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PII: S0165-1781(17)30916-2
DOI: https://doi.org/10.1016/j.psychres.2017.12.016
Reference: PSY11052
To appear in: Psychiatry Research
Received date: 24 May 2017
Revised date: 10 November 2017
Accepted date: 8 December 2017
Cite this article as: Mingyue Hu, Ping Zhang, Minmin Leng, Chen Li and Li
Chen, Animal-assisted intervention for individuals with cognitive impairment: a
meta-analysis of randomized controlled trials and quasi-randomized controlled
trials, Psychiatry Research, https://doi.org/10.1016/j.psychres.2017.12.016
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Animal-assisted intervention for individuals with cognitive impairment: a
meta-analysis of randomized controlled trials and quasi-randomized controlled trials
Abstract
The aim of this meta-analysis was to systematically examine the efficacy of
animal-assisted intervention (AAI) for cognitive impairment patients. PubMed,
Embase, the Cochrane library, PsycINFO, and Web of Science databases were
searched up to June 2017 to collect studies related to AAI conducted in patients with
cognitive impairment. Five randomized controlled trials (RCTs) and five
quasi-randomized controlled trials (quasi-RCTs) involving 413 participants were
included. Compared with control groups, AAI groups exhibited significantly fewer
behavioral and psychological symptoms of dementia (BPSD), especially depression
and agitation. In both the short and long term, AAI had beneficial effects on BPSD in
cognitive impairment patients. However, no significant improvements were found in
daily living activities, quality of life or cognitive score. The present meta-analysis
showed that AAI can be effective in reducing BPSD in patients with cognitive
impairment.
Keywords: animal-assisted intervention, AAI, cognitive impairment, dementia
1. Introduction
With the accelerating shift toward an aging global population, age-related
diseases have become a major focus of public health issues. According to World
Alzheimer Reports 2015 and 2016 (Prince et al., 2016; Prince et al., 2015), dementia
affects almost 50 million people globally, with a new case of dementia occurring
somewhere in the world every 3 seconds; this number is projected to increase to more
than 131 million by 2050. Furthermore, due to the insidious onset of cognitive
function decline, only 40-50% of those living with dementia in high-income countries
have received a diagnosis, a rate that is unlikely to exceed 5-10% in low- and
middle-income countries (Prince et al., 2015). There are over 100 forms of dementia,
of which the best known is Alzheimer’s disease (AD), accounting for 50-60% of all
cases (Alzheimer’s Disease International, 2017). Although there is currently no cure
for most types of dementia, treatment and support are available.
Behavioral and psychological symptoms of dementia (BPSD) are defined as
signs and symptoms of disturbed behavior, mood, thought or perception that
frequently occur in all stages of dementia but generally become more prevalent as
severity increases (Finkel et al., 1997; Rosenberg et al., 2015). The most common
BPSD in AD are agitation and depression; other BPSD include aggression, sleep
problems, and a variety of socially inappropriate behaviors (Kales et al., 2015;
Lyketsos et al., 2011; Rosenberg et al., 2015). Overall, BPSD are associated with
more rapid progression from mild AD to severe dementia and/or death, and they lead
to a heavy caregiver burden, distress, decreased quality of life and reduced well-being
(Givens et al., 2015; Peters et al., 2015; Wetzels et al., 2010).
Due to the adverse side effects of pharmacological therapies for treating BPSD
(Bierman et al., 2007; Russ, 2014), efforts are focusing on less risky
non-pharmacological interventions. A recent systematic review (Abraha et al., 2017)
showed that various non-pharmacological interventions, such as music therapy and
behavioral management techniques, are effective at reducing BPSD. Among the many
non-pharmacological interventions that exist, AAI (animal-assisted intervention) is a
prescribed, goal-directed approach aimed at ‘training’ the individual in one or more
specific abilities, and the results are promising (Abraha et al., 2017; Edwards and
Beck, 2002; Morrison, 2007). Indeed, studies since 1944 have shown that pets and
humans might have beneficial relationships for each (Bossard, 1944). In March 2013,
the International Association of Human-Animal Interaction Organizations (IAHAIO)
established AAI as a goal-oriented and structured intervention that intentionally
includes or incorporates animals in health, education, and human services for the
purpose of therapeutic gains in humans. AAIs incorporate human–animal teams in
formal human service such as animal-assisted therapy (AAT), animal-assisted
education (AAE), or, under certain conditions, animal-assisted activity (AAA)
(Jegatheesan et al., 2015). In addition to AAI’s underlying positive effects on
cognition, there is also research demonstrating that AAI has positive effects in many
other domains, such as the cardiovascular system, mood management, pain perception,
social contact, autism spectrum disorder, and general health (Barker et al., 2003;
Headey, 2008; McCune et al., 2017; Motooka et al., 2006). The underlying
mechanism can be explained by increased activation of the oxytocin system when
people are in contact with animals (Handlin et al., 2012; Odendaal and Meintjes,
2003). Moreover, the theory of anthropomorphism interprets the undesirable tendency
of humans to treat companion animals in a manner similar to humans as an efficient
way to provide social support and communication (Urquiza-Haas and Kotrschal,
2015). Other theories such as biophilia, attachment, verbal-symbolic system,
motivation, and social support may also be invoked to interpret the effects (Barker et
al., 2003; Beetz, 2017; Heinrichs et al., 2003).
A previous study showed that agitated behaviors significantly decreased while
social interaction significantly increased in dementia patients after AAI (Richeson,
2003). Conversely, another study indicated that although dementia patients had a
good impression of AAI, there was no significant difference in BPSD (Motomura et
al., 2004). In a recent review, the author included 18 articles to assess the effects of
AAI on elderly patients with dementia or psychiatric disorders, concluding that AAI
can reduce agitation and improve social interaction. Nonetheless, due to insufficient
data, there were no conclusions regarding effects of AAI on cognitive functions.
Although that review described encouraging results for AAI, a meta-analysis was not
involved, and the types of included studies were diverse. Moreover, new studies have
since emerged (Bernabei et al., 2013). Overall, some results of AAI have shown
promise, but no definite conclusion has been reached. Hence, the value of AAI in
those with cognitive impairment remains to be further investigated. The aim of the
present review was to conduct a meta-analysis of all studies completed thus far. The
study design encompassed randomized controlled trials (RCTs) and quasi-randomized
controlled trials (quasi-RCTs) that aimed to quantify the effect of AAI across patients
with cognitive impairment.
2. Method
2.1 Literature research
Although we were unable to register the protocol, we still followed the Preferred
Reporting Items for Systematic Reviews and Meta-Analyses (PRISMA) guidelines
(Moher et al., 2009). A comprehensive literature search in the electronic PubMed,
Embase, the Cochrane Library, PsycINFO, and Web of Science databases was
performed by two reviewers (HMY, LMM). To include all possible publications, we
searched all these databases up to June 2017. The language was restricted to English,
but the publication data were not restricted. The key search terms utilized a
combination of MeSH and entry terms (using the PubMed query as an example):
"Cognitive Dysfunction"[Mesh] OR "Cognitive Impairments" OR "Cognitive
Impairments" OR "Mild Neurocognitive Disorder" OR "Neurocognitive Disorder"
OR "Mild Cognitive Decline" OR "Cognitive Disorders" OR "Mental Disorder"[Mesh]
OR "Mental Deterioration" OR "Behavior Disorders" OR "Dementia"[Mesh] OR
"Amentia" OR "Alzheimer’s disease" OR "MCI" OR "Senile Paranoid Dementia" OR
"Familial Dementia", "Animal Assisted Therapy"[Mesh] OR "Pet Therapy" OR
"Assisted Therapy, Animal" OR " Animal Facilitated Therapy" OR "Therapies, Pet
Facilitated" OR "Animal Assisted Intervention" OR "animal-assisted activity",
"Randomized Controlled Trial"[Mesh], "Controlled Clinical Trial" OR "Randomized"
OR "Randomized Controlled Study" OR "Randomly" OR "Trial". Similar strategies
were used to search other databases.
2.2 Inclusion and exclusion criteria
Two reviewers (HMY, LMM) independently reviewed the list of potential
articles produced by the search strategy. Criteria for inclusion and exclusion were
determined a priori. The PICOS approach was used for eligibility criteria. The
inclusion criteria were as follows. (1) Study participants were diagnosed with
cognitive dysfunction, such as mild cognitive impairment, dementia, or Alzheimer’s
disease. (2) The intervention method was AAI. (3) The study was an RCT or a
quasi-RCT. We included quasi-RCTs because we had anticipated that there would be
a dearth of evidence from RCTs. (4) The study results reported details on the effects
of the intervention, or detailed data could be obtained by contacting the corresponding
authors. The exclusion criteria were as follows. (1) The study did not meet all the
PICOS standards. (2) There was no control group. (3) Cognitive dysfunction was
caused by other psychiatric or neurological disease, such as depression, stroke, and
accompanying medical disorders. (4) The publication only reported the protocol.
Missing data regarding outcomes of interest were obtained by contacting the
corresponding authors.
2.3 Study selection
After duplicate studies were eliminated (EndNote X7), titles were first reviewed
for obvious exclusions. After reading the abstract, the full text was reviewed if it was
unclear whether the article should be excluded. Two reviewers (HMY, LMM)
selected articles and extracted data independently and then compared their lists of
articles to ensure that the same studies had been included or excluded. The two
reviewers resolved any discrepancy by discussion. If discrepancies could not be
resolved, a third person (ZP) joined the discussion on how to classify the articles.
2.4 Data extraction
Two reviewers (HMY, LMM) independently extracted data from the included
studies and completed an a priori data table. The table of extracted data was reviewed
by a third person (ZP) to ensure that there were no errors. A standardized extraction
form was created to record the following data from the studies: author and year, types
of analysis, population, intervention type, intervention methods, allocation, mean age,
intervention format, follow-up times, frequency of intervention, drop-out, assessment
for level of cognitive impairment and outcome measures. The primary outcome was
BPSD; secondary outcomes were activities of daily living, cognitive state and quality
of life.
2.5 Quality assessment
The quality of the RCTs in six areas of bias known to affect clinical outcomes
(selection bias, performance bias, detection bias, attrition bias, reporting bias and
other bias) was assessed using the “Risk of Bias Tool” recommended by Cochrane
Handbook for Systematic Reviews of Interventions (Higgins and Green, 2011). The
methodological index for non-randomized studies (MINORS) was applied to further
assess the quality of each non-randomized study. The maximum global score for
comparative studies is 24 (Slim et al., 2003). All included studies were independently
assessed, and scores were determined via consensus.
2.6 Statistical analysis
The SMD (standardized mean difference) was calculated if there was variation in
the scale used by the trials. We pooled the results of trials using a fixed-effects model
when the heterogeneity test showed p > 0.05 and I2 < 50%. Otherwise, a
random-effects model and subgroup analysis were used to analyze the sources of
heterogeneity; the weight given to each study was based on the inverse of the variance.
All reported probabilities (p values) were two-sided, with p < 0.05 considered to be
statistically significant.
3. Results
3.1. Literature search and study characteristics
A total of 975 articles were identified from the four databases; 102 articles
remained after duplicate documents were removed and titles or abstracts were
reviewed. After reviewing the full text, 10 articles were included in the meta-analysis.
The selection process is shown in Fig. 1. Among the 10 articles, five each are RCTs
(Bono et al., 2015; Friedmann et al., 2015; Menna et al., 2016; Olsen et al., 2016a;
Olsen et al., 2016b) and quasi-RCTs (Churchill et al., 1999; Kanamori et al., 2001;
Majic et al., 2013; Moretti et al., 2011; Nordgren and Engström, 2014b). The detailed
characteristics of the included studies are presented in Table 1. Most of the
participants had a diagnosis of dementia, and dogs were used in most of the included
studies. The control groups in nine studies were exposed to the same conditions as the
corresponding intervention groups, except for the implementation of AAI in the latter.
However, in one study, the control group underwent reminiscence therapy, whereas
the intervention group received AAI. Figures on secondary outcomes are not
displayed.
Fig. 1. PRISMA flowchart of search and selection guidelines.
5. Limitation
Our meta-analysis is limited in that we searched only the English literature. Thus,
some studies may have been missed. Due to the dearth of evidence from RCTs, we
also included quasi-RCTs. The small sample size included is another main limitation,
but we believe that with the development of non-pharmacological interventions, an
increasing number of researchers will explore the effectiveness of AAI in cognitive
impairment patients.
Funding sources
This research did not receive any specific grants from funding agencies in the
public, commercial, or not-for-profit sectors.
Conflict of interest
The authors declare no conflicts of interest.
Acknowledgment
We thank all the authors of the included papers.
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Alzheim Day-care EC: dog Dogs and - - EC: 7 81.4 Individua 2 Once 0% MMSE Mini-Mental
er’s center and cat cats. CC: 12 89.47% l sessions: every State
Kanamo disease, therapy baseline, two Examination/
ri et al. vascular interventi 3 months weeks, Nishimura’s
2001 dementia on 12 ADL/Behavio
quasi-R CG: weeks, ral Pathology
CT routine in
care Alzheimer’s
Disease
Mild and Alzheimer’ EG: dog Dog: Structured Reintroduci EG: 16 75.2 Group 2 Once a 0% MMSE Global
moderate s daycare therapy Labrador activities: ng the dog CG: 7 75% sessions: week, 6 Deterioration
Alzheim center interventi retriever. To stimulate to each baseline, months, Scale/
er’s on cognitive patient and 6 months 45 mins Mini-Mental
disease CG: functions helping the State
Menna
routine including patient Examination
et al.
care attention, develop
2016
language spatial-temp
RCT
skills, and oral
spatial-temp orientation,
oral structured
orientation. activity with
the dog.
Minor Alzheimer EG: dog Dogs: 2 Specific & - EG: 16 80.2 Individua 2 Once 25% MMSE Barthel Index
and mild evaluation therapy Border standard identificatio CG: 16 66.67% l sessions: every
AD unit interventi Collie; 1 activities: n of the dog baseline, two
on Golden To stimulate breed 8 months weeks, 8
CG: Retriever cognitive looking at months,
routine s; 1 functions, illustrations, 60
care Weimara communicat recalling of minutes
ner. ion with personal
peers, and events with
manual animals,
Bono et
skills. learning
al. 2015
basic
RCT
commands,
rememberin
g some play
with the
animal.
-learning
the body
language
of the
animal.
Abbreviations: RCT, randomized controlled trials; quasi-RCT: quasi-experimental studies; EG, experimental group; CG: control group. DSM-IV: Diagnostic and Statistical
Manual of Mental Disorders, Fourth Edition; BDBRS: Burke Dementia Behavioral Rating Scale.
Table 2. Quality assessment with the Cochrane Collaboration’s Risk of Bias Tool and MINORS.
RCT quasi-RCT
Intention-t Incomplete Selective Other
Studies Sequence Allocation Blinding of Assessor MINORS
o-treat outcome outcome potential
generation concealment participants blinding score
analysis data reporting bias
Olsen et al. (2016) L L L H L L L L
Nordgren et al. (2014) 17
Majic et al. (2013) 21
Olsen et al. (2016) L L L U L L L L
Friedmann et al. (2015) L L L L L L L L
Moretti et al. (2011) 19
Churchill et al. (1999) 18
Kanamori et al. (2001) 21
Menna et al. (2016) H H U U L L L L
Bono et al. (2015) L L L L L L L L
Abbreviations: RCT, randomized controlled trials; quasi-RCT: quasi-experimental studies; L, low risk; H, high risk; U, unclear risk.
Hights:
Using meta-analysis to examine the efficacy of Animal-assisted intervention (AAI) for cognitive impairment patients.