Mindfulness-Based Interventions For Coping With Cancer

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Ann. N.Y. Acad. Sci.

ISSN 0077-8923

A N N A L S O F T H E N E W Y O R K A C A D E M Y O F SC I E N C E S
Issue: Meditation

Mindfulness-based interventions for coping with cancer


Linda E. Carlson
Division of Psychosocial Oncology, Department of Oncology, Cumming School of Medicine, University of Calgary, and
Department of Psychosocial Resources, Tom Baker Cancer Centre, Alberta Health Services CancerControl, Calgary, Alberta,
Canada

Address for correspondence: Dr. Linda E. Carlson, Department of Psychosocial Resources, Holy Cross Site, 2202 2nd St.
S.W., Calgary, Alberta, Canada T2S 3C1. l.carlson@ucalgary.ca

Work in the development and evaluation of mindfulness-based interventions (MBIs) for cancer care has been
underway for the last 20 years, and a growing body of literature now supports their efficacy. MBIs are particularly
helpful in dealing with common experiences related to cancer diagnosis, treatment, and survivorship, including loss
of control, uncertainty about the future, and fears of recurrence, as well as a range of physical and psychological
symptoms, including depression, anxiety, insomnia, and fatigue. Our adaptation, mindfulness-based cancer recovery
(MBCR), has resulted in improvements across a range of psychological and biological outcomes, including cortisol
slopes, blood pressure, and telomere length, in various groups of cancer survivors. In this paper, I review the rationale
for MBIs in cancer care and provide an overview of the state of the current literature, with a focus on results from three
recent clinical trials conducted by our research group. These include a comparative efficacy trial comparing MBCR
to supportive–expressive therapy in distressed breast cancer survivors, a non-inferiority trial comparing MBCR to
cognitive behavioral therapy for insomnia in cancer survivors with clinical insomnia, and an online adaptation of
MBCR for rural and remote cancer survivors without access to in-person groups. I conclude by outlining work in
progress and future directions for MBI research and applications in cancer care.

Keywords: meditation; mindfulness; cancer; stress; anxiety; depression

Introduction and behavioral flexibility, exposure to challenging


stimuli, and clarification of key life values and
Mindfulness is often defined as paying attention in
priorities.1,2
the present moment, with nonjudgmental accep-
Within the realm of cancer care, my group and
tance of experience. Shapiro and I have defined
others have been applying principles of mind-
mindfulness as consisting of three key axioms:
fulness, explicitly training people diagnosed with
intention, attention, and attitude.1 Intention lightly
cancer in mindfulness meditation, and assessing
directs the focus of practice, while attentional
the effects of such training since the mid-1990s. We
skills are trained through sustained practice of
have learned much about the feasibility and efficacy
directing and redirecting attention to aspects of the
of these interventions across a wide range patients
present moment. All of this is done with attitudes
and outcomes, including psychological, behavioral,
of kindness and curiosity. Mindfulness is thought
physiological, and biological markers of health. In
of both as a way of being in the world (one can be
this paper, I review the rationale for the application
mindful) and as a concrete practice (mindfulness
of mindfulness-based interventions (MBIs) for
meditation). One objective of the wide variety of
people living with cancer and review some of the key
mindfulness meditation practices is to enhance
studies and outcomes, especially newer, larger, and
the quality of being mindful in everyday life. The
well-designed studies, with a focus on work from
effects of systematically practicing mindfulness are
our research group evaluating the mindfulness-
thought to arise through a variety of mechanisms,
based cancer recovery3 (MBCR) program.
including improved emotion regulation, cognitive

doi: 10.1111/nyas.13029
Ann. N.Y. Acad. Sci. xxxx (2016) 1–8 
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Mindfulness and cancer Carlson

Why mindfulness? repetitive and consistent application of awareness


of present-moment experience, with a kind, curi-
There are several characteristics of a cancer experi-
ous, and nonjudgmental attitude. This typically
ence, and of illness experience in general, that are
begins with training in focused attention on the
especially amenable to a mindfulness approach. A
breath or bodily sensation through body scanning,
diagnosis often challenges the commonly held world
sitting meditation, and mindful movement. Once
view that life is predictable and controllable. On an
stability of attention has been established through
existential level, people are forced to confront their
ongoing practice, a broadening of attention (“bare
own mortality in a real way, often for the first time.
awareness”) is applied, which allows an individual
Substantial and potentially permanent changes in
to directly experience one’s own mind for what it
functional abilities, appearance, and lifestyle may
is: transient, impersonal, and constantly changing.
follow, as well as having to face the possibility of
Through observation, participants can also directly
ongoing pain and dysfunction. Life plans are neces-
experience how grasping at certain outcomes or
sarily altered, and the future is premised on whether
states of being causes suffering, and through that
the illness comes back or gets worse. Most people
insight, learn to let go of clinging and personaliza-
experience significant fear, anxiety, and depression.
tion of experience. Repetitive practice of alternative
After treatment, no matter how positive the progno-
responses to difficult emotions or thoughts dur-
sis may be, for most people, there is a lingering fear
ing meditation helps retrain the brain to respond
of recurrence or progression, which turns every ache
in ways that are supportive of more positive
and pain into a potential life threat and can result
emotions.
in constant anxious monitoring. Mindfulness prac-
A mindfulness approach is eminently adaptable
tices allow a short-circuiting of this process to pre-
to a wide array of circumstances, including living
vent such escalation. Indeed, many of these common
with cancer. Simply absorbing the general under-
cancer-related problems are amenable to treatment
standing that the only certainty in life is change, and
through mindfulness training, which is especially
that sometimes the best thing to do to solve a prob-
helpful in dealing with uncontrollable, unpre-
lem is accept it, can be extremely relieving and even
dictable, and emotionally charged life stressors.
liberating to people who are desperately and often
Psychologists often classify problems as either
frantically trying to fix things. Acceptance in this
those that can be solved with problem-focused
context does not equate to “giving up” or not trying
coping techniques or those that require emotion-
to treat one’s illness; rather, it acknowledges the facts
focused coping. Problem-focused coping is useful
and allows a turning away from blame toward accep-
when there are tasks to be done to solve the prob-
tance of the reality of loss and grief. Realizing that,
lem. People therefore embrace their treatment reg-
in fact, one can slow down and see things as they
imens, attend their appointments, and do whatever
are, without blinders, and learn ways to hold strong
they can to ensure a positive outcome. In response to
emotions and sensations even in the face of can-
feeling a loss of control, many people try even harder
cer, can be transformative. The further realization
to control some aspects of their lives and solve the
that, although specific symptoms may be unpleas-
problems, but this is often a losing battle. Much
ant, they are tolerable and constantly in flux can
of the illness experience requires emotion-focused
provide alleviation of suffering. Stepping back and
coping, rather than problem solving, which can be
seeing the racing thoughts, worries, and self-blame
difficult for many people who are not well trained
as just thoughts, and not necessarily the truth, pro-
in that area. MBIs offer a form of emotion-focused
vides further relief. Hence, change occurs not only
coping, which allow people to actually embrace
by training the mind through formal mindfulness
uncertainty. Learning how to accept our fundamen-
practice, but through a shift in attitude and perspec-
tal inability to control or change the course of ill-
tive that allows people to see their illness in a new
ness progression (and ultimately death) is where
light, without allowing fear to consume them and
emotion-focused approaches, such as MBIs, can
drive behavior. This approach can provide energy
be especially helpful for people facing a cancer
and motivation for moving forward in life’s jour-
diagnosis.
ney, whatever the future holds.
The core training in MBIs involves the develop-
Hence, mindfulness training offers a venue
ment of stable and kind mindful attention, through
for coping with these often uncomfortable and
2 Ann. N.Y. Acad. Sci. xxxx (2016) 1–8 
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Carlson Mindfulness and cancer

difficult emotions elicited by a cancer diagnosis, in a Our program for people living with cancer,
safe and controlled container of one’s own making. MBCR, is an adaptation of MBSR. Structurally, we
By adopting a stance of observer to overwhelming still have 8 sessions with a weekend retreat and
thoughts and emotions, patients can take a step back require similar daily home practice, but the sessions
and allow themselves to process these experiences at are shorter—1.5 to 2 h—in recognition of the lim-
their own pace, seeing their experience as constantly ited energy of many of our participants. The core
changing and their distressing thoughts as simply principles and practices are essentially the same.
mind events that are often untrue. Ultimately, they We have included specific material on coping with
begin to see that they are more than a cancer patient; cancer; further focus on symptoms, such as sleep
they are connected to, and supported by, everyone problems, pain, and fear of cancer recurrence; and
who shares this human condition. some cognitive coping strategies based on cognitive
behavioral therapy principles. We include helpful
imagery, such as the mountain meditation, and also
Mindfulness-based interventions
emphasize loving-kindness practice toward the self
Over the past three decades, there has been a grow- and others. There is a strong component of mindful
ing clinical and research interest in the practice of movement through yoga postures and emphasis on
mindfulness meditation, owing in large part to the group process and group support.
pioneering work of Jon Kabat-Zinn at the University
Summary of the literature
of Massachusetts Medical Center. The mindfulness-
based stress reduction (MBSR)4 program that he There is now a large body of work investigating the
devised in the late 1970s, based on intensive secu- efficacy of MBIs for patients with various types of
lar training in mindfulness meditation techniques, cancer, which has been reviewed repeatedly over the
has since been adapted for treating many differ- last decade.5–18 A 2009 meta-analysis of 10 stud-
ent conditions, and thousands of studies have been ies found a medium-sized effect on psychosocial
conducted investigating its efficacy. The original outcome variables (d = 0.48), but only a small
impetus for developing MBSR was to help patients effect on the handful of physical biomarker vari-
who seemed to be falling through the cracks of the ables measured up to that point (d = 0.18).5 A more
system, suffering from unrelieved complex medi- recent meta-analysis of 19 studies reported similar
cal conditions and symptoms that often involved effect sizes on mood (d = 0.42) and distress (d =
untreated pain and anxiety. In the first stud- 0.48), but did not look at biological outcomes.7 Two
ies of MBSR, Kabat-Zinn documented improve- other recent meta-analyses focused on breast can-
ments in pain and anxiety that proved to be long cer patients exclusively, reporting large effect sizes
lasting.4 on stress (d = 0.71) and anxiety (d = 0.73) across
The MBSR program is structured as an 8-week nine studies with various designs,15 as well as small
group program of 2.5-h weekly sessions that incor- effects on depression (d = 0.37) and medium effects
porate intensive training in mindfulness medita- on anxiety (d = 0.51) in three randomized con-
tion with group reflection and mindful Hatha yoga trolled trials (RCTs).16 Piet et al. examined 22 ran-
practice. In weekly sessions participants learn fun- domized and nonrandomized studies and reported
damentals of the mind–body connection and how moderate effect sizes on anxiety and depression in
their interpretations of the world can cause both nonrandomized studies (d = 0.60 and 0.42, respec-
physical and mental suffering. The primary medita- tively) and slightly smaller effects for RCTs.18 I also
tion techniques used to cultivate mindfulness in the reviewed MBI studies for all medical illnesses, apply-
MBSR program are the body scan, sitting medita- ing the criteria for assigning levels of evidence, and
tion, walking meditation, and loving-kindness med- concluded there is level 1 (highest) evidence for the
itation, in conjunction with mindful yoga postures, efficacy of MBIs in oncology.17
with new material building upon previous weeks’ Looking at individual studies, the first publica-
training and practice. Participants are instructed to tion of an MBI in cancer was from our research
practice at home daily for 45 min, 6 days per week. group, in which we randomized 89 patients with a
Instructors are highly trained in meditation, group variety of cancer diagnoses to MBCR or a waitlist
process, and didactic instruction. control condition.19 Patients in the MBCR program

Ann. N.Y. Acad. Sci. xxxx (2016) 1–8 


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Mindfulness and cancer Carlson

improved significantly more on mood states and Recent trials


symptoms of stress than those in the control
More recently, we conducted two comparative effec-
condition, with large improvements of approxi-
tiveness RCTs of the MBCR program, the MINDSET
mately 65% on mood and 35% on stress symptoms.
and I-CAN Sleep trials, and developed an online
These patients, as well as the control group, were
adaptation of the program tested in the eCALM
followed up 6 months after treatment completion,
trial, each of which is described below.
and similar benefits were maintained over the
The MINDSET trial directly compared MBCR
follow-up period.20 In the combined group the
to another active group intervention for cancer
greatest improvements were seen on anxiety,
support in over 270 distressed breast cancer
depression, and irritability.
patients, supportive–expressive therapy (SET),27
Since that time, many pre–post observa-
and a minimal-intervention control condition (a
tional studies without comparison groups, quasi-
1-day stress management seminar). This trial was
experimental studies, and RCTs with usual-care or
unique in a number of ways: (1) we included only
waitlist control groups have been published, cit-
distressed breast cancer survivors, in order to avoid
ing improvements in a range of outcomes, includ-
floor or ceiling effects on outcomes wherein par-
ing quality of life (QOL) domains, such as emo-
ticipants do not improve because they are already
tional, social, role and physical functioning, and
doing quite well; (2) outcomes were both psycho-
psychological improvements on measures includ-
logical and biological; (3) psychological outcomes
ing stress symptoms, anxiety, depression, fear, and
included measures of both symptom reduction
avoidance (for reviews, see Refs. 5–18). Other out-
(mood disturbance, anxiety, stress symptoms),
comes assessed include cancer-related symptoms,
as well as enhancement of positive psychological
such as fatigue, pain, and sleep, and existential pos-
constructs (posttraumatic growth, spirituality);
itive psychology outcomes, including spirituality,
(4) we included a third group who participated
posttraumatic growth, loss, and grief.14
in only a 1-day stress management seminar, as a
While some RCTs comparing MBIs to waitlist or
minimal-intervention control, who after the active
usual-care controls have large sample sizes,21–25 still
intervention period were re-randomized into one
only a few studies have included randomized active
of the two longer interventions; (5) we followed
comparison groups. Henderson et al.26 randomized
all participants for a full year post-program to
172 early-stage breast cancer patients into an 8-week
determine long-term outcomes; and (6) the study
MBSR program, a nutrition education program
included moderator analyses to determine if
matched on time, or a usual-care control condition,
outcomes differed across groups for people with
and included follow-up assessments post-program,
different baseline characteristics, personalities, and
1 and 2 years later. The MBSR group improved more
preferences.
than the other two groups on many measures post-
Overall, women in the MBCR group showed
program, including QOL, active behavioral and
more improvement on stress symptoms compared
cognitive coping, and avoidance and spirituality, as
with women in both the SET and control groups, on
well as depression, hostility, anxiety, unhappiness,
QOL compared with the control group, and in social
meaningfulness, and several measures of emotional
support compared with the SET group,28 but both
control. These group differences eroded over time,
active-intervention groups’ cortisol slopes (a marker
however, as participants in the other two groups
of stress responding) were maintained over time
continued to improve more slowly: by 24 months the
relative to the control group, whose cortisol slopes
only group differences were on measures of anxiety,
became flatter. Steeper slopes are generally consid-
unhappiness, and emotional control, still favoring
ered to be healthier. The two intervention groups
MBSR over usual care, but not over the educational
also maintained their telomere length, a potentially
group. It seems that MBSR may have helped to speed
important marker of cell aging, over time compared
up the natural course of cancer recovery across
to controls.29 Over the longer-term follow-up of
many domains, but also added a more lasting and
1 year, the MBCR participants maintained all of
distinct shift in perspective and skills in emotion
the benefits received in the group, while the SET
regulation.
participants still had higher levels of stress, mood

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Carlson Mindfulness and cancer

disturbance, and lower QOL.30 This suggests that sleep onset were observed for both groups. Total
the 8-week group provided longer-term protection sleep time increased by 0.6 h for CBT-I and 0.75 h for
from distress for these women compared to those MBCR. CBT-I improved sleep quality and dysfunc-
who did not participate. tional sleep beliefs, and both programs resulted in
The most preferred treatment (by over half of reduced stress and mood disturbance. The percent-
participants) was MBCR, and those who received age of patients reporting severe insomnia dropped
their preferred treatment (regardless of what it was) to 0% in both groups, while moderate insomnia in
improved more on QOL and spirituality over time.31 the MBCR group dropped from 41% at baseline to
Preference seemed to be a more powerful predic- 19% post-program and continued to drop to 15% at
tor of outcome than individual personality traits. follow-up, whereas moderate insomnia in the CBT-I
Indeed, while we measured baseline levels of neu- group dropped from 50% to 10% post-program,
roticism, extraversion, conscientiousness, openness but then increased to 17% at follow-up. Rates of
to experience, and agreeableness (the “big 5” per- mild insomnia increased in both groups, as peo-
sonality traits), as well as emotional suppression ple shifted from the moderate and severe categories
and repression, contrary to our original hypothe- when they improved. At the follow-up assessment,
ses, none of these traits had significant effects on 22% of patients in MBCR and 50% of patients in
most outcomes. This begins to indicate something CBT-I no longer had clinically significant insomnia
beyond what can be learned from classic RCT in any range; however, these categorical differences
designs—preference matters more than individual between groups were not statistically significant.34
differences in personality or coping styles. Treat- Overall, these findings indicated that while MBCR
ment credibility and expectancy for benefit are likely was slower to take effect, it could be as effective as
important components in harnessing the power of the gold-standard treatment for insomnia in cancer
the individual to produce meaningful change. survivors over time.
In another head-to-head comparative effective- One final example of stretching the boundaries
ness trial (I-CAN Sleep), we also tried something of traditional service delivery is a study by our
relatively novel for behavioral interventions— research group of an online adaptation of MBCR,35
blinding participants to treatment. We did this which included a broad range of both men and
by advertising the study simply as “I-CAN Sleep: women who could either be on active treatment or
non-drug treatments for insomnia in cancer have completed treatment within the past 3 years,
survivors,” and did not tell participants what the with any type of cancer. They all were experiencing
treatments were until they were already enrolled. at least moderate levels of distress. Because it was
Even then, they only knew about the treatment that offered to people living in rural and remote areas
they received, not what the other treatment was.32 and who otherwise didn’t have access to face-to-
They were randomly assigned to either MBCR or face MBCR groups, we couldn’t directly compare
cognitive behavioral therapy for insomnia (CBT-I), in-person to online versions. Instead, we conducted
the gold-standard treatment for insomnia. This is a waitlist RCT comparing those in the online pro-
a very tough test of efficacy for MBCR and was gram to a group randomly assigned to wait for the
designed as a non-inferiority trial to test whether next online program. Our primary interest was fea-
the novel treatment for sleep (MBCR) was as sibility: whether people would sign up, complete the
effective as the gold standard. program, and receive much benefit. The program
In total, 111 patients with a variety of cancer types was offered through a website called emindful.com,
were randomly assigned to either an 8-week CBT- which already offered online MBSR and had a plat-
I program (n = 47) or the 8-week MBCR group form where people used webcams and microphones
(n = 64).33 Immediately post-program, MBCR was to connect to live online groups. The participants
found to be inferior to CBT-I in improving the attended each week for 8 weeks at a set time, as in a
primary outcome of insomnia severity, but MBCR face-to-face group, and could see and interact with
was noninferior at follow-up 3 months later. The the instructor and the other participants in the
time to fall asleep was reduced by 22 min in the online classroom. We enrolled 62 people, 83% of
CBT-I group and by 14 min in the MBCR group whom completed the program, which is a similar
at follow-up. Similar reductions in wake time after completion rate as for in-person programs. All

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Mindfulness and cancer Carlson

participants said the program either met (40%) or minimal. Currently, we have yet to investigate the
exceeded (60%) their expectations, and all said they feasibility of this approach and whether outcomes
would recommend the program to other cancer would be similar in type and magnitude. I sug-
patients. There were significant improvements gest caution in adapting MBIs to self-study pro-
and medium effect sizes in the online MBCR grams without first rigorously evaluating outcomes,
group, relative to controls, for scores of total mood knowing from clinical experience the value of both
disturbance, stress symptoms, and spirituality,36 group interaction and facilitator expertise and sup-
again of similar magnitude to in-person groups. port. Whether participants can benefit similarly on
their own with minimal interaction or support is
Future directions
an empirical question but one of significant interest
Following the eCALM trial, our next steps to fur- because of the potential to reach so many more peo-
ther enhance the reach of these interventions are ple. However, proceeding carefully and thoughtfully
to develop and test home-study self-managed ver- is necessary to avoid diluting or adapting interven-
sions of the online intervention. The idea is to tions to the point where harm is possible or benefit
record online sessions and allow participants to fol- is minimal.
low along at their own pace, still doing the daily One final study that has recently been funded,
home practice, with an opportunity for questions and will be conducted in Calgary and Toronto
and answers in a nonsynchronous format from an from 2016 to 2021, is a preference-based compar-
instructor. This would improve the scalability and ative effectiveness trial comparing MBCR to Tai
sustainability of such programs as costs would be Chi/Qigong in cancer survivors. It is a four-arm

Figure 1. Preference-based trial design. Depicted is a standard pragmatic preference-based clinical trial. Participants with a
preference are assigned to either treatment 1-P or 2-P, whichever they prefer. Without a preference, they are randomized to either
1-R or 2-R. The comparison of 1-P versus 2-P looks at real-world comparative effectiveness of interventions (Box A). 1R versus 2R
is a standard RCT assessing efficacy (Box B). 1-P versus 1-R looks at the same treatment but compares those who preferred it to
those without a preference; hence, isolating the effect of preference on outcome in intervention 1 (Box C). The same is done for
intervention 2 (Box D). Finally the combination of all participants in each intervention can be summed and the two interventions
compared with greater power to allow correlational and subgroup analyses (Box E).

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Carlson Mindfulness and cancer

trial in which distressed participants with a pref- widespread dissemination of these approaches,
erence receive the intervention of their preference with the potential to benefit many more people, but
in a pragmatic design, while those without any I also behoove those who promote and study such
preference are randomized to one or the other approaches to proceed carefully and document
intervention, in the manner of a traditional RCT outcomes including both benefits and potential
(see Fig. 1 for trial design). Outcomes include psy- limitations.
chological self-reported measures and symptoms,
Acknowledgments
as well as a range of biomarkers, including cytokine
production, telomere length, salivary cortisol, gene Dr. Linda E. Carlson holds the Enbridge Research
expression, and blood pressure, as well as health Chair in Psychosocial Oncology, co-funded by the
economic outcomes. Using this design, we can Alberta Cancer Foundation and the Canadian Can-
isolate the effect of each intervention in the RCT cer Society Alberta/North West Territories Division.
portion and begin to understand the nuances of She is also an Alberta Innovates–Health Solutions
how each intervention affects specific symptoms Health Scholar. Research discussed in this paper was
and outcomes, and also see the impact of preference funded by the Canadian Breast Cancer Research
and expectancy on outcomes in a real-world Alliance, Canadian Cancer Society Research Insti-
scenario. This design has similar advantages to tute, Mind and Life Institute (Varela Award), and
the MINDSET study, but with the addition of the the John and Lotte Hecht Foundation.
ability to isolate the effects of preference.
Other pressing research questions revolve around Conflicts of interest
potential mechanisms of action, which is currently The author declares no conflicts of interest.
an active area of study and debate. The role of
home practice, including how much is necessary
and whether dose–response relationships with out- References
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C 2016 New York Academy of Sciences.

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