Mindfulness-based interventions and cognitive function among breast cancer survivors: a systematic review

We included studies that used mindfulness as the primary intervention and assessed impact on cognitive change in breast cancer survivors. A total of six studies were included in this review (Fig. 2). Of the included studies, five used a randomized controlled design [17, 22‐25]. The sixth study was a prospective cohort study comparing pre- and post- scores in a group of women participating in a mindfulness-based stress reduction intervention (MBSR) [26]. Studies included were conducted in the United States, Germany and Iran. Control groups included usual care (UC) [23‐25], waitlist controls [22], and fatigue education and support (ES) [17]. The sample size ranged from 24 to 322 breast cancer survivors. The mean age of mindfulness group participants was 53.1 years. Mean time since diagnosis was reported for two [22, 26] of the studies (2.3 ± 3.88 and 3.9 ± 5.1 years), while mean time since treatment was reported in two [17, 25] other studies (0.66 ± 0.51 and 2.4 years). The last two studies reported neither elapsed time measure [23, 24]. Five of the studies only included survivors of non-metastatic breast cancer [17, 23‐26], while the sixth included all post-treatment breast cancer survivors [22]. Follow-up time occurred at post-intervention (6, 8 or 11 weeks) in all of the studies, as well as 2, 3 or 6-months post-intervention in five of the studies [17, 23‐26]. Study characteristics are summarized in Tables 1 and 2.

Generally, rates of retention were high in the included studies. Retention in MBSR intervention groups ranged from 83.8–94.3%, with comparable rates of retention in the control groups [17, 22, 25, 26]. Two studies did not include information on loss-to- follow-up [23, 24]. Still, future studies should continue to consider methods to recruit and retain participants.

In five of the included intervention studies, participants were randomized to receive mindfulness therapy or a control therapy, which ranged from wait-list control to cognitive, psychosocial, or fatigue education. Four of the programs utilized the MBSR program developed by Kabat-Zinn [17, 22‐24]. MBSR was developed for chronic pain and anxiety, and consists of 8 weekly 2-h long classes [27]. Each class contains elements of controlling and self-regulating attention, in order to help control and reduce stress and associated symptoms. Participants are given education materials on mind-body practices and mediations, are instructed to practice meditation during weekly sessions and at home, and receive practice tools to reduce barriers to mindfulness. Attention on the breath, focused body-scans, Hatha yoga, and walking meditation are also emphasized as mind-body practices. Additionally, in traditional MBSR, a 7.5-h meditation retreat takes place during the sixth week of the intervention. Lengacher et al. adapted the widely-used MBSR program for breast cancer survivors (MBSR-BC) [28] which was used by Reich et al. study [25]. Similar in structure to MBSR, MBSR(BC) involves 2-h sessions for 6 to 8 weeks that focus on the same elements of attention and attention control. The modified program also encourages 15–45 min of formal meditation 6 days a week, as well as 15–45 min of informal meditation while doing usual activities (e.g. walking, driving, or eating). Participants are given audio recordings of daily, guided meditations and are asked to keep a daily meditation diary. MBSR(BC) does not always include a meditation retreat [29]. Doctoral level clinical psychologists or physicians with MBSR experience instruct both versions of this mind-body intervention. There is no specified group size, but the majority of groups range from 10 to 15 participants.

The other study included in our review combined elements of MBSR, naturopathic and self-care methods and a Mediterranean diet, during a weekly semi-residential 6-h session once weekly over 11 weeks [26]. This program was designed to include an entire MBSR course, including the mindfulness retreat, in addition to the other elements, to create a longer and more intensive intervention. MSc- or PhD-level health professionals, who are trained in MBSR and psychosocial counseling, delivered the program.

A major challenge in comparing and summarizing studies of cognitive function in cancer survivors stems from variation in cognitive measurement. There is no single validated scale for self-reported cognition assessment in breast cancer patients, and 2011 research recommendations suggest objective tests of cognition or subjectively assessing mood and fatigue may more adequately measure cognitive impairment [6]. The tools used in the studies included in this review are summarized in Table 3 including example questions. Self-report measures included the European Organization for Research and Treatment of Cancer Quality of Life Questionnaire - C30 (EORTC QLQ-C30) survey [22‐24, 26], Cognitive and Affective Mindfulness Scale (CAMS) [25], Everyday Cognition Scale (ECog) [25], Attentional Function Index (AFI) [17], and the Calgary Symptoms of Stress Index (C-SOSI) [22].The EORTC QLQ-C30 is designed for cancer patients in clinical trials and includes a cognitive functioning sub-scale with two questions assessing difficulty with concentration and memory [30]. The CAMS is used to conceptualize and report on mindfulness, with questions specific to concentration and attention regulation [31]. The informant-rated ECog scale has been validated against the Blessed Dementia Rating Scale (BDSR), Clinical Dementia Rating Scale (CDR), Mini-Mental State Exam (MMSE), and clinical diagnosis records, and includes 6 sub-factors (everyday memory, language, visuospatial abilities, planning, organization, and divided attention) and one global factor, to create an assessment of everyday cognitive function [32]. The AFI assesses self-perceived selective attention and working memory in completing daily activities [33]. Last, the C-SOSI was designed to measure multiple domains of stress in a concise manner, and includes a sub-scale evaluating cognitive disorganization [34]. The study by Reich et al. specifically sought to evaluate the relationship between symptom assessment tools and four symptom clusters (pain, psychological, fatigue and cognition), and reported a beta of 0.94 between the ECOG (memory scale) and the cognitive cluster, but a beta value of only 0.33 between the CAMS (total score) and the cognitive cluster, suggesting the importance of tool selection in evaluating cognition [25]. One study [17] also used a widely used neuropsychological test, the Stroop-Word Test, which was designed to evaluate inhibition of cognitive interference, as well as attention, processing speed, cognitive flexibility and working memory [35‐38].

In the included studies, mindfulness interventions had heterogeneous impacts on cognition (Table 1). One study showed no significant differences comparing post-intervention cognitive cluster scores between the mindfulness and control groups [25], while another study showed no significant differences in improvements to cognitive disorder between the mindfulness intervention and waitlist controls groups (p = 0.052) [22]. Two studies showed significant cognitive improvements in mindfulness intervention groups in a pre-and-post test assessment compared to usual care. Improvements were sustained to a lesser extent at the two (η = 0.20) [24] or three (R² = 0.234) [26] month follow-up. Two other studies showed significantly improved cognition in the mindfulness group compared to control groups, with results sustained at both two- (ηp² = 0.35) [23] and six- month (Cohen’s d = 0.55) [17] follow-ups. No studies reported significant differences by group at baseline, with the exception of greater use of anxiolytic medications in the MBSR(BC) group in the study by Reich et al [25].

Johns et al. also noted that cognitive function improved over time in both the MBSR and fatigue education/support groups, but that the MBSR participants experienced greater improvements and that the improvements were sustained at the six-month follow-up [17]. In the two studies showing sustained improvement, cognition was assessed using the EORTC QLQ-C30 [23] and the AFI [17]. Cognitive impairment in studies utilizing the EORTC QLQ-C30 specifically assessed attention and memory, based on two questions within a larger scale. Meanwhile, significant results on the AFI suggested improvement in both effective action and attentional lapse, as well as on overall attentional function.

Furthermore, using the Stroop-Word test, Johns et al. found that women in the MBSR group made fewer errors compared to the fatigue education group both at the eight-week post-intervention assessment at the six-month follow-up, suggesting sustained improvement in accuracy over time [17]. Stroop reaction time did not differ between groups. Furthermore, in the study conducted by Lerman et al. no significant improvement was noted for the cognitive disorganization (attention, planning, and organization) subscale of the SOSI [22].

Of note, the study by Reich et al. examined symptom clusters and found that although there were no significant improvements in the cognition symptom cluster, which consisted of everyday memory and an overall cognition and mindfulness score, MBSR did result in significant improvements in the fatigue and psychological symptom clusters, which may impact cognitive impairment in breast cancer patients [25]. Reich et al. commented on the potential use of MBSR to address multiple co-occurring symptoms, with the added benefit of individuals being able to practice techniques on their own [25]. The authors emphasized the importance of understanding related symptoms and managing multiple symptoms to improve overall well-being.

Three of the included studies [17, 25, 26] received a rating of “good”, one study [22] received a rating of “fair”, and the other two studies [23, 24] received a rating of “poor.”

The study by Lerman et al., rated as “fair,” did not have any major shortcomings, but there was insufficient information to answer all of the questions on the risk of bias assessment. Of note, the “poor” studies both reported associations between mindfulness and cognitive function improvement.’ The results of the risk of bias assessments are included in Additional file 1: Table S1A and B.