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Journal of Motor Behavior

ISSN: 0022-2895 (Print) 1940-1027 (Online) Journal homepage: http://www.tandfonline.com/loi/vjmb20

Exercise Training for Persons with Alzheimer's


Disease and Caregivers: A Review of Dyadic
Exercise Interventions

Guillaume Lamotte, Raj C. Shah, Orly Lazarov & Daniel M. Corcos

To cite this article: Guillaume Lamotte, Raj C. Shah, Orly Lazarov & Daniel M. Corcos (2016):
Exercise Training for Persons with Alzheimer's Disease and Caregivers: A Review of Dyadic
Exercise Interventions, Journal of Motor Behavior, DOI: 10.1080/00222895.2016.1241739

To link to this article: http://dx.doi.org/10.1080/00222895.2016.1241739

Published online: 21 Nov 2016.

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Download by: [University Of South Australia Library] Date: 24 November 2016, At: 01:28
Journal of Motor Behavior, Vol. 0, No. 0, 2016
Copyright Taylor & Francis Group, LLC

RESEARCH ARTICLE
Exercise Training for Persons with Alzheimers Disease and
Caregivers: A Review of Dyadic Exercise Interventions
Guillaume Lamotte1, Raj C. Shah2, Orly Lazarov3, Daniel M. Corcos4,5
1
Department of Neurology, MedStar Georgetown University Hospital, Washington, DC. 2Rush Alzheimers Disease Center,
Rush University, Chicago, Illinois. 3Department of Anatomy and Cell Biology, College of Medicine, The University of Illinois at
Chicago, Chicago, Illinois. 4Department of Physical Therapy and Human Movement Sciences, Feinberg School of Medicine,
Northwestern University, Chicago, Illinois. 5Department of Neurological Sciences, Rush University Medical Center, Chicago,
Illinois.

ABSTRACT. Alzheimers disease (AD) is the most common form There is no known cure for AD. Currently available
of dementia and the prevalence will increase dramatically in the medications offer, at best, symptomatic relief and are
next decades. Although exercise has shown benefits for people
with dementia due to AD as well as their caregivers, the impact of associated with potential side effects (Alzheimers Associa-
a dyadic exercise intervention including both groups as study par- tion, 2016). Therefore, alternative effective approaches are
ticipants remains to be determined. The authors review the current essential. Exercise training has been shown to be feasible
clinical evidence for dyadic exercise interventions, which are exer- for persons with dementia due to AD and their caregivers
cise regimens applied to both the person with dementia and the with potential benefits in cognitive and noncognitive
caregiver. A total of 4 controlled trials were reviewed. This review
shows that dyadic exercise interventions are feasible and may pro- outcomes for persons with dementia due to AD (Forbes,
duce a positive effect on functional independence and caregiver Forbes, Blake, Thiessen, & Forbes, 2015). It is important to
burden. However, there was insufficient evidence to support a bene- gauge the value of exercise for individuals with dementia
fit of dyadic exercise intervention on cognitive performance and on due to AD and their caregivers in studies that provide the
behavioral and neuropsychiatric symptoms in participants with exercise intervention to (a) persons with dementia due to
dementia due to AD. A dyadic exercise intervention improves func-
tional independence and caregiver burden. However, there is a need AD, (b) caregivers, and (c) both persons with AD and their
for well-designed randomized controlled clinical trials to confirm caregivers.
these benefits and to investigate several important points such as In this article, we review the current clinical evidence for
the effects of a dyadic exercise intervention on cognitive and non- dyadic exercise interventions including both the persons
cognitive outcomes of AD, the optimal intensity of exercise train- with dementia due to AD and their caregivers. For the
ing, and the cost effectiveness of such a program.
purpose of this review, a study was included if the care-
Keywords: Alzheimers disease, caregivers, clinical trial, exercise givers and the persons with dementia due to AD were
actively following the exercise protocol (individual with
dementia and caregivers exercising together or individu-

A lzheimers disease (AD) is the most common form of


dementia. The prevalence of AD in Americans of all
ages was estimated to be 5.4 million in 2016 and this num-
ally). We focus on four types of outcomes: cognitive perfor-
mance, neuropsychiatric and behavioral symptoms,
functional outcomes, and caregivers outcomes. We will
ber will increase dramatically in the next decades then discuss the current clinical evidence for exercise-
(Alzheimers Association, 2016). Individuals with AD pres- induced changes in individuals with dementia due to AD
ent with impaired short- and long-term memory as well as and their caregivers. Finally, we discuss the role of the care-
impairment of abstract thinking and judgment, disturbances givers in a dyadic intervention, the cost effectiveness of
of higher cortical function (e.g., aphasia, apraxia), changes such programs and the potential challenges associated with
in personality, and behavioral abnormalities. Both cognitive implementing an exercise trial with this dyad.
and noncognitive features of the disease impact the quality
of life of people living with AD as well as their caregivers
(Alzheimers Association, 2016). A caregiver is defined as Methods
an individual who provides support and care to a person liv-
ing with AD. Unpaid caregivers are usually immediate fam- Search Strategy
ily members and the number is estimated to be more than To identify controlled clinical trials using dyadic
15 million in the US (three caregivers per person with AD; exercise interventions, the following electronic databases
Alzheimers Association, 2016). They play a central role in were searched: PubMed (1990 to April 1, 2016), Cochrane
the management of AD and other dementias and the physi- Library (1990 to April 1, 2016), Embase (1990 to April 1,
cal and psychological effort required to provide ongoing 2016), and Google Scholar (1990 to April 1, 2016).
care grows as the patients cognitive impairment worsens.
Caregivers have been shown to be at increased risk of stress
Correspondence address: Guillaume Lamotte, Department of
and depression, experience sleep problems more often, and Neurology, MedStar Georgetown University Hospital, 3800
have poor physical health (Adelman, Tmanova, Delgado, Reservoir Road NW, Washington, DC, 20007, USA. e-mail:
Dion, & Lachs, 2014). guillaumelamotte14@gmail.com

1
G. Lamotte, R. C. Shah, O. Lazarov & D. M. Corcos

Searches were performed utilizing the following terms: Walking with progressively increasing intensity was used
exercise, dyad, Alzheimers disease, physical activity, in one study (Lowery et al., 2014), whereas a combination
caregiver, dementia. In addition, citation tracking was used of flexibility, strength, agility and balance exercises as well
to identify reference lists from included studies. as walking and dancing were used in another study
A study was included in the present review if it met the (Canonici et al., 2012). Three studies reported supervision
following criteria: (a) the target population was patients for the exercise intervention (Lowery et al., 2014; Pitkala et
with dementia due to AD according to international diag- al., 2013; Prick et al., 2015). Patients trained under direct
nostic criteria (if patients with other forms of dementia supervision of exercise physiologists for each exercise ses-
were studied, the proportion of patient with a clinical diag- sion in one study (Pitkala et al., 2013). In one study, exer-
nosis of dementia due to AD should be > 70% of the total cise training was supervised by an exercise trainer weekly
sample for a study to be included in the review); (b) exer- for the first four weeks and biweekly for the next eight
cise training was the intervention evaluated for both the weeks (Prick et al., 2015), whereas in another study the
individual with dementia and the caregiver; (c) the effects exercise therapist supervised the exercise program for
of treatment intervention were tested as the primary out- the first six weeks and the dyad was expected to perform
come; (d) the effects of exercise training were compared the exercise regimen regularly and independently at least
with control or comparison groups, including other forms five times per week for the next six weeks (Lowery et al.,
of physical activity or exercise; (e) the article was available 2014). Only one study reported the expected exercise inten-
in English; (f) the study was a controlled clinical trial sity (Lowery et al., 2014). All studies included in this
restricting the review to class I, II, and III studies according review examined the exercise-induced changes in individu-
to the classification of level of evidence of the American als with dementia in the on-medicated state.
Academy of Neurology (Gross & Johnston, 2009).
Participants
Results
A total of 484 dyads were included in the four studies
The search strategy led to four controlled trials reported in this review and 391 dyads completed their
investigating the effect of a dyadic exercise intervention allocated intervention protocol and were included in the
including both the persons with dementia due to AD and primary analysis. The number of screened patients was
the caregivers (Canonici et al., 2012; Lowery et al., 2014; reported in three studies (Lowery et al., 2014; Pitkala et al.,
Pitkala et al., 2013; Prick, de Lange, Twisk, & Pot, 2015). 2013; Prick et al., 2015). Prick et al. assessed 146 dyads for
We also included secondary analyses of the Pitkala et al. eligibility to randomize 111 dyads. Lowery et al. screened

study (Ohman et al., 2016). The main characteristics and 474 dyads to select 131 dyads for participation in the study.
results of each study are summarized in Table 1. 1,264 dyads received a letter from the Social Insurance
Institution of Finland offering the possibility to participate
in the exercise trial, and of these 390 were screened by
Intervention
phone to select 210 dyads in another study (Pitkala et al.,
All the studies evaluated a dyadic exercise intervention 2013). Regarding the inclusion criteria, two studies
against a no-exercise control group (usual care; Canonici et included only participants diagnosed with AD who fulfilled

al., 2012; Lowery et al., 2014; Ohman et al., 2016; Pitkala the criteria for probable dementia due to AD according to
et al., 2013; Prick et al., 2015). One study also compared the National Institute of Neurological and Communicative
two different types of intervention: customized home-based Disorders and Stroke and the Alzheimers Disease and
exercise and group-based exercise (Pitkala et al., 2013). In Related Disorders Association Alzheimers criteria
one study, the control group also received monthly informa- (Canonici et al., 2012; Pitkala et al., 2013). The two other
tion bulletins and monthly phone calls for the duration of studies included participants with a clinical diagnosis of
the study (Prick et al., 2015). Across all of the studies, the dementia made by a physician (Lowery et al. also used
interventions were clinically heterogeneous with regard to ICD-10 Diagnostic Criteria for Research to confirm the
the frequency and duration of exercise being undertaken diagnosis; Lowery et al., 2014; Prick et al., 2015). AD was
and duration of intervention: between 20 and 45 min of the clinical diagnosis for 124 of the 131 participants in one
exercise per session, between two and five times per week study (other n D 7 of 131; Lowery et al., 2014), whereas 78
for 312 months. The studies also were heterogeneous with of the 111 care receivers had a clinical diagnosis of demen-
regard to the exercise interventions: one study used a tia due to AD in the other study (vascular dementia n D 17
combination of aerobic (e.g., Nordic walking), strength, of 111, other n D 16 of 111; Prick et al., 2015). Studies
dual-task (e.g., talking while walking), and balance training were heterogeneous with respect to the severity of demen-
(Pitkala et al., 2013). One study used a combination of flex- tia. The Clinical Dementia Rating (CDR) was used to assess
ibility, strengthening, balance, and endurance exercises as the severity of dementia in two studies (Canonici et al.,
well as psychoeducation, communication training, skills 2012; Pitkala et al., 2013). One study included individuals
training, and pleasant activities training (Prick et al., 2015). with mild to moderate dementia due to AD (CDR 12;

2 Journal of Motor Behavior


TABLE 1. Clinical Trials Investigating the Effect of a Dyadic Exercise Training Intervention Including Both the Persons with AD and the Caregivers

2016, Vol. 0, No. 0


Trial Design Intervention Sample Outcomes Results Limitations

Pitkala et al. Randomized (1) HB Community-dwelling (1) Cognition: CDT, VF, Between-group differences - Caregivers were
(2013) controlled (2) GB dyads (n D 210) of CDR, and MMSE CDT: HB > CG (p D .07) included in the trial

Ohman et al. trial (3) CG individuals with (2) Neuropsychiatric and VF: NS but caregivers
(2016) Exercise: aerobic, strength AD and their behavioral outcomes: MMSE: NS burden was not
and endurance, dual- spousal caregivers NA 10-m walking speed: NS reported as an
task, and balance (1) n D 70 (59 at 12 (3) Physical functioning FIM: HB and GB > CG outcome
training (15 min for months) (primary outcome): Falls: HB and GB fewer falls vs. CG
each component) C (2) n D 70 (51 at 12 FIM, Short Physical (p < .05)
executive functioning months) Performance Battery, 10-m Within-group differences: change from
training (15 min), two (3) n D 70 (51 at 12 walking test baseline
times/week months) (4) Caregivers outcomes: CDT
Intensity: not reported NA HB C0.48 (95% CI [0.06, 0.91])
HE: physical exercise at (5) Other: NA GB C0.01 (95% CI [0.44, 0.46])
home for 1 h two times/ CG 0.21 (95% CI [0.67, 0.25])
week for 12 months, VF
supervised by a HB 0.99 (95% CI [1.67, 0.32])
physiotherapist GB 0.95 (95% CI D 0.00, 0.23])
GE: 4-hr sessions (1 h of CG 1.14 (95% CI [1.86, 0.41])
exercise) in adult MMSE
daycare centers two HB 1.63 (95% CI [2.64, 0.61])
times/w for 12 months. GB 1.23 (95% CI [2.33, 0.14])
Groups of 10 supervised CG 1.08 (95% CI [2.17, 0.02])
by two physiotherapists. 10-m walking test
Assessments at baseline, HB 0.09 (95% CI [0.14, 0.03])
three months, six GB 0.12 (95% CI [0.17, 0.06])
months, and 12 months CG 0.16 (95% CI [0.22, 0.11])
FIM
HB 7.1 (95% CI [3.7, 10.5])
GB 10.3 (95% CI [6.7, 13.9])
CG 14.4 (95% CI [10.9, 18.0])

(Continued on next page)


Exercise for Alzheimers Disease Persons and Caregivers

3
4
TABLE 1. Clinical Trials Investigating the Effect of a Dyadic Exercise Training Intervention Including Both the Persons with AD and the Caregivers
(Continued)

Trial Design Intervention Sample Outcomes Results Limitations

Prick et al. Randomized (1) Ex Community-dwelling (1) Cognition: MMSE Between-group differences - Inclusion criteria not
(2015) controlled (2) C (usual care C three patients with (only at baseline) NS on any of the outcomes limited to AD
trial written information dementia and their (2) Neuropsychiatric and Within-group differences - Compliance: full
bulletins and three caregivers with a behavioral outcomes: NS on any of the outcomes compliance D nine
phone calls) score on the CES- Dutch version of the dyads (15.8%),
Exercise: four types of D>5 RMBPC moderate compliance
G. Lamotte, R. C. Shah, O. Lazarov & D. M. Corcos

physical exercises: n D 111 dyads (3) Physical functioning: D 43 dyads (75.4%)


flexibility, randomized Standard single item- - Small sample size
strengthening, balance (1) n D 57 (45 scale for self-rated according to power
and endurance exercises. caregivers and 45 general health calculation
>30 min per session, persons with (4) Caregivers outcomes: - No result for MMSE at
three times/week for dementia at six CES-D (primary follow-up
three months months) outcome), Dutch SPICC - Short duration of the
Support component: (a) (2) n D 54 (43 (5) Other: salivary cortisol study
psychoeducation, (b) caregivers and 42
communication, skills persons with
training, (c) pleasant dementia at six
activities training months)
Intensity: not reported
Supervision by a coach
weekly the first four
weeks, biweekly the
next eight weeks
Assessments at baseline,
three months, and at six-
month follow-up

Journal of Motor Behavior


Lowery et al. Randomized (1) Ex Community-dwelling (1) Cognition: NA Between-group differences - Adherence: prescribed
(2013) controlled (2) C (usual care) patients with ICD- (2) Neuropsychiatric and NPI composite: NS frequency of walks
trial Exercise: walking designed 10 confirmed behavioral outcomes: Ex 41% more likely to reach a clinically was achieved by only
to become progressively dementia and composite NPI score significant reduction  3 points of NPI 30.77% of the Ex
more intensive and last significant (primary endpoint)*, composite score by week 12. group, and prescribed
between 20 and 30 min. behavioural and mean differences in NPI However, NS between Ex and C intensity was

2016, Vol. 0, No. 0


Goal: five times/week psychological score, GHQ Mean NPI: NS achieved in only
for 12 weeks symptoms and (3) Physical functioning: ZCBS: Ex (23% to 17%) > C (16 to 53.25% of the walks.
Intensity: RPE 12-14 their caregivers. NA 32%; p D 0.01) - Inclusion criteria not
Supervision with a physical n D 131 dyads (4) Caregivers outcomes: GHQ, DemQOL-Proxy: NS limited to AD
therapist for the first six (1) n D 67 (59 at DemQOL-Proxy Self-reported walking time: NS - Short duration of the
weeks 12w) (DemQol), ZCBS Within-group differences study
Assessments at baseline, (2) n D 64 (57 at (5) Other: NA No within-group statistical analysis - Weakness of self-
six weeks, and 12 weeks 12w) *Clinically significant report in measuring
reduction exercise
(BaselineWeek 12):
reduction of the
composite NPI score  3
points
Canonici et Controlled (1) Ex Community patients (1) Cognition: MMSE Between-group differences - Randomization not
al. (20129 trial (2) C (usual care) with probable mild (only at baseline) NPI (patient): Ex > C mentioned
Exercise: (i) initial warm to moderate AD (2) Neuropsychiatric and FIM: Ex > C (p D .01) - Evaluation not blinded
up; (ii) initial stretching; and their behavioral outcomes: BFBS: Ex > C (p D .001) - Small sample size
(iii) flexibility, strength, caregivers NPI and Cornell Scale Pfeffer quest: NS - Primary and secondary
agility and balance; (iv) n D 32 dyads for Depression in NPI-caregiver: Ex > C (p D .01) endpoint not clearly
return to physical calm; (1) n D 16 (16 at six Dementia ZCBS: Ex > C (p D .01) stated - - No result for
and (v) final stretching. months) (3) Physical functioning: Within-group differences: change from MMSE at follow-up
Walking and dancing (2) n D 16 (11 at six FIM, BFBS, baseline
were also part of the months) instrumental daily NPI (patient): Ex: 40.3 34.0 to 16.9
program. three times/ activities assessed with 17.6 vs. C: 39.6 25.to 43.3 18.4
week for six months the Pfeffer FIM (total): Ex: 09.6 12.5 vs. C: 108.4
Intensity: not reported Questionnaire 10.299.5 18.0 to 71.6 31.0 1
Supervision: not reported (4) Caregivers outcomes: BFBS: Ex: 46.4 7.8 to 51.9 3.4 vs.
Assessments at baseline NPI-caregiver, ZCBS C: 46.4 8.1 to 26.9 17.7
and six months (5) Other: NA Pfeffer quest: Ex: 19.8 7.4 to 22.3
7.4
vs. C: 23.0 5.3 to 28.2 3.0
NPI-Caregivers: Ex: 18.3 13.8 to 3.3
6.5 vs. C: 19.6 14.3 to 20.4 9.6
ZCBS: Ex: 32.3 14.7 to 14.6 8.1 vs.
C 35.6 14.9 to 35.5 13.7
AD D Alzheimers disease; BFBS D Berg Functional Balance Scale; CES-D D Centre for Epidemiologic Studies-Depression; DemQol D DemQOL-Proxy; HB D home-based exercise; C D control group;
CDT D Clock Drawing Test; CDR D Clinical Dementia Rating; CG D control group (usual care); Ex D exercise group; FIM D Functional Independence Measure; GB D group-based exercise; GHQ D
General Health Questionnaire; MMSE D Mini-Mental State Examination; NA D not assessed; NPI D Neuropsychiatric Inventory; NS D no significant difference (p > .05); RMBPC D Dutch version of
the Revised Memory and Behavioral Problem Checklist; RPE D rating of perceived exertion; SPICC D Dutch Self-Perceived from Family Care; VF D Verbal Fluency; ZCBS D Zarit Caregiver Burden
Scale.
Exercise for Alzheimers Disease Persons and Caregivers

5
G. Lamotte, R. C. Shah, O. Lazarov & D. M. Corcos

Canonici et al., 2012), whereas another included individuals reduction of the Neuropsychiatric Inventory (NPI) score
with mild to severe dementia due to AD (CDR 0.53; Pit- (Lowery et al., 2014). However, the difference was not sta-
kala et al., 2013). The two other studies used the Mini-Men- tistically significant at week 12 between the intervention
tal State Examination (MMSE) to assess the severity of and control groups (p D .6; Lowery et al., 2014). The
dementia (Lowery et al., 2014; Prick et al., 2015). The authors also did not find any significant effect of exercise
mean MMSE was 14.9 8.7 in controls and 16.3 7.4 in training on mental well being assessed with the General
the intervention group in one study (Lowery et al., 2014), Health Questionnaire in individuals with dementia (Lowery
whereas the mean MMSE was 21 5.56 in controls and 21 et al., 2014). A smaller controlled study found that individ-
4.86 in the intervention group in the other study (Prick et uals with mild to moderate AD randomized to the exercise
al., 2015). Caregivers were a partner or spouse in two stud- group showed a significant decrease in the NPI score rela-
ies (Lowery et al., 2014; Pitkala et al., 2013). The demo- tive to the controls (40.3 34.0 to 16.9 17.6 at six
graphic characteristics of the caregivers were not reported months vs. 39.6 25.to 43.3 18.4 at six months; Canon-
in one study, whereas there were 39 female controls ici et al., 2012). The third study did not find any significant
(60.9%) and 50 women (74.6%) in the intervention group effect of exercise training on behavioral symptoms in indi-
in the other study (Lowery et al., 2014). In one study, 30 of viduals with AD when assessed with the Revised Memory
the 32 caregivers were women (93.7%) but the relationship and Behavior Checklist, a 24-item caregiver-report measure
between caregiver and care receiver was not characterized of observable behavioral problems in the care receiver with
(Canonici et al., 2012). Prick et al. included spouses (100 of dementia (Prick et al., 2015).
111 dyads) and child or other caregivers (11 of 111) and
caregivers were predominantly women (72.1% in the total
Functional Performances and General Health
sample). The adherence was reported as good in the inter-
vention group in two studies (Canonici et al., 2012; Two studies investigated the effect of exercise training
Pitkala et al., 2013), whereas the adherence to the full exer- on functional performances in individuals with AD across
cise regimen was poor in two studies (Lowery et al., 2014; several outcomes including the Functional Independence
Prick et al., 2015). Measure (FIM; Canonici et al., 2012; Pitkala et al., 2013),
the Short Physical Performance Battery and the 10-m walk-
ing test (Pitkala et al., 2013), the Berg Functional Balance
Outcomes
Scale and instrumental daily activities assessed with the
Pfeffer Questionnaire (Canonici et al., 2012). One study
Cognition
also assessed general health with the Standard single-item
One study investigated the effect of exercise training on scale for self-rated general health (Prick et al., 2015). The
cognition in individuals with dementia across several out- FIM was preserved following a six-month multicomponent
come measures including the Clock Drawing Test (CDT), motor intervention program focusing on stretching, flexibil-
verbal fluency (VF), and the MMSE (Ohman et al., 2016). ity, strength, agility, and balance, whereas the controls
Executive function, measured using CDT, improved in the showed a significant decline (p D .01; Canonici et al.,
home-based exercise group, and changes in the score were 2012). This study also reported better scores in functional
significantly better than those of the control group at 12 balance (Berg scale) in the exercise group compared to
months. All groups deteriorated in VF and MMSE score the control group (Canonici et al., 2012). In another study,
during the intervention, and no significant differences the decline in functional independence was slower for the
between the groups were detected at 12 months (Ohman et home-based and the group-based exercise groups compared
al., 2016). In this study, 67% of individuals with AD had to controls (Pitkala et al., 2013). Even though there was no
moderate or severe AD (CDR 23), and 96% were taking statistically significant difference regarding the walking

AD medication (Ohman et al., 2016). The three other stud- speed between the three groups, participants in the exercise
ies did not report cognitive assessment after the interven- groups had significantly fewer falls than the controls during
tion in individuals with AD or other types of dementia follow-up (Pitkala et al., 2013). Prick et al. did not find any
(Canonici et al., 2012; Lowery et al., 2014; Prick et al., significant difference between the exercise group and the
2015). control group regarding general health (Prick et al., 2015).

Neuropsychiatric and Behavioral Symptoms Caregiver Burden


Three studies investigated the effect of exercise training Caregiver burden was assessed in three studies (Canonici
on neuropsychiatric and behavioral symptoms (Canonici et et al., 2012; Lowery et al., 2014; Prick et al., 2015). Care-
al., 2012; Lowery et al., 2014; Prick et al., 2015). In a con- giver burden as measured by the Zarit Caregiver Burden
trolled, single-blind, parallel-group trial of a walking regi- Interview doubled from 16% at baseline to 32% by week
men with incremental intensity, the intervention group was 12 for the control group participants (usual care) but
41% more likely to experience a clinically important decreased from 23% to 17% for those in the intervention

6 Journal of Motor Behavior


Exercise for Alzheimers Disease Persons and Caregivers

group (p D .01) in one study (Lowery et al., 2014). Another Potential Benefits of Exercise Training for Physical
study using the same scale found that caregivers burden Functioning and General Health in Individuals with AD
decreased in the intervention group while it remained stable
This review supports the fact that a dyadic exercise train-
in the controls (p < .5; Canonici et al., 2012). Conversely,
ing intervention can improve functional outcome and bal-
one study did not find any significant effect of the dyadic
ance in individuals with AD. Balance and mobility
exercise intervention on caregivers burden, caregivers
impairments in older people have been shown to be a strong
mood or salivary cortisol used as a noninvasive assessment
independent risk factor for falling (Deandrea et al., 2010).
of stress in caregivers (Prick et al., 2015).
Falls lead to a fear of falling and loss of confidence, which
may result in a decline in activity and ultimately a decrease
Discussion in strength, balance, and mobility, leading to decreased
functional ability and a loss of independence (Rasinaho,
Potential Benefits of Exercise Training on the Symptoms of Hirvensalo, Leinonen, Lintunen, & Rantanen, 2007). Falls
Dementia: Cognitive Performances, Neuropsychiatric and are also often a trigger for emergency department or hospi-
Behavioral Symptoms tal admission for older people with dementia or admission
to residential care (Rowe & Fehrenbach, 2004). In line with
Given the current review, a dyadic exercise intervention
the results of the present review, a systematic review and
may improve executive function in individuals with demen-
meta-analysis of four randomized controlled studies found
tia when compared to a control group. However, change in
that strength, balance, and endurance or mobility training
cognitive performance was only assessed in one study
can assist in the reduction of falls in individuals with
(Ohman et al., 2016) and there is a need for a well-designed
dementia (Burton et al., 2015).
controlled clinical trial that is powered to detect differences
Going beyond the outcomes reported in the four studies
in cognitive outcomes in individuals with AD and that
included in this review, another point to consider is the
includes both on and off anticholinergic medication testing
potential impact of exercise training on several aspects of
to truly assess cognitive changes without any confounding
health in persons with AD. The benefits of exercise training
effect of medication. It is important to note that, even
for cardiovascular function are well established for several
though the study by Ohman et al. had a rigorous methodol-
diseases including heart diseases, diabetes and obesity
ogy with a large sample size (n D 210 dyads at baseline,
(Ades et al., 2011; Church et al., 2011; Khan et al., 2012).
n D 161 assessed at 12 months), the findings presented
Because of the possible inverse relationship between car-
were secondary outcomes and the effects were mild and
diovascular fitness and cognitive impairment in the elderly
limited to executive functioning. Based on the present
and the fact that atherosclerosis and vascular pathology
review, it is also unclear if a dyadic exercise intervention
within the brain may play an important role in the patho-
provides benefit for neuropsychiatric and behavioral symp-
physiology of AD and other dementias, we suggest that
toms in individuals with dementia. A recent Cochrane
exercise training (especially endurance exercise training)
review on the effect of exercise on people with dementia
not only may be a therapy of choice in this population, but
included 17 trials with a total of 1,067 participants, most of
may have an even greater benefit for people with dementia
whom were older individuals with a clinical diagnosis of
with comorbid complications (Buratti et al., 2015; Hillman,
AD (Forbes et al., 2015). This review suggested that exer-
Erickson, & Kramer, 2008; Prins & Scheltens, 2015).
cise training may improve the ability to perform activities
Moreover, beside the potential benefits for the brain and the
of daily living in people with dementia but found no signifi-
cardiovascular system, exercise training has been shown to
cant effect of exercise on cognition, behavior disorders, and
be beneficial for depression, fatigue, sleep-disorders, auto-
depression (Forbes et al., 2015). The studies included in
nomic dysfunction and constipation in older adults
this review were heterogeneous with regard to the type of
(Billman & Kukielka, 2006; Kelley & McClellan, 1994;
intervention program, the duration of the intervention, or
King, Oman, Brassington, Bliwise, & Haskell, 1997; Peters,
the severity of the disease preventing us from making any
De Vries, Vanberge-Henegouwen, & Akkermans, 2001).
clear conclusion in patients with dementia. Other clinical
These symptoms are very common in AD and exercise
trials have shown that exercise training has positive effects
training may have the same beneficial effects in those with
on global cognition and executive function in individuals at
AD as in healthy people.
risk for AD (Lautenschlager et al., 2008; van Uffelen, Chi-
napaw, van Mechelen, & Hopman-Rock, 2008). Therefore,
individuals with dementia may have less cognitive benefit
Potential Benefits of Exercise Training for the
from exercise than those at risk of AD (i.e., mild cognitive
Caregivers
impairment). Further study is needed to investigate the
effect of exercise training on different domains of cogni-
Direct Benefit of Exercise Training on Caregivers Burden
tion, and to understand central mechanisms that may be
responsible for changes in cognitive performances in indi- Studies have shown that caregivers often do not have the
viduals with AD and it risk of AD. time to engage in preventive health behaviors such as

2016, Vol. 0, No. 0 7


G. Lamotte, R. C. Shah, O. Lazarov & D. M. Corcos

regular exercise training, and studies have found that care- training may improve psychological outcomes in caregivers
givers participate in less formal exercise compared to non- of patients with dementia. The heterogeneity between the
caregivers (Fredman, Bertrand, Martire, Hochberg, & type of intervention, the inclusion and exclusion criteria,
Harris, 2006; Hirano et al., 2011). Two of the studies and the small sample sizes restrict the generalizability of
included in this present review reported positive effects of results and more research is needed to assess the potential
exercise training on caregiver burden (Canonici et al., benefit of exercise training in caregivers on psychological
2012; Lowery et al., 2014) whereas one study did not find and nonpsychological outcomes.
any significant benefit (Prick et al., 2015). The negative
results in this study may partially be explained by the low
Indirect Benefits of Exercise Training on Caregivers
compliance during the intervention (Prick et al., 2015).
Burden
Indeed, only nine dyads (15.8%) were fully compliant with
the exercise program and 43 dyads (75.4%) were character- Exercise training in persons with AD has potential indi-
ized as moderately compliant (Prick et al., 2015). There- rect benefits for the caregivers. In a Cochrane review, none
fore, there is evidence that a dyadic exercise training of the 17 studies included caregivers as actual exercise par-
intervention may improve caregivers burden. A systematic ticipants and no studies reported data on caregivers quality
review including four randomized clinical trials comparing of life (Forbes et al., 2015). However, two clinical trials
physical activity in caregivers of people with dementia with have investigated caregiver burden as a secondary outcome
a control group found that physical activity may have direct (Steinberg, Leoutsakos, Podewils, & Lyketsos, 2009;
psychological benefits for the caregivers and may reduce Vreugdenhil, Cannell, Davies, & Razay, 2012). In one
subjective caregiver burden (Orgeta & Miranda-Castillo, study, a community-based exercise program for participants
2014). For instance, King and Brassington (1997) showed with AD consisting of 10 simple exercises in addition to
that brisk walking was associated with a significant brisk walking revealed a significant improvement in care-
improvement in anger expression in comparison to controls giver burden evaluated with the Zarit Burden Interview
(usual activity). In another study, brisk walking was associ- (Vreugdenhil et al., 2012). This study provides evidence
ated with a significant improvement in caregivers subjec- that challenging and potentially improving motor function
tive burden assessed by the Screen for Caregiver Burden of the individual with AD can lead to a reduced burden of
scale, depression assessed by the Beck Depression Inven- care. However, in the second study, an exercise intervention
tory scale and stress assessed by the Total Manifest Anxiety delivered by caregivers to home-dwelling participants with
Scale (TMAS; King et al., 2002). However, there was no AD was not associated with a reduction of the caregiver
significant difference regarding depression and stress burden evaluated with the Screen for Caregiver Burden
between the exercise group and a group following a nutri- (Steinberg et al., 2009). In this study, the role of the care-
tion education program (King, 2002). A recent 36-week giver was to supervise the exercise regimen consisting of
crossover pilot clinical trial investigated the effect of exer- three components: aerobic fitness, strength training and bal-
cise in both individuals with AD and caregivers but was not ance and flexibility training. This supervising role may
included in Table 1 (Barnes et al., 2015). Even though par- have been a confounding factor when analyzing caregiver
ticipants and caregivers were enrolled as dyads, caregivers burden. In another study, 26 individuals with mild to mod-
were not actively following the exercise protocol and care- erate AD performed a six-month cycling program and care-
giver measures included questionnaires about the partic- giver burden was assessed using the NPI Caregiver scale
ipants functional status, quality of life, and dementia- (Yu et al., 2015). Caregiver distress decreased by 40%
related behaviors as well as their own level of distress with between baseline and the final assessment at six months
behaviors and overall burden (Barnes et al., 2015). With (30% reduction in baseline score is considered to be clini-
respect to caregiver burden, the results were not statistically cally meaningful). According to the authors, this finding
significant but suggested potentially clinically meaningful goes beyond the 810 hr of respite per week for the care-
improvement (Barnes et al., 2015). The positive effect of givers and they reported improved attitudes and confidence
an exercise-training program on caregiver burden could be in individuals with AD, which made it easier for them to
secondary to several potential benefits for the caregivers. provide care (Yu & Swartwood, 2012; Yu et al., 2015).
First, exercise can decrease levels of stress and has been More research is needed to investigate the indirect impact
shown to have a positive effect on depression (Loi et al., of exercise training in persons with dementia on caregivers
2014). Second, exercise can improve motor and nonmotor psychological outcomes.
functioning of the individual with dementia leading to a
reduced burden of care. Third, fostering a bonding experi-
Potential Benefits of a Dyadic Exercise Intervention
ence and establishing mutual purpose with the individual
with dementia may reduce caregiver burden. Last, there are Using a dyadic intervention could be seen as effective
likely personal health benefits for the caregiver following because of the mutual influence between the person with
an exercise regimen and it may increase their capacity to dementia and the informal caregiver. A systematic review
care for individuals with dementia. Therefore, exercise including 50 studies between 1992 and 2005 showed that

8 Journal of Motor Behavior


Exercise for Alzheimers Disease Persons and Caregivers

dyadic psychosocial interventions are effective in improv- and judgment, the motivation of the demented persons is
ing various outcomes in individuals with AD and their care- directly influenced by caregivers implementation. This is a
givers including behavioral problems, quality of life, and very important point to consider in designing an exercise
mood. However, the outcomes for the person with dementia clinical trial for persons with dementia as well as in gener-
and the caregiver varied between studies using different alizing and applying the results in routine practice settings.
interventions, designs, or methodologies (Vant Leven et Optimal rehabilitation training should involve the active
al., 2013). The authors concluded that studies should care- participation of the patient as opposed to passive manipula-
fully match the targeted functional domains, intervention tion (Katalinic, Harvey, & Herbert, 2011; Nielsen,
components, and delivery characteristics of a program with Willersley-Olsen, Christiansen, Lundbye-Jensen, & Lorent-
the needs of the person with dementia and the family care- zen, 2015). The other key components of an optimal reha-
giver (Vant Leven et al., 2013). This present review dem- bilitation program include challenging the skill of the
onstrates that including both persons with AD and their person training, motivating and rewarding, intensive train-
caregivers in exercise clinical trials is feasible and may pro- ing for as long a period of time that is feasible, and care-
duce a positive effect on the tested outcomes, especially fully organizing the training in the setting of other activities
when programs target caregiver burden and functional inde- (Nielsen et al., 2015). Importantly, the patients and care-
pendence. However, further study is needed to investigate givers need to understand that consistent training several
the effect of a dyadic exercise intervention on cognitive times a week will be part of the rest of their lives if they
performances, behavioral and neuropsychiatric symptoms, want to maintain any potential benefits. Ideally, a therapist
quality of life, and other common symptoms in people with would be available during all training sessions, however
dementia (e.g., sleep disturbances, fatigue). this is not practically possible for the majority of patients
outside of a clinical trial setting due to cost, accessibility
issues, and other prohibitive factors. Therefore, trained
What Should be the Role of the Caregiver in a Dyadic
caregivers could play a central role by continuing regular
Exercise Intervention?
and challenging training with the persons with AD in the
A dyadic exercise intervention provides new information absence of a therapist. Periodic reinforcement with a thera-
on the effects of exercise training in individuals with pist will be a component of the rehabilitation training regi-
dementia and their caregivers. Involving caregivers has men to adapt the level of difficulty of training with the
been evaluated in other nonpharmocological interventions, goals of improving the performance of a given task and
such as cognitive stimulation interventions, and it has achieving new skills to promote brain plasticity (Burke &
shown positive benefits for both caregivers and people with Barnes, 2006; Nielsen et al., 2015). Thus, we propose that
dementia (Onder et al., 2005; Quayhagen et al., 2000). To the caregivers would also play a significant role in the train-
maintain any potential benefit after the end of a trial for the ing of persons with AD and the promotion of short- and
individual with dementia, the caregiver should continue to long-term brain plasticity by increasing adherence to the
implement the skills he or she gained during the study. Ini- exercise program.
tial readiness and therapeutic engagement were two factors
associated with caregiver readiness to use nonpharmacolog-
Cost Effectiveness and Health Care Implications
ical strategies to manage behavioral symptoms of dementia
in one study (Gitlin & Rose, 2014). There is also evidence Including both the persons with AD and the caregivers in
that the dynamic and multidimensional relationship exercise training clinical trials would also allow more pre-
between the caregivers and the person with AD is cise cost effectiveness analyses. Lowery et al. (2014) found
extremely important, and is a key factor in maintaining a that a dyadic exercise intervention was more cost effective
sense of self and personhood for the patient (Whitlatch, than usual treatment from both societal as well as health
2001). Whitlatch argued that the integration of persons and social care perspectives with respect to behavioral and
with dementia in family caregiving research could provide psychological symptoms as an outcome measure. However,
new insight into caregivers burden while promoting auton- it did not appear to be cost effective in terms of cost per
omy of the individual with dementia. We agree with Whit- quality-adjusted life-year gain (Lowery et al., 2014). The
lachs point of view and we suggest that exercise research costs of dementia include direct medical costs for the per-
is an excellent approach to conducting randomized con- sons with dementia, informal (family) care and social care
trolled trials including both populations. costs (World Alzheimer Report, 2010). In a review, Knapp,
The treatment success of nonpharmacological interven- Iemmi, & Romeo, (2013)found no evidence that physical
tions such as exercise training in persons with dementia exercise programs were cost-effective, whereas cognitive
depends on the skills and motivation of the medical staff, stimulation therapy, tailored activity programs and occupa-
hospital and primary care environment, and motivation of tional therapy were more cost-effective than usual care for
the persons with dementia to complete the exercise program people with AD. The results regarding exercise programs
(Teodorczuk, Welfare, Corbett, & Mukaetova-Ladinska, should be interpreted with caution due to low methodologi-
2010). However, because of impaired memory, thinking, cal quality of available studies, the difficulty of

2016, Vol. 0, No. 0 9


G. Lamotte, R. C. Shah, O. Lazarov & D. M. Corcos

generalizing from available evidence, and the narrowness these methods has relative strengths and weaknesses in
of cost measures (Knapp et al., 2013). For these reasons, terms of accuracy, cost, and feasibility (Linke, Gallo, &
there is a need for large trials with cost effectiveness analy- Norman, 2011). Therefore, we recommend using a combi-
ses that evaluate medical, informal and social costs. With nation of subjective and objective measurements to assess
regard to direct medical care, nonpharmacological interven- adherence to the exercise intervention. In this review,
tion has been evaluated and occupational therapy was found adherence to the exercise regimen for individuals with
to be highly cost effective as financial expenditures were dementia ranged greatly between studies and explicit rea-
reduced for general practitioner and hospital visits for sons why exercise adherence was low were not always
patients with caregivers who received therapeutic interven- reported. Suttanon et al. (2012) and Suttanon et al. (2013)
tions (Graff et al., 2008). By improving caregiver health conducted a detailed analysis, interviewing the persons
and well-being, exercise training has the potential to reduce with dementia and caregivers included in a randomized
informal care. Cost of institutionalization is the major com- clinical trial investigating the effect of a home-based exer-
ponent of the social care cost in dementia (World Alz- cise programme for older people with AD. They found that
heimer Report, 2010). In a hospital setting, a randomized preexisting or acute health conditions, a dislike of struc-
controlled study found that structured caregiver training tured exercise, and caregiver causes (health and unavail-
prolonged the time to nursing home admission and accord- able) were reasons for lower levels of adherence and
ingly increased survival of dementia patients over an obser- concluded that regular support from a physiotherapist and
vation period of eight years (Brodaty, Gresham, & caregiver were key elements facilitating program adherence
Luscombe, 1997). We expect that including caregivers in in people with AD (Suttanon et al., 2012). Behavioral and
exercise training clinical trials will not only improve care- cognitive strategies have been reported to increase the
giver burden, but also lead to better training and a more adherence to exercise (Woodard & Berry, 2001) and cogni-
beneficial role for the caregivers, in turn extending the time tive behavioral therapy has also been shown to be effective
to nursing home admission. A combined exercise interven- in reducing symptoms of depression and anxiety for people
tion for both persons with AD and their caregivers benefits with dementia (Orgeta, Qazi, Spector, & Orrell, 2015).
the health of both groups, and for this reason demonstrates Therefore, we recommend including the caregiver as an
the potential to be cost-effective. active participant and using a multicomponent intervention
with exercise, cognitive behavioral therapy, skills training,
or coping strategies for the caregivers as a way to improve
Potential Challenges of Implementing a Dyadic Exercise
adherence to the exercise regimen and decrease drop out.
Intervention
As exercise awareness increases, it will also be more diffi-
Interventional studies provide social engagement and cult to include patients and caregivers in a control group as
interaction in individuals with dementia and their care- motivated patients with mild dementia or caregivers in the
givers. However, many caregivers still carry professional control group may recognize potential exercise benefits and
and familial responsibilities and one can imagine a poten- engage on their own. Maintaining persistent adequate levels
tial burden for caregivers with an exercise program of exercise for several months may also be a challenge in
repeated several times a week with the same type of exer- clinical trials. Furthermore, to maintain any potential bene-
cise for several weeks. This could influence recruitment of fit, people will likely need to exercise on their own with the
dyads and outcomes such as quality of life or caregiver bur- risk of developing poor exercise habits without supervision.
den as well as compliance to the exercise regimen. On the Another gap in our knowledge is whether exercise is still
other hand, elderly spouses or partners may have physical beneficial to patients in the later stages of dementia. Indeed,
limitation or mental illness themselves and may not be able with the progression of the disease, individuals with demen-
to provide support and follow an exercise regimen. By tia often have increased fall risk, dysautonomia, hallucina-
using a dyadic intervention design, one may predict that tions, depression, and psychosis. Therefore, patients in a
caregivers would spend more time with the care recipients. later stage of their disease may not be able to follow an
Even though the benefit of respite care for caregivers is exercise protocol safely. Future studies of longer duration
unclear (Maayan, Soares-Weiser, & Lee, 2014) it has been and with appropriate follow-up are necessary to consider
shown to have potential beneficial effects for the care recip- the impact of the stage of disease progression as the goal of
ients and possibly delay nursing home admission (Health the intervention may be different at different stages of the
Quality Ontario, 2008). The issue of low compliance with disease.
exercise interventions is an important point to consider and
adherence rates to an exercise regimen are difficult to mea-
Limitations
sure accurately. Several assessment methods are used
including self-report inventories and exercise logs, objec- There were several limitations to this review. We limited
tive measurements such as heart rate monitors, and observa- our search strategy and subsequent review to evidence
tional measurements such as research assistants recording ranked as level I, II, or III in articles that were published in
the amount of exercise participants completed. Each of English-language, peer-reviewed publications. Therefore,

10 Journal of Motor Behavior


Exercise for Alzheimers Disease Persons and Caregivers

studies with positive results and lower level of evidence sudden cardiac death: protection is not due to enhanced cardiac
were not analyzed. Most of the studies that have investi- vagal regulation. Journal of Applied Physiology, 100, 896906.
gated the effects of exercise training in dementia and their http://dx.doi.org/10.1152/japplphysiol.01328.2005
Brodaty, H., Gresham, M., & Luscombe, G. (1997). The Prince
caregivers included a limited number of participants with Henry Hospital dementia caregivers training programme. Inter-
mild to moderate disease severity and were highly super- national Journal of Geriatric Psychiatry, 12, 183192.
vised with a short duration. Therefore, the results of the Buratti, L., Balestrini, S., Altamura, C., Viticchi, G., Falsetti, L.,
study are not fully generalizable to the population with Luzzi, S., & Silvestrini, M. (2015). Markers for the risk of pro-
dementia and their caregivers at large. Finally, two of the gression from mild cognitive impairment to Alzheimers dis-
ease. Journal of Alzheimers Disease, 45, 883890. http://dx.
studies in this review used a diagnosis-related sample (AD; doi.org/10.3233/jad-143135
Canonici et al., 2012; Pitkala et al., 2013), whereas the Burke, S. N., & Barnes, C. A. (2006). Neural plasticity in the age-
other two studies included participants with other types of ing brain. Nature Reviews Neuroscience, 7, 3040. http://dx.
dementia (Lowery et al., 2014; Prick et al., 2015). Given doi.org/10.1038/nrn1809
the differing etiology, pathology, symptoms, and progres- Burton, E., Cavalheri, V., Adams, R., Browne, C. O., Bovery-
Spencer, P., Fenton, A. M., & Hill, K. D. (2015). Effectiveness
sion of disease between the various types of dementia, of exercise programs to reduce falls in older people with demen-
future researchers should focus on a specific diagnosis. tia living in the community: a systematic review and meta-anal-
ysis. Clinical Interventions in Aging, 10, 421434. http://dx.doi.
org/10.2147/cia.s71691
Conclusion Canonici, A. P., Andrade, L. P., Gobbi, S., Santos-Galduroz, R. F.,
Gobbi, L. T., & Stella, F. (2012). Functional dependence and
Including both persons with AD and their caregivers in caregiver burden in Alzheimers disease: a controlled trial on
exercise clinical trials is feasible and may produce a posi- the benefits of motor intervention. Psychogeriatrics, 12, 186
tive effect on caregiver burden and functional indepen- 192. http://dx.doi.org/10.1111/j.1479-8301.2012.00407.x
Church, T. S., Thomas, D. M., Tudor-Locke, C., Katzmarzyk, P.
dence. However, there is not yet a proven effect of a dyadic T., Earnest, C. P., Rodarte, R. Q., & Bouchard, C. (2011).
exercise intervention on cognitive performances, behav- Trends over 5 decades in U.S. occupation-related physical
ioral and neuropsychiatric symptoms, quality of life, and activity and their associations with obesity. PLoS One, 6,
other common symptoms in people with dementia (e.g., e19657. http://dx.doi.org/10.1371/journal.pone.0019657
sleep disturbances, fatigue). In conclusion, there is a need Deandrea, S., Lucenteforte, E., Bravi, F., Foschi, R., La Vecchia,
C., & Negri, E. (2010). Risk factors for falls in community-
for more studies that include both persons with AD and dwelling older people: a systematic review and meta-analysis.
their caregivers to assess several important points: (a) the Epidemiology, 21, 658668. http://dx.doi.org/10.1097/
feasibility of a combined AD person-caregiver exercise EDE.0b013e3181e89905
program; (b) the effects of a combined AD person-care- Forbes, D., Forbes, S. C., Blake, C. M., Thiessen, E. J., & Forbes,
giver intervention on the mood and burden of caregivers S. (2015). Exercise programs for people with dementia.
Cochrane Database of Systematic Reviews, 4, Cd006489. http://
and cognitive and noncognitive outcomes of persons with dx.doi.org/10.1002/14651858.CD006489.pub4
AD; (c) the optimal intensity of exercise training; (d) the Fredman, L., Bertrand, R. M., Martire, L. M., Hochberg, M., &
impact of exercise training on the dynamic relationship Harris, E. L. (2006). Leisure-time exercise and overall physical
between the persons with AD and their caregivers; (e) activity in older women caregivers and non-caregivers from the
determination of which people benefit most from exercise Caregiver-SOF Study. Preventive Medicine, 43, 226229.
http://dx.doi.org/10.1016/j.ypmed.2006.04.009
training; and (f) the cost effectiveness of such a program. Gitlin, L. N., & Rose, K. (2014). Factors associated with caregiver
readiness to use nonpharmacologic strategies to manage demen-
tia-related behavioral symptoms. International Journal of Geriat-
References
ric Psychiatry, 29, 93102. http://dx.doi.org/10.1002/gps.3979
Adelman, R. D., Tmanova, L. L., Delgado, D., Dion, S., & Lachs, Graff, M. J., Adang, E. M., Vernooij-Dassen, M. J., Dekker, J.,
M. S. (2014). Caregiver burden: a clinical review. JAMA, 311, Jonsson, L., Thijssen, M., & Rikkert, M. G. (2008). Community
10521060. http://dx.doi.org/10.1001/jama.2014.304 occupational therapy for older patients with dementia and their
Ades, P. A., Savage, P. D., Lischke, S., Toth, M. J., Harvey- care givers: cost effectiveness study. BMJ (Clinical Research
Berino, J., Bunn, J. Y., & Schneider, D. J. (2011). The effect of Edition), 336, 134138. http://dx.doi.org/10.1136/
weight loss and exercise training on flow-mediated dilatation in bmj.39408.481898.BE
coronary heart disease: a randomized trial. Chest, 140, 1420 Gross, R. A., & Johnston, K. C. (2009). Levels of evidence: Tak-
1427. http://dx.doi.org/10.1378/chest.10-3289 ing Neurology to the next level. Neurology, 72, 810. http://dx.
Alzheimers Association. (2016). 2016 Alzheimers disease facts doi.org/10.1212/01.wnl.0000342200.58823.6a
and figures. Alzheimers & Dementia, 12, 459509. http://dx. Health Quality Ontario. (2008). Caregiver- and patient-directed
doi.org/10.1016/j.jalz.2016.03.001 interventions for dementia: An evidence-based analysis.
Barnes, D. E., Mehling, W., Wu, E., Beristianos, M., Yaffe, K., Ontario Health Technology Assessment Series, 8(4), 198.
Skultety, K., & Chesney, M. A. (2015). Preventing loss of inde- Hillman, C. H., Erickson, K. I., & Kramer, A. F. (2008). Be smart,
pendence through exercise (PLIE): a pilot clinical trial in older exercise your heart: exercise effects on brain and cognition.
adults with dementia. PLoS One, 10, e0113367. http://dx.doi. Nature Reviews Neuroscience, 9, 5865. http://dx.doi.org/
org/10.1371/journal.pone.0113367 10.1038/nrn2298
Billman, G. E., & Kukielka, M. (2006). Effects of endurance Hirano, A., Suzuki, Y., Kuzuya, M., Onishi, J., Hasegawa, J., Ban,
exercise training on heart rate variability and susceptibility to N., & Umegaki, H. (2011). Association between the caregivers

2016, Vol. 0, No. 0 11


G. Lamotte, R. C. Shah, O. Lazarov & D. M. Corcos

burden and physical activity in community-dwelling caregivers Onder, G., Zanetti, O., Giacobini, E., Frisoni, G. B., Bartorelli, L.,
of dementia patients. Archives of Gerontology and Geriatrics, Carbone, G., & Bernabei, R. (2005). Reality orientation therapy
52, 295298. http://dx.doi.org/10.1016/j.archger.2010.04.011 combined with cholinesterase inhibitors in Alzheimers disease:
Katalinic, O. M., Harvey, L. A., & Herbert, R. D. (2011). Effec- randomised controlled trial. British Journal of Psychiatry, 187,
tiveness of stretch for the treatment and prevention of contrac- 450455. http://dx.doi.org/10.1192/bjp.187.5.450
tures in people with neurological conditions: a systematic Orgeta, V., & Miranda-Castillo, C. (2014). Does physical activity
review. Physical Therapy, 91, 1124. http://dx.doi.org/10.2522/ reduce burden in carers of people with dementia? A literature
ptj.20100265 review. International Journal of Geriatric Psychiatry, 29, 771
Kelley, G., & McClellan, P. (1994). Antihypertensive effects of 783.
aerobic exercise. A brief meta-analytic review of randomized Orgeta, V., Qazi, A., Spector, A., & Orrell, M. (2015). Psychologi-
controlled trials. American Journal of Hypertension, 7, 115119. cal treatments for depression and anxiety in dementia and mild
Khan, K. M., Thompson, A. M., Blair, S. N., Sallis, J. F., Powell, cognitive impairment: systematic review and meta-analysis.
K. E., Bull, F. C., & Bauman, A. E. (2012). Sport and exercise British Journal of Psychiatry, 207, 293298. http://dx.doi.org/
as contributors to the health of nations. Lancet, 380, 5964. 10.1192/bjp.bp.114.148130
http://dx.doi.org/10.1016/S0140-6736(12)60865-4 Peters, H. P., De Vries, W. R., Vanberge-Henegouwen, G. P., &
King, A. C., & Brassington, G. (1997). Enhancing physical and Akkermans, L. M. (2001). Potential benefits and hazards of
psychological functioning in older family caregivers: the role of physical activity and exercise on the gastrointestinal tract. Gut,
regular physical activity. Annals of Behavioral Medicine, 19, 48, 435439.
91100. Pitkala, K. H., Poysti, M. M., Laakkonen, M. L., Tilvis, R. S.,
King, A. C., Oman, R. F., Brassington, G. S., Bliwise, D. L., & Savikko, N., Kautiainen, H., & Strandberg, T. E. (2013). Effects
Haskell, W. L. (1997). Moderate-intensity exercise and self- of the finnish alzheimer disease exercise trial (FINALEX): A
rated quality of sleep in older adults. A randomized controlled randomized controlled trial. JAMA Internal Medicine, 173,
trial. JAMA, 277, 3237. 894901. http://dx.doi.org/10.1001/jamainternmed.2013.359
King AC, Baumann K, OSullivan P, Wilcox S, Castro C. (2002). Prick, A. E., de Lange, J., Twisk, J., & Pot, A. M. (2015). The
Effects of moderate-intensity exercise on physiological, behav- effects of a multi-component dyadic intervention on the psycho-
ioral, and emotional responses to family caregiving: a random- logical distress of family caregivers providing care to people
ized controlled trial. Journals of Gerontology Series A: with dementia: a randomized controlled trial. International Psy-
Biological Sciences and Medical Sciences, 57(1), M2636. chogeriatrics, 27, 20312044. http://dx.doi.org/10.1017/
Knapp, M., Iemmi, V., & Romeo, R. (2013). Dementia care costs and s104161021500071x
outcomes: a systematic review. International Journal of Geriatric Prins, N. D., & Scheltens, P. (2015). White matter hyperinten-
Psychiatry, 28, 551561. http://dx.doi.org/10.1002/gps.3864 sities, cognitive impairment and dementia: an update. Nature
Lautenschlager, N. T., Cox, K. L., Flicker, L., Foster, J. K., van Reviews Neurology, 11, 157165. http://dx.doi.org/10.1038/
Bockxmeer, F. M., Xiao, J., & Almeida, O. P. (2008). Effect of nrneurol.2015.10
physical activity on cognitive function in older adults at risk for Quayhagen, M. P., Quayhagen, M., Corbeil, R. R., Hendrix, R. C.,
Alzheimer disease: a randomized trial. JAMA, 300, 10271037. Jackson, J. E., Snyder, L., & Bower, D. (2000). Coping with
http://dx.doi.org/10.1001/jama.300.9.1027 dementia: evaluation of four nonpharmacologic interventions.
Linke, S. E., Gallo, L. C., & Norman, G. J. (2011). Attrition and International Psychogeriatrics, 12, 249265.
adherence rates of sustained vs. intermittent exercise interven- Rasinaho, M., Hirvensalo, M., Leinonen, R., Lintunen, T., & Ran-
tions. Annals of Behavioral Medicine, 42, 197209. http://dx. tanen, T. (2007). Motives for and barriers to physical activity
doi.org/10.1007/s12160-011-9279-8 among older adults with mobility limitations. Journal of Aging
Loi, S. M., Dow, B., Ames, D., Moore, K., Hill, K., Russell, M., & and Physical Activity, 15, 90102.
Lautenschlager, N. (2014). Physical activity in caregivers: Rowe, M. A., & Fehrenbach, N. (2004). Injuries sustained by com-
What are the psychological benefits? Archives of Gerontology munity-dwelling individuals with dementia. Clinical Nursing
and Geriatrics, 59, 204210. http://dx.doi.org/10.1016/j. Research, 13, 98110, discussion 111116. http://dx.doi.org/
archger.2014.04.001 10.1177/1054773803262520
Lowery, D., Cerga-Pashoja, A., Iliffe, S., Thune-Boyle, I., Griffin, Steinberg, M., Leoutsakos, J. M., Podewils, L. J., & Lyketsos, C. G.
M., Lee, J., & Warner, J. (2014). The effect of exercise on (2009). Evaluation of a home-based exercise program in the treat-
behavioural and psychological symptoms of dementia: the EVI- ment of Alzheimers disease: the Maximizing Independence in
DEM-E randomised controlled clinical trial. International Jour- Dementia (MIND) study. International Journal of Geriatric Psy-
nal of Geriatric Psychiatry, 29, 819827. http://dx.doi.org/ chiatry, 24, 680685. http://dx.doi.org/10.1002/gps.2175
10.1002/gps.4062 Suttanon, P., Hill, K. D., Said, C. M., Byrne, K. N., & Dodd, K. J.
Maayan, N., Soares-Weiser, K., & Lee, H. (2014). Respite care for (2012). Factors influencing commencement and adherence to a
people with dementia and their carers. Cochrane Database of home-based balance exercise program for reducing risk of falls:
Systematic Reviews, 1, Cd004396. http://dx.doi.org/10.1002/ perceptions of people with Alzheimers disease and their care-
14651858.CD004396.pub3 givers. International Psychogeriatrics, 24, 11721182. http://
Nielsen, J. B., Willerslev-Olsen, M., Christiansen, L., Lundbye- dx.doi.org/10.1017/s1041610211002729
Jensen, J., & Lorentzen, J. (2015). Science-based neurorehabili- Suttanon, P., Hill, K. D., Said, C. M., Williams, S. B., Byrne, K.
tation: recommendations for neurorehabilitation from basic sci- N., LoGiudice, D., & Dodd, K. J. (2013). Feasibility, safety and
ence. Journal of Motor Behavior, 47, 717. http://dx.doi.org/ preliminary evidence of the effectiveness of a home-based exer-
10.1080/00222895.2014.931273 cise programme for older people with Alzheimers disease: a

Ohman, H., Savikko, N., Strandberg, T. E., Kautiainen, H., Raivio, pilot randomized controlled trial. Clinical Rehabilitation, 27,
M. M., Laakkonen, M. L., & Pitkala, K. H. (2016). Effects of 427438. http://dx.doi.org/10.1177/0269215512460877
exercise on cognition: The Finnish Alzheimer disease exercise Teodorczuk, A., Welfare, M., Corbett, S., & Mukaetova-Ladinska,
trial: A randomized, controlled trial. Journal of the American E. (2010). Developing effective educational approaches for
Geriatrics Society, 64, 731738. http://dx.doi.org/10.1111/ Liaison Old Age Psychiatry teams: a literature review of the
jgs.14059 learning needs of hospital staff in relation to managing the

12 Journal of Motor Behavior


Exercise for Alzheimers Disease Persons and Caregivers

confused older patient. International Psychogeriatrics, 22, 874 clinical exercise programs. Journal of Cardiopulmonary
885. http://dx.doi.org/10.1017/s1041610209991475 Rehabilitation, 21, 2019.
van Uffelen, J. G., Chinapaw, M. J., van Mechelen, W., & Hop- World Alzheimer Report (2010). The Global Economic Impact of
man-Rock, M. (2008). Walking or vitamin B for cognition in Dementia. https://www.alz.co.uk/research/files/WorldAlzhei
older adults with mild cognitive impairment? A randomised merReport2010.pdf
controlled trial. British Journal of Sports Medicine, 42, 344 Yu, F., & Swartwood, R. M. (2012). Feasibility and perception of
351. http://dx.doi.org/10.1136/bjsm.2007.044735 the impact from aerobic exercise in older adults with
Vant Leven, N., Prick, A. E., Groenewoud, J. G., Roelofs, P. D., Alzheimers disease. American Journal of Alzheimers Disease
de Lange, J., & Pot, A. M. (2013). Dyadic interventions for and Other Dementias, 27, 397405. http://dx.doi.org/10.1177/
community-dwelling people with dementia and their family 1533317512453492
caregivers: a systematic review. International Psychogeriatrics, Yu, F., Thomas, W., Nelson, N. W., Bronas, U. G., Dysken,
25, 15811603. http://dx.doi.org/10.1017/s1041610213000860 M., & Wyman, J. F. (2015). Impact of 6-month aerobic
Vreugdenhil, A., Cannell, J., Davies, A., & Razay, G. (2012). A exercise on Alzheimers symptoms. Journal of Applied
community-based exercise programme to improve functional Gerontology, 34, 484500. http://dx.doi.org/10.1177/073346
ability in people with Alzheimers disease: a randomized 4813512895
controlled trial. Scandinavian Journal of Caring Science, 26,
1219. http://dx.doi.org/10.1111/j.1471-6712.2011.00895.x
Whitlatch, C. J. (2001). Including the person with dementia in
Received December 20, 2015
family care-giving research. Aging & Mental Health, 5, S2022.
Revised July 4, 2016
Woodard, C. M., & Berry, M. J. (2001). Enhancing adherence to
Accepted July 11, 2016
prescribed exercise: structured behavioral interventions in

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