Horticultural Therapy has Beneficial Effects on Brain Functions in Cerebrovascular Diseases
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2. Keywords
Horticultural therapy (HT), fMRI, Supramarginal gyrus (SMG), Visual area, Cerebrovascular
disease, Functional independence measure (FIM)
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1. INTRODUCTION
Horticulture is defined as the art and science of
growing flowers, fruits, vegetables, and trees
and shrubs resulting in the development of the
minds and emotions of individuals and the
enrichment and health of communities
civilization [1]. Horticultural therapy (HT) is a
remedial process in which plants and
gardening activities are used to improve the
body, mind, and spirits of people [2]. HT is
thought to be an effective and beneficial
treatment for people of all ages, backgrounds,
and abilities. The therapeutic benefits of
peaceful garden environments have been
understood since ancient times. In the 19th
century, Dr. Benjamin Rush, a signer of the
Declaration of Independence considered to be
the “Father of American Psychiatry,” reported
that garden settings held curative effects for
people with mental illness [2].
Soderback reviewed the literature on HT and
described its use in rehabilitation following
brain damage [3]. He showed that HT affected
emotional, cognitive and/or sensory motor
functional improvement and increased social
participation, health, well-being and
satisfaction with life. Jones and Haight
reviewed articles on the use of the natural
environment in the form of plants or plant
material as therapeutic interventions [4]. They
showed that there was a beneficial relationship
between humans and the natural environment
in the current therapeutic uses.
Although HT has been strongly advocated, its
effect is less established. Most papers on HT
have been reported from the view of
occupational therapy and nursing care.
Therefore, the effectiveness of these
interventionist approaches from the medical
point of view remains to be proved, and it
would have been desirable to perform
subjective assessment of the approaches.
Ulrich [5] reported the positive influence of
nature on patients in the hospital. Surgical
patients assigned to rooms with windows
looking out on a natural scene had shorter
postoperative hospital stays, received fewer
negative evaluative comments in nurses’ notes,
and took fewer potent analgesics than patients
in similar rooms with windows facing a brick
wall.
Ulrich et al. showed that influences of nature
could reduce the emotional, attentional, and
physiological aspects of stress using the
Zuckerman Inventory of Personal Reactions
(ZIPERS), which is questionnaire using affects
(subjective aspects of feeling or emotion) to
assess feelings [6]. Ulrich et al. also measured
physiological reactions using an
electrocardiogram (ECG), pulse transit time,
spontaneous skin conductance response, and
frontalis muscle tension using an
electromyogram (EMG), and documented
physiological changes related to recovering
from stress, including low blood pressure,
reduced muscle tension, and differences in
cardiac responses.
Soderback indicated that HT could categorize
four different intervention approaches:
“virtual”, “viewing”, “interaction”, and
“action” [3]. In the routine occupational or
physical therapies, a patient executes “actions”
only according to the therapist’s instruction.
On the other hand, in HT the patient can
objectively imagine the growth of vegetation in
his or her own way, actually see that the
vegetation is growing and simultaneously
perform his/her own activities as
rehabilitations. Ulrich suggested that the
benefits of nature such as trees and other
vegetations were positive influences on
emotional and physiological states of the
people, and the benefits came from visual
encounters with nature from urban planning
point of view [7].
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We have investigated the effectiveness of HT
on the hypotheses that (1) imagination,
observation, and participation in growing
vegetation makes a positive effect on a
patient’s actual activities, and (2) viewing
colorful vegetation in nature under sunlight
improves the visual abilities in the brain. To
prove these hypotheses, we designed
experimental fMRI protocols that reveal
visual, recognitional, motor, and emotional
functions/abilities. In addition, we used the
questionnaires to measure the activities of
daily living (ADL) and the mental mood of the
patients.
The aim of this paper is to assess whether
horticulture therapy is effective for
improvement of brain functional activity in
brain-damaged patients from the medical point
of view.
2. METHODS
Case #1 was a 75-year-old right-handed male
patient who had suffered a right internal
carotid artery occlusion and had left
hemiplegia and dysarthria. Case #2 was a
42-year-old right-handed male patient who had
suffered a left cerebral infarction and had right
hemiplegia and aphasia. Case #3 was a
60-year-old right-handed female patient who
had suffered a right anterior cerebral artery
occlusion and had left hemiplegia. Case #4 was
a 56-year-old right-handed male patient who
had suffered right thalamic bleeding and had
left hemiplegia. Case #5 was a 68-year-old
right-handed female patient who had suffered
bleeding in the right frontal lobe and had left
hemiplegia and dysarthria. Written informed
consent was obtained from all subjects and
patients after a detailed briefing of the
experimental purposes and protocol.
The functional independence measure (FIM) is
an evaluation tool used to quantify the ability
of patients to enter rehabilitation treatment and
to chart their progress until discharged into the
community or to another facility [8]. The FIM
is an assessment instrument rating a patient’s
level of function in 18 physical and mental
tasks that represent the basic ADL. The total
score rage is from 18 as a perfect dependent to
126 as a perfect independent. There are 13
motor items ranging from 13 to 91 (eating,
grooming, bathing, dressing the upper body,
dressing the lower body, toileting, bladder and
bowel management, transfers to bed/chair,
toilet and tub/shower, walking/wheelchair, and
stair climbing) and 5 cognitive items ranging
from 5 to 35 (comprehension, expression,
social interaction, problem-solving, and
memory). Each patient’s FIM was scored at the
beginning and ending of the HT to assess levels
of ADL.
All patients were evaluated as to whether or not
they suffered from depression, based on the
DSM IV-TR (Diagnostic and Statistical
Manual of Mental Disorders Fourth Edition
TR) criteria. A medical doctor also evaluated
mental status using indicators such as mood,
motivation, communication, and expression
with an observational study. Moreover, the
Self-Rating Depression Scale (SDS) was used
to evaluate not only “depression” but also the
“patients’ depressive states” influenced by
their mental mood. All patients were rated
using the SDS in scoring only 20 items of the
questionnaire. The relationship between mean
SDS score of patients and diagnosis of major
depression was reported [9]. This report
showed that the SDS had a sensitivity of 80
percent and specificity of 88 percent for
detecting patients with major depression. The
SDS was performed before and after the HT to
assess changes in depressive state. The SDS
score ranged from 20 to 80. A score of more
than 50 is supposed to show the possibility of a
severe depressive state (possibility of severe
major depression is high), and a score of 40-50
is supposed to show a moderate depressive
state (possibility of a moderate depression is
high).
Five patients were invited to participate in HT
designed by horticultural therapists for a month
in addition to the routine medical and physical
treatment given in Ishikawa Hospital. The
purpose of HT program was to bring about
effects in mental healing, cognitive
re-organization, and training of sensory motor
function. The HT consisted of three steps:
imagining nature, designing a flowerbed, and
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actually planting a tree. The therapists
instructed the patients in all these processes.
Table 1 shows an example of the HT program
for each session in Case #2. The subject was
able to experience the whole process of
growing flowers including designing a garden,
creating a planting plan, preparing a flowerbed
for seeding, seeding, watering, and making
pressed flowers from his/her own flowers from
the flowerbed. It took about a month to
complete this process. Figure 7 in the
Appendix shows some pictures of scenes from
HT programs in Table 1.
Table 1. Horticultural Therapy Program for Case #2.
Session Description of Programs
1 Flowerbed preparation (weeding)
2 Flowerbed preparation (weeding)
3 Readying the soil
4 Creating a planting plan for flowerbeds
5 Briefing on future activities and selecting seedling
6 Cultivating
7 Terrarium making
8 Planting to the flowerbed according to plan
9 Planting seedling to flowerbed
10 Soil readying, watering, and dividing seedling
11 Watering, and picking up withered flowers
12 Doing crafts using moss, and watering
13 Watering
14 Planting vegetables, weeding, dividing
15 Making name plates for the flowerbeds
16 Watering and weeding
17 Watering, weeding, and appreciating other patients’ flowerbeds
18 Making a container garden
19 Making pressed flowers
20 Working in the garden
Functional magnetic resonance imaging
(fMRI) under recognition tasks was measured
before and after HT. The experimental fMRI
protocols were designed to reveal the
hypotheses on the effectiveness of HT as we
mentioned in Introduction. In the other words,
viewing, recognition, movement, and the
emotional functions/abilities of the patients
were trying to be clarified. Subjects performed
two kinds of tasks, in which they fixated on an
image and categorized it into a “pleasant”
image or an “unpleasant” image based on the
previous instructions for each trial. Images
included two kinds of emotional photos: a
girl’s smiling facial expression (pleasant) or an
angry facial expression (unpleasant) in task 1,
and a healthy forest landscape (pleasant) or a
dying forest (unpleasant) in task 2. Each trial
involved the consecutive presentation of the
photos for 2 seconds proceeded by a crosshair
image for 20-30 seconds (Figure 1). Subjects
were instructed to fixate on a photo, and judge
whether or not the photo was pleasant by
moving their right index finger, or unpleasant
by moving both the right index and middle
fingers. Each task consisted of 20 blocks, half
of which were pleasant, and half of which were
unpleasant. Photos were randomly ordered
within each task. The duration of each task was
516 seconds. In the study, five patients
performed this experimental protocol using the
fMRI scanner before and after HT.
5. 1 block
20 blocks (516 sec)
Figure 1. Schematic diagram of fMRI measurement task.
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MR images were acquired on a 1.5 Tesla
SIGNA CV/i scanner (GE Medical Systems,
Milwaukee, WI). After initial acquisition of T1
structural images, echo planar imaging (EPI)
was used to acquire data sensitive to the BOLD
signal at a repetition time (TR) of 2000 ms and
an echo time (TE) of 40 ms. High-resolution
T1 images were acquired to aid in anatomic
normalization. The spatial resolution of BOLD
images was set by a 64 by 64 voxel matrix
covering 260 × 260 mm2 with a 5 mm slice
thickness. The image gave an in-plane
resolution of 4.06 by 4.06 mm2. Twenty axial
slices with 5 mm thickness were acquired to
cover the whole brain. During the data
acquisition, 258 images (phases) per slice were
obtained in 516 seconds (= 258 x 2.0 sec). This
produced a 4-D dataset consisting 64 × 64 × 20
× 258 voxels, in which a voxel is referred to as
(x, y, z, t).
Data analysis was performed with the
Statistical Parametric Mapping analytic
package (SPM5, Wellcome Department of
Cognitive Neurology, London, UK). In the
first step, we identified regions that showed
significant activation during the pleasant or
unpleasant images compared to those during
the crosshair image. Activations were reported
if they exceeded p < 0.05 (uncorrected) on the
single voxel level in each patient. We showed
images of the activation areas before and after
HT. In the next step, the differences between
the images before and after HT were calculated
using the t-statistic, and contrast maps were
generated for each patient. We extracted the
increased areas in activity after HT compared
to those before HT in each patient (p < 0.1). In
the figures the areas in which activation
decreased or did not change after HT were
omitted.
3. RESULTS
The doctors’ clinical observations of the whole
process left the impression that all the patients’
expressions and motivation had improved after
the HT.
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Table 2 shows date information of subjects:
onset of disorders, beginning of general
rehabilitation, beginning of HT, first, before
HT and second, after HT measurement of
fMRI. HT began 6 months after the onset of
disorder in Case #1 and 2 years and 8 months
after the onset in Case #2 although HT began
2-3 months after the onsets in Cases #3, #4, and
#5.
Table 2. Date Information of subjects
Case #1 Case #2 Case #3 Case #4 Case #5
Onset of disorder 12/6/2003 10/1/2001 6/28/2004 6/21/2004 1/26/2005
Beginning of rehabilitation 4/22/2004 4/2/2002 7/27/2004 8/14/2004 3/11/2005
Beginning of HT 6/8/2004 6/8/2004 9/25/2004 9/25/2004 4/4/2005
First trial 6/1/2004 6/1/2004 fMRI 9/25/2004 9/25/2004 4/4/2005 Second trial 7/16/2004 7/16/2004 10/25/2004 10/25/2004 5/19/2005
Table 3 shows the total scores of FIM before
and after the HT. The scores of motor and
cognitive items are also shown in the table. The
total scores of all the cases after HT are
significantly larger than those before HT
(paired T test: p < 0.03). The scores on motor
items of all cases after HT are also significantly
larger than those before HT (paired T test: p <
0.03), while there are no significant differences
between the scores on cognitive items before
and after HT (paired T test: p = 0.16).
The medical doctor ruled out all the patients
except Case #2 as depression based on a
diagnosis of DSM IV-TR criteria from the
clinical point of view. Table 4 shows the scores
of SDS before and after HT. Case #2 before
and after HT is categorized into a severe
depressive state, and Case #4 before and after
HT and Case #5 after HT are categorized into a
moderate depressive state as assessed by the
SDS score. However, there are no significant
differences between the SDS scores of all cases
before and after HT (paired T test: p = 0.88).
Table 3. Scores of FIM
Case #1 Case #2 Case #3 Case #4 Case #5
Total score 62 91 86 64 59
Before HT Motor items 38 72 53 39 33
Cognitive items 24 19 33 25 26
Total score 92 89 116 114 104
After HT Motor items 68 71 81 85 75
Cognitive items 24 18 35 29 29
* p < 0.03
Table 4. Scores of SDS
Case #1 Case #2 Case #3 Case #4 Case #5
Before HT 39 57 38 47 36
After HT 37 61 32 45 44
p = N.S.
Figures 3 to 6 show the activated areas during
the cognitive tasks before and after HT (p <
0.05), and the increased areas in activation
after HT, compared to the level before HT (p <
0.1) in Cases #1 through #5, respectively.
Figure 3 shows that the bilateral visual areas
(Brodmann areas: BAs 17 and 18), the right
motor area (BA 4), and the left supplementary
motor area (SMA) (BA 6), the right sensory
areas (BAs 3 and 2), the right supramarginal
*
*
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gyrus (SMG) (BA 40), and the left cerebellum
were activated after HT to compare to their
activation level before HT in Case #1. Figure 3
shows that the bilateral visual areas (BAs 17
and 18), the left motor area (BA 4), left SMA
(BA 6), the left sensory areas (BA 2), the
bilateral temporal pole (BA 38), the right
fusiform gyrus (BA 37), and the right
cerebellum were activated in Case #2. Figure 4
shows that the bilateral visual areas (BAs 17
and 18) and the left cerebellum were activated
in Case #3. Figure 5 shows that the left visual
areas (BAs 17 and 18) and the right prefrontal
areas (BAs 10, 11, and 47), the sensory area
(BA 1), the left SMG (BA 40), the bilateral
middle temporal gyrus (BA 21), the right
inferior temporal gyrus and fusiform gyrus
(BA 20), the right temporal pole (BA 38), and
the bilateral cerebellum were activated in Case
#4. Figure 6 shows that the bilateral cerebellum
was activated in Case #5.
Figure 2. Activated areas of Case #1 before HT (left) and after HT (middle) (p < 0.05), and
increased areas in activation after HT, compared to the activation level before HT (right) (p <
0.1).
Figure 3. Activated areas of Case #2 before HT (left) and after HT (middle) (p < 0.05), and
increased areas in activation after HT, compared to the activation level before HT (right) (p <
0.1).
8. Figure 4. Activated areas of Case #3 before HT (left) and after HT (middle) (p < 0.05), and
increased areas in activation after HT, compared to the activation level before HT (right) (p <
0.1).
Figure 5. Activated areas of Case #4 before HT (left) and after HT (middle) (p < 0.05), and
increased areas in activation after HT, compared to the activation level before HT (right) (p <
0.1).
Figure 6. Activated areas of Case #5 before HT (left) and after HT (middle) (p < 0.05), and
increased areas in activation after HT, compared to the activation level before HT (right) (p <
0.1).
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Table 5 shows a summary of the activated
areas after HT in each patient (Cases #1
through #5). In the table, the letter “A”
represents an increase of activation after HT,
compared to the level before HT (p < 0.1). The
letters “O”, “F”, “P”, “T”, and “C” represent
occipital, frontal, parietal, temporal, and
cerebellum, respectively. Each area number
shows the Brodmann area in occipital, frontal,
parietal, and temporal lobes. “L” and “R” show
left and right hemispheres, respectively. The
column in gray shows a disabled side in each
patient.
The visual areas (BAs 17 and 18), the motor
area (BA 4), SMA (BA 6), the prefrontal areas
(BAs 10, 11, and 47), the sensory areas (BAs 3,
1, and 2), SMG (BA 40), the middle temporal
gyrus (BA 21), the inferior temporal gyrus and
fusiform gyrus (BAs 20 and 37), the temporal
pole (BA 38), and the left cerebellum were
activated after HT to compare to the activation
level before HT. These events occurred in an
unaffected side of cerebellum in all patients
and the occipital area in all but one.
Table 5. Increased areas in activation after horticultural therapy in each patient
(Cases #1 through #5).
The letter “A” represents increased areas in activation after HT, compared to the level before
HT (p < 0.1). The letters “O”, “F”, “P”, “T”, and “C” represent occipital, frontal, parietal,
temporal, and cerebellum, respectively. Each area number shows the Brodmann area in
occipital, frontal, parietal, and temporal lobes. “L” and “R” show left and right hemispheres,
respectively. The column in gray shows a disabled side in each patient.
Case #1 #2 #3 #4 #5
Area # L R L R L R L R L R
17 A A A A A A A
O
18 A A A A A
4 A A
6 A A
10 A
11 A
F
47 A
3 A
1 A
2 A A
P
40 A A
21 A A
20 A
38 A A A
T
37 A
C A A A A A A A
p < 0.1
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4. DISCUSSION
The effects of HT in the brain functions of
cerebrovascular diseases were investigated
using fMRI studies and questionnaires. The
results in this paper show an increase of
activations in the visual area, the motor area,
SMG, sensory area, SMA, the prefrontal area,
the inferior and middle temporal gyrus, the
fusiform gyrus, the temporal pole, and the
cerebellum. Recent fMRI studies reported that
mainly recovered areas after the stroke using
the routine rehabilitation were the sensory
area, motor area, premotor area (PMA),
cerebellum, SMA, and parietal areas[10, 11,
12]. Our results show that the visual area, the
inferior temporal gyrus, the fusiform gyrus,
and the SMG were activated in addition to the
ordinarily recovering areas. HT could cause
these differences in the process of recovering
brain activities.
The fusiform gyrus and the inferior temporal
cortex are considered to be related to human
color processing [13, 14, 15]. These color
processing areas and visual areas increased
their activities after HT. This result shows that
processes of HT: “virtual” elements such as
creating a planting plan (Figure 7-A),
“viewing” nature (Figures 7-B to 7-G),
“interaction”, and “action” through doing
gardening jobs, under the sunlight, could have
an effect on the color processing areas and
visual areas in the brain. Our results show that
viewing and concerning color processing
might be essential in the effectiveness of HT.
SMG is well known to play a roll in perception
and discernment in the association area [16].
SMG might mediate a nonspatial attentional
function, such as stimulus detection or alerting
other areas to the appearance of a salient
stimulus irrespective of a precise spatial
location [17, 18]. The results presented here
demonstrate that this kind of network area of
the brain in addition to the motor, sensory, and
visual areas increased its activities after HT.
These findings suggest that the improved
motor and sensory skills in the patients could
be associated with reactivation or
compensation of a physiological network such
as SMG in the brain. Our results show that HT
contributes to their activations.
HT can stimulate parts of brain not always
evoked through routine physical rehabilitation.
HT can compensate for routine physical
rehabilitation and help to improve damaged
brain function.
Our results from one questionnaire showed that
the daily activities in total score and motor
items of FIM significantly improved.
Compares with other therapies such as routine
physical therapy, occupational therapy, music
therapy, and animal therapy, HT has the
following features: (1) a patient can objectively
observe vegetation growing, (2) the patient can
intervene in the process of growing vegetation
from seeds, (3) the patient can actually see the
results of his/her efforts when the vegetation
has grown, (4) the patient can amicably share
his/her achievements with other people.
Spontaneous rehabilitation of the patient could
be encouraged by repeated successful
experiences of growing plants. We think that
these features can help the patient improve
his/her ADL.
Our results from the other questionnaire, SDS,
showed that mood was not changed
remarkably in most patients. For mental mood
or emotional improvement, a tailor-made
program of HT during a long period would be
needed.
Another feature of HT is its beginning or onset
time. Case #1 and Case #2 began 6 months and
2 years and 8 months, respectively after the
onset (Table 2). In spite of the long time after
the onset of disorders, Case #1’s and Case #2’s
brain function activated after HT. This
activation shows that HT can effectively
improve brain function even if HT begins
several months or years after the onset. The
time of the onset of disorders therefore, might
be irrelevant, because HT contains multi-functional
elements, and the patient can move
from fundamental activities to complex
activities.
We report here changes in brain function of
five cases after HT. Now we are planning to
11. 179
target a larger number of patients who will
participate in HT and we will investigate their
brain activities through a quantitative
statistical analysis in the future. We are also
planning to compare patients given HT with
patients not given HT. These five case studies
proved the possibility that HT accelerates an
improvement of activities in the “visual and
color processing area” and the “association
area” of brains in the patients with
cerebrovascular diseases. Moreover, HT can
also help to contribute to improvement in the
patients’ ADL. We think the research
presented here is necessary to accomplish
further studies.
ACKNOWLEDGEMENTS
This work is partially supported by a
Grant-in-Aid from the Ministry of Education,
Culture, Sports, Science and Technology, JP
(19500393).
APPENDIX
A. Creating a planting plan B. Selecting seedlings for flowerbeds
C. A flowerbed before weeding D. A flowerbed soon after planting
12. E. A flowerbed a month after planting
F. Flowerbeds and flowerpots planted by patient
G. Watering
Figure 7. Scenes from Horticultural Therapy Programs
180
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AUTHOR INFORMATION
Yuko Mizuno-
Matsumoto received
the M.D. degree from
Shiga University of
Medical Science,
Japan, in 1991, and
Ph.D. degrees in
Medical Science and
Engineering from
Osaka University,
Japan, in 1996 and 2003, respectively. From
1999 to 2000, she was a Post-Doctoral
14. 182
Research Fellow in the Department of
Neurology, Johns Hopkins University,
Baltimore, MD. Since 2004, she has been an
Associate Professor in the Graduate School of
Applied Informatics, University of Hyogo,
Kobe, Japan. She is a Certifying Physician of
The Japanese Society of Psychiatry and
Neurology, and a Certifying Physician &
Electroencephalographer of Japanese Society
of Clinical Neurophysiology.
Syoji Kobashi is an
associate professor in
Graduate School of
Engineering, University
of Hyogo, Japan. His
research interests
include soft computing
approach to medical
signal/image processing
and human brain functions. He received the
Joseph F. Engelberger Best Paper Award at the
2nd World Automation Congress in 2000, the
IEEE EMBS Japan Young Investigators
Competition from IEEE EMBS Japan Chapter
in 2003.
Yutaka Hata is a
professor in Graduate
School of Engi-neering,
University of
Hyogo, Japan. He
spent one year in
BISC Group, Uni-versity
of California
at Berkeley from
1995 to 1996 as a visiting scholar. He is the
Founding Editor-in-Chief of the International
Journal of Intelligent Computing in Medical
Sciences and Image Processing, and the re-gional
editor of Intelligent Automation & Soft
Computing. He received Joseph F. Engelber-ger
Best Paper Award and Best Paper Award at
the WAC2000, USA. and WAC Contribution
Award, at 2002, 2004 and 2006.
Osamu Ishikawa is a
Vice-President of
Ishikawa Hospital,
Japan. He is also the
President of A Geriatric
Health Services
Facility, SEIYOU. His
research interests are in
medical imaging,
surgery systems, and
care systems for elderly persons.
Fusayo Asano, Ph.D.
in Agriculture, is a
professor of Labora-tory
of Plant Assisted
Therapy, Department
of Bio- therapy, faculty
of Agriculture, Tokyo
University of Agri-culture,
Japan. She is a
Horticultural Therapist Master at the American
Horticultural Therapy Association and re-ceived
Rhea McCandliss Professional Service
Award in 2004 for her contribution to the field
of horticultural therapy, especially in educa-tion.
She is a founding director of the Japanese
Society of People-Plant Relationships and
Japanese Horticultural Therapy Association.