuscript is original, has not been published before and is not currently being considered for publication elsewhere. We confirm that the manuscript has been read and approved by all named authors and that there are no other persons who satisfied the criteria for authorship but are not listed. We further confirm that the order of authors listed in the manuscript has been approved by all of us. We understand that the Corresponding Author is the sole contact for the Editorial process. He/she is responsible for communicating with the other authors about progress, submissions of revisions and final approval of proofs.

      Declaration of interests

      The authors declare that they have no known competing financial interests or personal relationships that could have appeared to influence the work reported in this paper.

      Acknowledgements

      The authors would like to acknowledge the funding support of the Chongqing Natural Science Foundation, the Basic Science and Frontier Technology Research Project of Chongqing, and the Medical Research Project which was jointly approved by the Chongqing Science and Technology Bureau and Health Commission of Chongqing Municipal City, China. We also thank the lung cancer patients who participated in this study.

      Appendix A. Supplementary data

      The following is/are the supplementary data to this article:

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