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December 2014, Supplement to Volume 18, Number
6
Article
Evidence-Based Interventions for Cancer- and Treatment-Related
Cognitive Impairment
Diane Von Ah, PhD, RN, FAAN,
Catherine E. Jansen, PhD, RN, CNS, AOCNS®, and Deborah H. Allen,
PhD, RN, CNS, FNP-BC, AOCNP®
Cancer- and cancer treatment–related cognitive impairment is a common,
bothersome, and potentially debilitating symptom incurred by cancer survivors.
Cognitive impairment has a significant impact on patients’ day-to-day
functioning and quality of life, but it remains under-recognized and
undertreated. This article, which is an update from the initial Oncology Nursing
Society Putting Evidence Into Practice for cancer- and
cancer treatment–related cognitive impairment, provides a comprehensive
critical review and summary of the evidence regarding interventions addressing
cognitive impairment for cancer survivors. This article examines the
effectiveness of interventions focused on cancer- and cancer treatment–related
cognitive impairment, makes recommendations for practice, and identifies gaps
in knowledge and areas for further research.
Cancer- and cancer treatment–related cognitive
impairment is a national research priority (LoBiondo-Wood et al., 2014). As many as 75% of U.S. cancer survivors have reported issues with
memory, attention, or feelings of mental slowness (Janelsins
et al., 2011). Cognitive deficits in memory, attention, processing
speed, and executive functioning have been documented on neuropsychological
examination (Falleti, Sanfilippo,
Maruff, Weih, &
Phillips, 2005; Jansen, Miaskowski, Dodd, Dowling,
& Kramer, 2005; Stewart, Bielajew, Collins,
Parkinson, & Tomiak, 2006) and functional
magnetic resonance imaging (Holohan, Von Ah,
McDonald, & Saykin, 2013).
Cognitive impairment is a complex problem that has
been associated with other symptoms (e.g., depression, anxiety, fatigue)
(Bender & Thelen, 2013), poorer quality of life (Mehnert et al., 2007; Myers, 2013; Von Ah, Russell, Storniolo, & Carpenter, 2009), and poorer perceived
work ability (Calvio, Peugeot, Bruns,
Todd, & Feuerstein, 2010; Feuerstein, Hansen, Calvio,
Johnson, & Ronquillo, 2007; Munir,
Burrows, Yarker, Kalawsky,
& Bains, 2010). Although cognitive impairment has
a significant impact on cancer survivors, it remains under-recognized and
undertreated (Vardy, Wefel, Ahles,
Tannock, & Schagen,
2008; Von Ah, Jansen, Allen, Schiavone, & Wulff, 2011). As a result, through the Oncology Nursing
Society (ONS) Putting Evidence Into Practice (PEP®) initiative, a
team of dedicated advanced practice nurses, nurse scientists, and ONS staff
have sought to improve patient outcomes by critically examining, synthesizing,
and evaluating interventional literature on the treatment and management of
cognitive impairment in cancer survivors. This article describes the current
evidence for interventions to treat and manage cognitive impairment following
cancer and its treatment.
Methods
An extensive review of the literature regarding
cognitive impairment was conducted. Search terms, limits, and databases are
described in Figure 1. Research studies included in
this supplement were retrieved since the initial ONS cognitive impairment PEP
review from August 2010 to February 2014. Cognitive impairment was defined as a
decline in function in one or more cognitive function domains, including
attention and concentration, executive function, information-processing speed, language,
visual-spatial skill, psychomotor ability, learning, and memory (Jansen, 2010).
Studies were excluded if they were descriptive only, involved pediatric or
adolescent patients with cancer, or evaluated long-term cognitive impairment
after a childhood or adolescent cancer or cancer-related treatment.
A systematic approach to reviewing, critiquing, and
assigning the level of evidence of the literature was used, as previously
reported (Von Ah et al., 2011). Briefly, each article was reviewed by two content
experts using a standardized worksheet, assigned an appropriate interventional
category, and added to the respective evidence tables. To determine the level
of evidence, the team examined the collective strength of each identified
intervention and recommended the level of evidence using the ONS PEP
weight-of-evidence classification schema (Mitchell & Friese,
2014).
Evidence
Twenty-four studies met inclusion criteria and were
added to the level of evidence for each interventional strategy, resulting in
51 empirical studies, one literature review, and one meta-analysis. Although
the number of interventional studies has almost doubled since the original
review (Von Ah et al., 2011), the research is still limited by small studies
with inconsistent findings and often lacking objective evaluations of
cognition. The following section provides the literature synthesis under the
classification of effectiveness schema categories. Figure
2 depicts a comprehensive list of empirical research by level of evidence
and intervention category.
Likely
to Be Effective
Cognitive training has been deemed as likely to be
effective in addressing cognitive impairment in cancer survivors. Cognitive
training programs have been defined as “any intervention aimed at improving,
maintaining or restoring mental function through the repeated and structured
practice of tasks which pose an inherent problem or mental challenge” (Sitzer, Twamley, & Jeste, 2006, p. 75). Seven trials provided cognitive
training; three delivered training in a group format (Hassler
et al., 2010; Poppelreuter, Weis, & Bartsch, 2009; Von Ah et al., 2012), and four provided
individualized training programs (Gehring et al.,
2009; Kesler et al., 2013; Miotto
et al., 2013; Zucchella et al., 2013). The studies targeted
two patient populations: patients with primary brain tumors and breast cancer
survivors. Sample sizes ranged from 11–140 participants, and all but one
study employed a randomized, controlled trial study design (Hassler
et al., 2010). These programs provided remediation to improve attention and
memory performance (Gehring et al., 2009; Hassler et al., 2010; Miotto et
al., 2013; Poppelreuter et al., 2009; Von Ah et al.,
2012; Zucchella et al., 2013), speed of processing
(Von Ah et al., 2012), and/or executive functioning (Gehring
et al., 2009; Kesler et al., 2013). Of note, six
studies demonstrated statistically significant improvement in cognitive
functioning on neuropsychological tests with effects that typically were
cognitive domain specific (e.g., training in memory resulted in improved memory
performance). For example, Von Ah et al. (2012) noted that memory training
improved memory performance (p = 0.036, d = 0.59) and speed-of-processing
training improved processing speed (p = 0.016, d = 0.67) at a two-month
follow-up assessment for breast cancer survivors. Similarly, Miotto et al. (2013) noted significant improvement in
verbal memory recall on neuropsychological examination in 21 adult patients
with postacute prefrontal cortex lesions. Conversely,
Poppelreuter et al. (2009) failed to demonstrate
significant improvement in 96 breast cancer survivors in an inpatient
rehabilitation center who were divided into two intervention groups receiving
attention and memory training. However, Poppelreuter
et al. (2009) noted improvement in cognitive
functioning in all groups and suggested that improvement may have been caused
by unspecified effects of inpatient rehabilitation and/or the timing of the
intervention coinciding with the completion of treatment and expected gains by
all participants. Overall, the evidence indicates that cognitive training is
likely to be effective in improving cognitive performance in cancer survivors,
and this finding is supported by a large volume of research in healthy
middle-aged and older adults (Ball, Edwards, & Ross, 2007; Ball et al.,
2002; Wolinsky et al., 2006; Wolinsky,
Vander Weg, Howren, Jones,
& Dotson, 2013).
Effectiveness
Not Established
Cognitive-behavioral training (CBT) has been used in
nine studies to address cognitive function in cancer survivors (Cherrier et al., 2013; Ferguson et al., 2007, 2012; Goedendorp, Knoop, Gielissen, Verhagen, & Bleijenberg, 2014; Locke et al., 2008; McDougall, 2001;
McDougall, Becker, Acee, Vaughan, & Delville, 2011; Schuurs &
Green, 2013; Sherer, Meyers, & Bergloff, 1997). Generally, CBT programs are designed to
change a person’s beliefs, expectations, appraisals, and attributions. In the
studies reviewed, researchers focused on enhancing self-efficacy (McDougall,
2001; McDougall et al., 2011), self-regulation, and self-awareness (Ferguson et
al., 2007, 2012), and provided psychoeducation (Schuurs & Green, 2013), education and counseling about
cognitive concerns (Sherer et al., 1997) and reducing
fatigue (Goedendorp et al., 2014), as well as
compensatory strategies for memory, attention (Cherrier
et al., 2013; Ferguson et al., 2007, 2012; McDougall, 2001; McDougall et al.,
2011), and problem solving (Locke et al., 2008). Most of the programs were
delivered using a group format and included mixed samples of cancer survivors,
but two focused on breast cancer survivors and two on patients with primary
brain tumors. Five studies used random assignment in their design (Cherrier et al., 2013; Ferguson et al., 2007, 2012; Goedendorp et al., 2014; Locke et al., 2008), and six
studies had small sample sizes of less than 30 participants (Cherrier et al., 2013; Ferguson et al., 2007; Locke et al.,
2008; McDougall, 2001; McDougall et al., 2011; Sherer
et al., 1997). Significant improvement in objectively measured cognitive
function was noted in only four studies (Ferguson et al., 2007, 2012;
McDougall, 2001; Schuurs & Green, 2013); two of
the studies did not control for practice effects in their intervention design,
which may have accounted for some of the improvement (Ferguson et al., 2007;
McDougall, 2001). In addition, one study did not randomly assign participants,
which may have introduced bias (Schuurs & Green,
2013). All of the CBT trials noted improvement in perceived functioning
(increased productivity, improved memory self-efficacy, less cognitive
disability or complaints). Although some improvements were noted in cognitive
function across the studies, the work varied in design, content, and duration, and most were limited by small sample sizes or
lack of a comparison group to establish effectiveness.
Electroencephalography biofeedback or neurofeedback involves real-time display of brain
electrical activity provided to the individual as visual or auditory
information. This method was investigated in a small study by Alvarez, Meyer, Granoff, and Lundy (2013) with 23 breast cancer survivors,
and improvements were noted in perceived cognitive function. However, objective
cognitive performance was not assessed, and further investigation to establish
efficacy is needed.
Exercise has been defined as physical activity that
is planned or structured and involves repetitive bodily movement to improve or
maintain cardiorespiratory endurance, muscular strength, muscular endurance,
flexibility, and/or body composition (Centers for Disease Contol
and Prevention, 2011). Four studies were conducted using some form of exercise:
tai chi (Reid-Arndt, Matsuda, & Cox, 2012), resistance training (60-minute
sessions twice weekly for 12 weeks) (Baumann et al., 2011), physical fitness
program combined with psychosocial education (Korstjens,
Mesters, van der Peet, Gijsen, & van den Borne, 2006), and aerobic exercise
(15-minute sessions four days per week) combined with methylphenidate
(Schwartz, Thompson, & Masood, 2002). Three of
the studies were limited by pre- and postintervention
designs, and only one study used a historic nonintervention comparison group
(Schwartz et al., 2002). Although some improvements were reported in perceived
cognitive function, the difference in the type of exercise intervention
programs, small sample sizes, and study designs (combined multiple
interventions) make determining the effect of an exercise intervention on
cognitive impairment difficult.
Meditation has not demonstrated efficacy in addressing
postcancer cognitive impairment. Tibetan sound
meditation, which includes breathing awareness, concentration techniques, and
visualization and sound exercises, was piloted in a randomized, controlled
trial with 47 breast cancer survivors (Milbury et
al., 2013). Although improvement was noted in verbal memory, short-term memory,
speed of processing, and subjective cognitive function, these results were not
statistically significant, and further research is warranted.
Mindfulness-based stress reduction focuses on
bringing attention and awareness to each moment in a nonjudgmental way. In a
randomized, controlled trial with 229 breast cancer survivors, Hoffman et al.
(2012) evaluated an eight-week program. They were primarily interested in
effects on mood but noted some improvement on the confusion subscale of the
Profile of Mood States. Further research, including objective cognitive
performance outcomes, is needed to establish efficacy on mindfulness-based
stress reduction in cancer survivors.
Natural restorative environment interventions, based
on the attention-restoring theory, indicate that the environment may influence
one’s ability to concentrate and capacity to direct attention (Cimprich & Ronis, 2003). Two
small studies evaluated the impact of natural restorative environmental
intervention on cognitive function in patients with breast cancer (Cimprich, 1993; Cimprich & Ronis, 2003). One study used a pre- and postintervention
design and the other used a randomized, controlled trial. Both studies noted
improvements in the capacity to direct attention for patients prior to adjuvant
therapy. Further research is needed to explore its effect on cognitive function
after cancer treatment.
Qigong incorporates the practice of coordinated
gentle exercise and relaxation through meditation and breathing. One study
examined the effects of a 10-week medical qigong program in 81 patients with
cancer (Oh et al., 2012). Although the researchers found significant
improvement in perceived cognitive function, further testing using objective
cognitive function tests is warranted to determine efficacy.
Structured rehabilitation was not found to be
effective in one trial. A total of 394 breast, prostate, and colon cancer
survivors were randomly assigned to a six-day residential psychosocial
rehabilitation program that included education, supportive discussions,
physical activity, relaxation, massage, social activities, and dietary
counseling or to a control group (Rottmann et al., 2012). Objective cognitive performance was
not assessed and perceived cognitive function (a one-item measure)
significantly improved in the control group when compared to those in the
structured rehabilitation intervention group.
Vitamin E, or alpha-tocopherol,
is a fat-soluble antioxidant and has been proposed to prevent the production of
reactive oxygen (Ahles & Saykin,
2007). Two studies examined the effect of vitamin E on cognitive function
(Chan, Cheung, Law, & Chan, 2004; Jatoi et al.,
2005). Chan et al. (2004) demonstrated improvements in domains of executive
function, verbal memory, and visual memory for patients who received 1,000 IU
of vitamin E twice daily for one year. However, Jatoi
et al. (2005) closed their randomized, double-blind placebo controlled study
early because of poor accrual and thus failed to demonstrate a significant
effect of vitamin E on cognitive impairment. In addition, two meta-analyses
suggest that vitamin E doses of 400 IU per day or more are associated with
a higher mortality risk (Bjelakovic, Nikolova, Gluud, Simonetti, & Gluud, 2007;
Miller et al., 2005). Further research is needed to establish effectiveness of
vitamin E (Bjelokovic et al., 2007); however, high
doses of vitamin E (400 IU per day or greater) should be avoided (Miller et
al., 2005).
Dexmethylphenidate and
methylphenidate are stimulants commonly used in the treatment of attention
deficit hyperactivity disorder for children. Nine empirical studies (Bruera, Miller, Macmillan, & Kuehn, 1992; Butler et
al., 2007; Escalante et al., 2014; Gagnon, Low, & Schreier,
2005; Gehring et al., 2012; Lower et al., 2009; Mar
Fan et al., 2008; Meyers, Weitzner, Valentine, &
Levin, 1998; Schwartz et al., 2002), one literature review that focused on
methylphenidate in palliative care (Stone & Minton, 2011), and one
meta-analysis that included two empirical studies (Gong et al., 2014) have been
conducted with equivocal results as to whether the stimulants improve cognitive
impairment in cancer survivors. Three studies examined the use of
methylphenidate in patients with advanced cancer and demonstrated improvement
in subjective reports of alertness and objective measures of attention, memory,
executive functioning, and psychomotor function; however, only one (Bruera et al., 1992) of the studies was a randomized, controlled
trial, and all had small sample sizes ranging from 14–30 (Gagnon et al., 2005;
Meyers et al., 1998). In addition, as part of a comprehensive literature review
to address central side effects of opioid use, the European Palliative Care
Research found that evidence is limited regarding the use of methylphenidate to
counteract sedation or cognitive dysfunction (Stone & Minton, 2011).
Similarly, trials among other cancer survivors did not demonstrate any
improvement in cognitive function (Butler et al., 2007; Lower et al., 2009; Mar
Fan et al., 2008), reported mixed results (Escalante et al., 2014; Gehring et al., 2012), or noted that results were
confounded by the receipt of other interventions (e.g., exercise) (Schwartz et
al., 2002). Overall, studies evaluating the impact of the stimulants on
cognitive function in cancer survivors produced mixed results and were
significantly limited by small sample sizes, failure to recruit participants,
and high attrition rates.
Memantine, an
N-methyl-D-aspartate receptor antagonist, has been shown to have a neuroprotective effect in preclinical models and has been
effective in treating patients with vascular disease (Orgogozo,
Rigaud, Stöffler, Möbius, & Forette, 2002; Wilcock, Mobius, Stoffler, &
MMM 500 Group, 2002). Memantine was used in one
randomized, double-blind, placebo-controlled trial to address radiation-induced
injury in 508 patients receiving whole brain radiation therapy (Brown et al.,
2013). Although patients in the memantine arm
demonstrated longer time to clinical decline and reduced rates of decline in
memory, executive function, and processing speed, the study failed to find a
significant difference in delayed recall, which was its primary endpoint. Brown
et al. (2013) suggested that they were underpowered to see a significant effect
because only 149 participants remained in the study at 24 weeks. More research
is needed to determine the effectiveness of memantine
for cognitive impairment in patients with cancer.
Modafinil, a psychostimulant used in the treatment of patients with
narcolepsy, has been used in four small trials among cancer survivors with
equivocal results (Blackhall, Petroni, Shu, Baum, & Farace, 2009; Gehring et al.,
2012; Kohli et al., 2009; Lundorff,
Jonsson, & Sjogren,
2009). Lundorff et al. (2009) noted improvements in
attention and psychomotor speed but not in the working memories of 28 patients
with advanced cancer. Similarly, Kohli et al. (2009)
reported improvement in speed of memory and episodic memory but not in working
memory in 68 breast cancer survivors. In contrast, Blackhall
et al. (2009) noted improvement in cognitive flexibility but failed to find
significant improvement in cognitive performance on neuropsychological
examination with escalating doses of modafinil (100–200
mg) among 27 patients with all stages of cancer. Most recently, Gehring et al. (2012) noted as much as a 50% improvement on
a test of executive functioning, which required divided attention in 24
patients with a primary brain tumor; however, no placebo control group was used
in the study, raising concerns of practice effects. Conflicting results may be
related to the varying study methodologies employed in the studies: variations
of the dose and duration of modafinil, population of
the patients examined, small sample sizes, and lack of control groups. Thus,
the effectiveness of modafinil is difficult to
determine without further research.
Donepezil, an acetylcholinesterase
inhibitor that is used to treat mild to moderate Alzheimer dementia, has been
used with mixed results in two small trials (Jatoi et
al., 2005; Shaw et al., 2006). Shaw et al. (2006) administered 5–10 mg per day
of donepezil and noted significant improvement in attention, concentration, and
verbal and figural memory in 35 patients with a brain tumor. Jatoi et al. (2005) attempted to evaluate the effect of
donepezil 5 mg daily in combination with vitamin E 1,000 IU daily on cognition
in patients with lung cancer, but no conclusions regarding efficacy could be
determined because the study closed early as a result of poor accrual.
Therefore, further clinical testing is warranted to establish the effectiveness
of donepezil in cancer survivors.
Effectiveness
Unlikely
Gingko biloba, an
antioxidant believed to possess neuroprotective effects
(Nada & Shah, 2012; Smith & Luo, 2004),
failed to demonstrate effectiveness in two randomized, controlled trials (Attia et al., 2012; Barton et al., 2013). Barton et al.
(2013) investigated 120 mg per day of gingko biloba
to prevent cognitive decline in 210 women with breast cancer receiving adjuvant
chemotherapy and did not find therapeutic benefit. Similarly, in a smaller
trial, Attia et al. (2012) found no therapeutic
benefit in 34 patients with an irradiated brain.
Not
Recommended for Practice
Erythropoiesis-stimulating agents are not
recommended for practice to address cognitive impairment following cancer and
cancer treatment. Erythropoietin-stimulating agents, which stimulate the
production of red blood cells in the bone marrow, have been evaluated in seven
studies addressing anemia, a potential underlying mechanism of cancer- and
cancer treatment–related cognitive impairment (Chang, Couture, Young, Lau,
& McWatters, 2004; Iconomou
et al., 2008; Mancuso, Migliorino, De Santis, Saponiero, & De Marinis, 2006; Mar Fan et al., 2009; Massa, Madeddu, Lusso, Gramignano, & Mantovani,
2006; O’Shaughnessy, 2002; O’Shaughnessy et al., 2005). Although conclusions
from the studies were inconsistent and ranged from no therapeutic benefit (Iconomou et al., 2008; Mancuso et al., 2006; Mar Fan et
al., 2009; O’Shaughnessy, 2002; O’Shaughnessy et al., 2005) to significant
improvements in cognitive functioning (Chang et al., 2004; Massa et al., 2006),
the U.S. Food and Drug Administration (2011) issued a black box warning
regarding the increased risk of serious cardiovascular and thrombovascular
events and their potential to shorten overall survival in patients with cancer.
As a result, the use of erythropoietin-stimulating agents is not recommended to
address cognitive impairment in cancer survivors.
Implications for Nursing and Conclusion
Oncology nurses may play an integral role in
identifying cancer survivors with clinically significant cognitive impairment.
Nurses need to listen carefully to their patients and recognize common
descriptions (e.g., expressions of difficulty concentrating, trouble following
directions, memory lapses, decreased awareness, inability to plan or problem
solve) as potential indicators of clinically
significant cognitive impairment (Jansen, 2013). Nurses should use readily
available and reputable resources such as ONS (2014), the American Society of
Clinical Oncology (2013), or Livestrong Foundation
(2014) to provide support to survivors with cognitive concerns. In addition, after careful assessment to address and eliminate
other correlated symptoms (Bender & Thelen,
2013), nurses may need to refer survivors with significant cognitive impairment
that affects everyday functioning to a specialist for
a comprehensive neuropsychological evaluation (Jansen, 2013).
With regard to evidence-based interventions, this
review demonstrated that cognitive training provided in a group or individual
format seems to provide the most improvement in cognitive function for cancer
survivors. Although other interventions, such as CBT, exercise, and mediation
or mindfulness-based stress reduction, may be beneficial to improve cognitive
function, empirical data are limited in their support of these approaches in
cancer survivors. Gingko biloba was not found to be
effective in a large randomized trial and, therefore, is unlikely to have a
positive impact to prevent or treat cognitive impairment after cancer. Nurses
also should warn their patients that erythropoietin is not recommended for
practice to address cognitive impairment.
Future research is needed and must explore the
underlying physiologic mechanisms associated with cognitive impairment and
potential genetic polymorphisms that may predispose patients to cognitive
impairment after cancer and its treatment. To date, most of the cognitive
intervention research has been primarily explored in small samples of patients
with brain tumors and breast cancer survivors. Large randomized, controlled
trials in multiple centers accessing a diverse population of cancer survivors,
including survivors with various types of cancer, of various ages, and from
differing ethnicities, are warranted to further test the effectiveness of the
pharmacologic and nonpharmacologic interventions for
cancer- and cancer treatment–related cognitive impairment.
Implications for Practice
Ø
Incorporate the evaluation of cognitive
concerns in nursing assessment, acknowledging any issues reported and educating
patients and their families about the possibility of cancer- and cancer
treatment–related cognitive impairment.
Ø
Acknowledge patient reports of cognitive
concerns and collaborate with the multidisciplinary team to provide referral
for neuropsychological testing if warranted.
Ø
Discuss use of cognitive training exercises as
an intervention likely to be effective in improving cancer- and cancer
treatment–related cognitive impairment.
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Diane
Von Ah, PhD, RN, FAAN, is an associate professor and a Robert Wood Johnson
Foundation Nurse Faculty Scholar Alumna in the School of Nursing at Indiana
University in Indianapolis; Catherine E. Jansen, PhD, RN, CNS, AOCNS®, is an oncology clinical
nurse specialist at Kaiser Permanente Medical Center in San Francisco, CA; and
Deborah H. Allen, PhD, RN, CNS, FNP-BC, AOCNP®, is an advanced practice nurse at Duke Cancer
Institute in Durham, NC. The authors take full responsibility for the content
of the article. The authors did not receive honoraria for this work. The
content of this article has been reviewed by independent peer reviewers to
ensure that it is balanced, objective, and free from commercial bias. No
financial relationships relevant to the content of this article have been
disclosed by the authors, planners, independent peer reviewers, or editorial
staff. Von Ah can be reached at dvonah@iu.edu,
with copy to editor at CJONEditor@ons.org.
(Submitted May 2014. Revision submitted July 2014. Accepted for publication July 11, 2014.)
Key words: cognitive impairment; intervention;
evidence-based practice
http://dx.doi.org/10.1188/14.CJON.S3.17-25