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Effect of forest bathing trips on human immune function

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Abstract

In Japan, a forest bathing trip, called "Shinrinyoku" in Japanese, is a short, leisurely visit to a forest; it is regarded as being similar to natural aromatherapy. This review focuses on the effects of forest bathing trips on human immune function. Beginning in 2005, adult Japanese individuals, both male and female, participated in a series of studies aimed at investigating the effect of forest bathing trips on human immune function. The subjects experienced a 3-day/2-night trip to forest areas, and blood and urine were sampled on days 2 (the first sampling during each trip) and 3 (the second sampling during each trip), and on days 7 and 30 after the trips. Natural killer (NK) activity, the numbers of NK, granulysin-, perforin-, and granzymes A/B-expressing lymphocytes in the blood, and the concentration of urinary adrenaline were measured. The same measurements were made before the trips on a normal working day as a control. The mean values of NK activity and the numbers of NK, granulysin-, perforin-, and granzymes A/B-expressing cells on forest bathing days were significantly higher than those on the control days, whereas the mean values of the concentration of urinary adrenaline on forest bathing days were significantly lower than that on the control days in both male and female subjects. The increased NK activity lasted for more than 30 days after the trip, suggesting that a forest bathing trip once a month would enable individuals to maintain a higher level of NK activity. In contrast, a visit to the city as a tourist did not increase NK activity, the numbers of NK cells, or the level of intracellular granulysin, perforin, and granzymes A/B. These findings indicate that forest bathing trips resulted in an increase in NK activity, which was mediated by increases in the number of NK cells and the levels of intracellular granulysin, perforin, and granzymes A/B.
SPECIAL FEATURE The Trends on the Research of Forest Bathing in Japan,
Korea and in the World
Effect of forest bathing trips on human immune function
Qing Li
Received: 14 July 2008 / Accepted: 6 December 2008 / Published online: 25 March 2009
ÓThe Japanese Society for Hygiene 2009
Abstract In Japan, a forest bathing trip, called ‘‘Shin-
rinyoku’’ in Japanese, is a short, leisurely visit to a forest; it
is regarded as being similar to natural aromatherapy. This
review focuses on the effects of forest bathing trips on
human immune function. Beginning in 2005, adult Japa-
nese individuals, both male and female, participated in a
series of studies aimed at investigating the effect of forest
bathing trips on human immune function. The subjects
experienced a 3-day/2-night trip to forest areas, and blood
and urine were sampled on days 2 (the first sampling
during each trip) and 3 (the second sampling during each
trip), and on days 7 and 30 after the trips. Natural killer
(NK) activity, the numbers of NK, granulysin-, perforin-,
and granzymes A/B-expressing lymphocytes in the blood,
and the concentration of urinary adrenaline were measured.
The same measurements were made before the trips on a
normal working day as a control. The mean values of NK
activity and the numbers of NK, granulysin-, perforin-, and
granzymes A/B-expressing cells on forest bathing days
were significantly higher than those on the control days,
whereas the mean values of the concentration of urinary
adrenaline on forest bathing days were significantly lower
than that on the control days in both male and female
subjects. The increased NK activity lasted for more than
30 days after the trip, suggesting that a forest bathing trip
once a month would enable individuals to maintain a
higher level of NK activity. In contrast, a visit to the city as
a tourist did not increase NK activity, the numbers of NK
cells, or the level of intracellular granulysin, perforin, and
granzymes A/B. These findings indicate that forest bathing
trips resulted in an increase in NK activity, which was
mediated by increases in the number of NK cells and the
levels of intracellular granulysin, perforin, and granzymes
A/B.
Keywords Forest bathing Granulysin
Granzyme NK activity Perforin
Introduction
What is a forest bathing trip?
The forest environment has been enjoyed by humans for a
long time because of the quiet atmosphere, beautiful
scenery, mild climate, and clean fresh air in forests. In
Japan, a forest bathing trip, called ‘‘Shinrinyoku’’ in
Japanese, is a short, leisurely visit to a forest and is
regarded as being similar to natural aromatherapy. A forest
bathing trip involves visiting a forest for relaxation and
recreation while breathing in volatile substances, called
phytoncides (wood essential oils), which are antimicrobial
volatile organic compounds derived from trees, such as
a-pinene and limonene [14]. Incorporating forest bathing
trips into a good lifestyle was first proposed in 1982 by the
Forest Agency of Japan. It has now become a recognized
relaxation and/or stress management activity in Japan
[26]. The results of a study using the Profile of Mood
States (POMS) test demonstrated that a forest bathing trip
significantly increased the score for vigor and decreased
the scores for anxiety, depression, and anger [2,4].
Habitual forest bathing may help to decrease the risk of
psychosocial stress-related diseases [6]. Because forests
Q. Li (&)
Department of Hygiene and Public Health,
Nippon Medical School, 1-1-5 Sendagi,
Bunkyo-ku, Tokyo 113-8602, Japan
e-mail: qing-li@nms.ac.jp
URL: http://forest-medicine.com
123
Environ Health Prev Med (2010) 15:9–17
DOI 10.1007/s12199-008-0068-3
occupy 67% of the land in Japan [7], forest bathing is
easily accessible, and according to a public opinion poll
conducted in Japan in 2003, 25.6% of respondents had
participated in a forest bathing trip, indicating its popu-
larity in Japan [6]. Moreover, forest bathing is possible in
similar environments throughout the world.
Effect of phytoncides (essential oils)
from trees on human immune function
To investigate the effect of a forest bathing trip on human
immune function, the effects of phytoncides on human
natural killer (NK) activity and intracellular levels of per-
forin, granzyme A (GrA), and granulysin (GRN) in NK
cells were studied in vitro. NK cells have been reported to
kill tumors or virus-infected cells through the release of
perforin, granzymes, and GRN via the granule exocytosis
pathway [812]. Li et al. [1] incubated NK-92MI cells, an
interleukin-2-independent human NK cell line, in the
presence of phytoncides, such as a-pinene, 1,8-cineole,
d-limonene, and essential oils extracted from trees
including Japanese cedar (Cryptomeria, Sugi in Japanese)
and Chamaecyparis obtuse (Hinoki in Japanese), for 48–
144 h and then measured NK activity and the intracellular
levels of perforin, GrA, and GRN [1]. They found that
phytoncides significantly increased the cytolytic activity of
NK-92MI cells in a dose-dependent manner and signifi-
cantly increased the intracellular levels of perforin, GrA,
and GRN in NK-92MI cells. Phytoncides also partially, but
significantly, restored the decreased human NK activity
and the decreased perforin, GrA, and GRN levels in
NK-92MI cells induced by dichlovos, an organophospho-
rus pesticide. Pretreatment with phytoncides partially
prevented dichlovos-induced inhibition of NK activity.
Taken together, these data indicate that phytoncides sig-
nificantly enhance human NK activity and that this effect is
at least partially mediated by the induction of intracellular
perforin, GrA, and GRN [1]. Komori et al. [13] reported
that the citrus fragrance found in forests affected human
endocrine and immune systems, based on the measurement
of urinary cortisol and dopamine levels, NK activity, and
CD4/8 ratios. da Silva et al. [14] found that volatile oil
from Zanthoxylum rhoifolium Lam leaves and certain
terpenes (a-humulene, b-caryophyllene, a-pinene, and
b-pinene) exhibited anti-tumor efficacy and significant
immunomodulatory action in vivo and in vitro in mice.
Moreover, Grassmann et al. [15] found that the essential oil
from Pinus mugo showed antioxidative properties. All of
these findings strongly suggest that forest environments
(forest bathing trip) have beneficial effects on human
immune function. However, to date, there have been no
published reports on the effect of forest bathing on human
immune function, with the exception of the studies con-
ducted by this author.
Effect of forest bathing trips on human
immune function
Within the framework of published results on forest bath-
ing trips, since 2005, a series of investigations with both
Japanese female and male subjects have been carried out
with the aim of studying the effect of forest bathing on
human immune function. To this end, investigators mea-
sured human NK activity and the numbers/proportions of
NK and T cells, perforin-, GrA/B-, and GRN-expressing
lymphocytes in human peripheral blood lymphocytes
(PBLs) in the subjects during visits to forest areas in Japan
[24].
In the first study [2], 12 healthy male subjects, aged 37–
55 years (43.1 ±6.1 years), were selected from three large
companies in Tokyo, Japan. The sociodemographic infor-
mation on the subjects, including age and lifestyle habits,
was obtained by means of a self-administered question-
naire and has been reported previously [16]. None of the
subjects had any signs or symptoms of infectious diseases,
used drugs that might affect immunological analysis, or
were taking any medication at the time of the study. It was
also confirmed that none of the subjects had taken forest
bathing trips within at least 3 months prior to the study. In
early September 2005, the subjects participated in a 3-day/
2-night trip to forest areas at Iiyama, Nagano prefecture,
located in northwest Japan. On day 1, the subjects walked
about 2.5 km in a forest field in about 2 h, which
approximates the amount of normal physical activity the
subjects would have on an average working day. The
participants were allowed to rest anywhere and anytime
they liked. On day 2, they walked about 2.5 km in the
morning and afternoon (each time approx. 2 h), respec-
tively, in two different forest fields. On day 3, the subjects
finished the trip, and after providing blood samples and
completing a questionnaire survey, they returned to Tokyo.
The main trees in the forests were Japanese cedar (Cryp-
tomeria), Japanese beech, and Japanese oak. Blood samples
were taken on the second (the first sampling during the trip)
and third days (the second sampling during the trip). White
blood cell (WBC) counts, NK activity, numbers of NK and
T cells, and numbers of GRN-, perforin-, and GrA/
B-expressing lymphocytes were determined in the blood
samples. The same measurements were made before the
trips on a normal working day as a control. Blood was
sampled at 0800 hours on all occasions. To control for the
effect of alcohol on NK activity, the subjects did not
consume alcohol for 2 days before providing the blood
samples. The subjects did not take hot spring baths or eat
10 Environ Health Prev Med (2010) 15:9–17
123
any special foods, such as herbs and alcoholic drinks,
which may have affected the immune function during the
trip. Phytoncide concentrations in forest air samples were
also measured.
There were significant differences in NK activity
(Fig. 1a) and in the numbers of NK cells (Fig. 1b) both
before and after the trip and between days 1 and 2,
indicating that the forest bathing trip significantly
increased NK activity (Fig. 1a) and the numbers of NK
cells (Fig. 1b). It has been reported that NK cells kill
tumor or virus-infected cells through the release of per-
forin, granzymes, and GRN via the granule exocytosis
pathway [812]. In order to explore the mechanism of
enhancement of NK activity induced by forest bathing,
the effect of forest bathing on the intracellular levels of
perforin, GRN, and GrA/B in PBL was investigated. The
results showed that the forest bathing trip also signifi-
cantly increased the numbers of intracellular perforin-,
GRN-, and GrA/B-expressing lymphocytes (Fig. 2).
Taken together, these findings indicate that a forest
bathing trip can increase NK activity and that this effect
might be at least partially mediated by increasing the
number of NK cells and by the induction of intracellular
perforin, GRN, and GrA/B [2].
How long does the increased NK activity
last after a forest bathing trip?
Following the first study, two questions remained to be
resolved: (1) will a trip to places without forest (a city
tourist visit) also increase NK activity? (2) How long does
the increased NK activity last after a forest bathing trip or a
city tourist visit? Two investigations were then conducted
to address these two questions [3]. Twelve healthy male
subjects, aged 35–56 years (mean 45.1 ±6.7 years), were
selected from four large companies in Tokyo, Japan.
Information on the subjects was gathered from a self-
administered questionnaire, including age and lifestyle
habits, as described previously [16]. None of the subjects
had any signs or symptoms of infectious disease, used
drugs that may affect the immunological analysis, or were
taking any medication at the time of the study. It was also
confirmed that none of the subjects had taken forest bathing
trips within at least 3 months prior to the study. In early
September 2006, the subjects experienced a 3-day/2-night
trip to three different Chamaecyparis obtuse (Japanese
cypress, Hinoki in Japanese) forests around Agematsu
town, Nagano prefecture, located in northwest Japan. The
schedule of the forest bathing trip was similar to that
described previously [2]. Prior to the forest visit, in mid-
May 2006, 11 of the same 12 subjects participated in a city
tourist visit consisting of 3-day/2-night trip to Nagoya city
[2,3]. On the first day, the subjects walked for 2 h in the
afternoon along a tourist route through a historical district
of Nagoya city and then stayed at a hotel in Nagoya. On the
second day, the subjects walked for 2 h around Nagoya
Before Da
y
1Da
y
2
0
200
400
600
800
1000
NK cell number/ul
∗∗
∗∗,#
B
0
10
20
30
40
NK activity (%)
A
∗∗,#
Fig. 1 Effect of a forest bathing trip on natural killer (NK) activity
(a) and the number of NK cells (b). Columns:Before values obtained
before the trip, Day 1 values obtained after the first day of the trip,
Day 2 values obtained after the second day of the trip. Data are
presented as the mean ±standard deviation (SD) (n=12).
*P\0.05, **P\0.01, significantly different from before the trip,
#
P\0.05 significantly different from day 1 by paired ttest. Cited
from Li et al. [2]
Granulysin Perforin Granzyme A Granzyme B
0
300
600
900
1200
1500
1800
Number in PBL/ul
Before Day 1 Day 2
∗∗ ∗∗
∗∗
∗∗
∗∗
∗∗
∗∗
∗∗,#
Fig. 2 Effect of a forest bathing trip on the number of granulysin-,
perforin-, and granzymes A/B-expressing cells in peripheral blood
lymphocytes (PBLs). Data are presented as the mean ±SD (n=12).
*P\0.05, **P\0.01, significantly different from before the trip,
#
P\0.05 significantly different from day 1 by the paired ttest. Cited
from Li et al. [2]
Environ Health Prev Med (2010) 15:9–17 11
123
baseball Dome in the morning and 2 hours around/in
Nagoya airport nearby Nagoya city in the afternoon. There
are some tree-covered areas in Nagoya city, but there are
almost no trees in the areas visited. The class of hotel and
the lifestyle of the subjects during the stays in the hotels
were the same for the city and forest trips. The walking
courses in both trips were 2.5 km, as in the previous study
[2]. Blood was sampled at 0800 hours on the second (the
first sampling during each trip) and third days (the second
sampling during each trip), on days 7 and 30 after the forest
bathing trip, and 3 days prior to the trips (control). The
WBC counts, NK activity, proportions of NK and T cells,
and GRN-, perforin-, and GrA/B-expressing cells in PBLs
were measured. The concentration of adrenaline in urine
was also determined. To control for the effect of alcohol on
NK activity, the subjects did not consume alcohol for
2 days prior to blood sampling, including before and dur-
ing the trips, and after the trip on days 7 and 30. The
purpose of setting the control experiment in a city in this
study was to determine whether just taking a trip (city
tourist visit) can also affect NK activity.
There were significant differences in NK activity
(Fig. 3a), the numbers of NK cells (data not shown), and
the percentages of GRN-, perforin-, and GrA/B-expressing
cells in PBLs (Fig. 4a) between before and after the forest
bathing trip, suggesting that this trip significantly increased
human NK activity, the number of CD16
?
NK cells, and
the percentages of GRN-, perforin-, and GrA/B-expressing
cells in PBLs. These results confirmed the earlier findings
[2]. The increases in NK activity and number of CD16
?
NK cells and the higher percentages of GRN-, perforin-,
and GrA/B-expressing cells lasted for more than 7 days,
while the increased NK activity and the higher number of
NK cells and GRN- and GrB-expressing cells lasted for 30
days (Figs. 3a, 4a). In contrast, the city tourist visit did not
increase human NK activity, numbers of NK cells, or the
expression of the selected intracellular perforin, GRN, and
GrA/B (Figs. 3b, 4b). Phytoncides, such as alpha-pinene
and beta-pinene, were detected in the forest air, but were
almost absent from city air. These findings indicate that a
forest bathing trip increased NK activity, the number of NK
cells, and the levels of intracellular perforin, GRN, and
GrA/B, and that these effects lasted for at least 7 days after
the trip [3]. The most important finding of these studies is
that visiting a forest—but not a city—increases NK activity
and the intracellular levels of perforin, GRN, and GrA/B.
Phytoncides released from the trees may partially contrib-
ute to increased NK activity [1].
Effect of forest bathing trips on NK activity
in female subjects [4]
Although these studies demonstrated that forest bathing
trips were able to enhance human NK activity in male
subjects, the question remaining to be resolved was whe-
ther or not forest bathing trips would also increase
NK activity in female subjects. It has been reported that
menstrual cycle significantly affects NK activity [17];
consequently, the influence of the menstrual cycle on NK
activity should be controlled for in experiments with
female subjects.
In this study [4], 13 healthy nurses, aged 25–43 years
(mean 28.8 ±4.6 years) and active in their profession for
4–18 years (mean 6.7 ±3.8), were selected with informed
consent. None of the subjects had any signs or symptoms of
infectious disease, used drugs that may affect immuno-
logical analysis, or were taking any medication at the time
of the study. The subjects experienced a 3-day/2-night trip
to forest fields around Shinano town, Nagano prefecture,
located in northwest Japan in early September 2007. The
schedule of the forest bathing trip and blood sampling was
similar to that described for the earlier studies [2,3], and
the same blood/urine tests were carried out (WBC counts,
NK activity, numbers of NK and T cells, and GRN-, per-
forin-, and GrA/B-expressing lymphocytes in the blood
samples; concentrations of adrenaline and noradrenaline in
urine) as well as tests measuring the concentrations of
Before Day 1 Day 2 Day 7 Day30
0
5
10
15
20
25
30
35
NK activity (%)
Before Day 1 Day 2
0
5
10
15
20
25
30
35
NK activity (%)
AB
∗∗ ∗∗
Fig. 3 Effect of a forest bathing
trip (a,n=12) and a city
tourist visit (b,n=11) on NK
activity. Data are presented as
the mean ±SE. *P\0.05,
**P\0.01, significantly
different from before the trip
by paired ttest. Cited from
Li et al. [3]
12 Environ Health Prev Med (2010) 15:9–17
123
estradiol and progesterone in serum. The same control
measurements were made before the trip on a normal
working day. Blood was sampled at 0800 hours on all days.
The concentrations of phytoncides in the forests were
measured.
The forest bathing trip significantly increased NK
activity (Fig. 5) and the positive rates of NK (Fig. 6) and
perforin-, GRN-, and GrA/B-expressing cells (Fig. 7). The
increased NK activity (Fig. 5) and the positive rates of NK
(Fig. 6) and perforin-, GRN-, and GrA/B-expressing cells
(Fig. 7) lasted for more than 7 days after the trip [4], which
confirmed the previous findings in male subjects [3].
Phytoncides, such as alpha-pinene and beta-pinene, were
detected in forest air. These findings indicate that a forest
bathing trip also increased NK activity, number of NK
cells, and the levels of intracellular anti-cancer proteins in
female subjects and that this effect lasted for at least 7 days
after the trip. Phytoncides released from trees may partially
contribute to the increased NK activity [1,4]. A forest
bathing trip was found to significantly decrease the per-
centage of T cells in female subjects (Fig. 8)[4]. It has
been reported that mental stress increases T cell levels
among PBLs [17,18] and that people with a poor lifestyle
have a higher percentage of T cells than people with a good
lifestyle [16]; therefore, it can be speculated that the pro-
portion of T cells in PBLs may reflect stress status.
Souza et al. reported that NK activity is significantly
higher in the follicular phase of the menstrual cycle than in
the luteal phase and that the levels of NK activity in post-
menopausal women are similar to those of women in the
follicular phase but significantly higher than those of women
in the luteal phase [19]. Conversely, Yovel et al. [20]
reported that the menstrual cycle had no significant effect on
the activity levels of NK cells. Roszkowski et al. [21] found
that patients with low (\50 pg/ml) and high ([200 pg/ml)
estradiol levels showed an increase and a decrease of NK
cell activity, respectively. Progesterone at 100–400 nM
(31.45–125.8 ng/ml) inhibits NK activity in healthy preg-
nant women, whereas 100-fold higher concentrations are
GRN Perforin GrA GrB
0
10
20
30
40
50
60
70
Positive rate in PBL (%)
Before Day 1 Day 2 Day 7 Day30
A
GRN Perforin GrA GrB
0
10
20
30
40
50
60
70
Positive rate in PBL (%)
Before Day 1 Day 2
B
∗∗
∗∗
∗∗
∗∗
∗∗ ∗∗
∗∗∗∗ ∗∗ ∗∗
Fig. 4 Effect of a forest bathing trip (a,n=12) and a city tourist
visit (b,n=11) on granulysin- (GRN), perforin-, and granzymes (Gr)
A/B-expressing cells in PBLs. Data are presented as the mean ±SE.
*P\0.05, **P\0.01, significantly different from before the trip by
paired ttest. Cited from Li et al. [3]
Before Day 1 Day 2 Day 7 Day 30
0
5
10
15
20
25
30
35
NK activity (%)
** ** *
Fig. 5 Effect of a forest bathing trip on NK activity in female
subjects. Data are presented as the mean ±SE (n=13). *P\0.05,
**P\0.01, significantly different from before the trip by the paired
ttest. Cited from Li et al. [4]
Before Da
y
1Da
y
2Da
y
7Da
y
30
0
5
10
15
20
25
30
NK cells (%)
∗∗
∗∗
∗∗
Fig. 6 Effect of a forest bathing trip on the percentage of NK cells.
Data are presented as the mean ±SE (n=13). **P\0.01, signif-
icantly different from before the trip by the paired ttest. Cited from
Li et al. [4]
Environ Health Prev Med (2010) 15:9–17 13
123
required for reducing NK activity in non-pregnant women
[22]. These suggest that the menstrual cycle and the levels of
estradiol and progesterone in serum may affect human NK
activity.
To control for the influence of menstrual cycle on NK
activity, a questionnaire was administered to obtain infor-
mation on the menstrual cycle of the subjects. The ratios of
subjects who were in the follicular phase during the
experiment were 5/13, 6/13, 6/13, 7/13, and 6/13 on the day
before the trip, days 1 and 2 during the trip, and days 7 and
30 after the trip, respectively, indicating that there was no
significant difference in the proportion of women in dif-
ferent phases of the menstrual cycle between the different
days. This observation suggests that the menstrual cycle
had a similar influence on the average of NK activity on the
different days. Therefore, statistical analyses to compare
the mean values of NK activity on the different days by a
paired ttest should be appropriate. In addition, the con-
centrations of estradiol and progesterone in the serum of
the subjects were also measured to confirm the influence of
estradiol and progesterone on NK activity. In this study,
there was no significant difference in the concentration of
estradiol in serum between the days before, during, and
after the forest bathing trip, indicating that, in this case,
estradiol had a similar effect in all subjects on NK activity
on the different days. Although the levels of progesterone
on days 1 and 2 were higher than that before the study, the
difference in serum progesterone concentration between
days 1 or 2 and before the trip was not significant, sug-
gesting that progesterone had a similar effect on NK
activity on the different days [4].
Many factors, including circadian variation [23], phys-
ical exercise [16,24], and alcohol consumption [16,25],
can affect human NK activity. In order to control for the
effect of circadian rhythm on NK activity, blood was
sampled at 0800 hours on all days [24]. To control for the
effect of physical exercise on NK activity, the number of
steps taken during the walking trips were limited to average
normal workday distances, as monitored by a pedometer.
The levels of physical activity among all trips were also
matched. To control for the effect of alcohol on NK
activity, the subjects did not consume alcohol for 2 days
before providing the blood sample during the study period
for both trips, including before the trips and after the trips
on days 7 and 30. The number of hours spent sleeping
during the trips were slightly more than those on average
working days; however, the difference was not significant
in either type of trip. Kusaka et al. [26] reported that the
number of sleeping hours did not affect NK activity or NK
cell numbers under physiological conditions. Li et al. [16]
also found that there was no difference in the number
of NK cells or the levels of perforin-, GRN-, or GrA/
B-expressing cells in PBL among subjects who slept for 5,
6, or 7 h, respectively. In addition, although the number of
hours slept during the city tourist visit were slightly more
than those on an average working days, the NK activities
during the trip were almost the same as for working days,
indicating that the longer sleeping hours did not affect NK
activity in the city tourist visit [3]. Taken together, it can be
concluded that although the number of sleeping hours
during the trips was slightly higher than those on average
working days, this difference did not affect NK activity or
cell numbers in the city tourist trip.
Effect of forest bathing trips on stress hormones
Adrenaline is released from the adrenal medulla, and
adrenaline levels increase under circumstances of novelty,
GRN Perforin GrA GrB
0
10
20
30
40
50
60
Positive rate in PBL (%)
Before Day 1 Day 2 Day 7 Day 30
∗∗
∗∗
∗∗
∗∗
∗∗
∗∗
∗∗
∗∗
∗∗
∗∗
∗∗
∗∗
Fig. 7 Effect of a forest bathing trip on the levels of GRN-, perforin-,
and GrA/B-expressing cells in PBLs. Data are presented as the
mean ±SE (n=13). *P\0.05, **P\0.01, significantly different
from before the trip by paired ttest. Cited from Li et al. [4]
Before Da
y
1Da
y
2Da
y
7Da
y
30
0
10
20
30
40
50
60
70
T cells (%)
∗∗
Fig. 8 Effect of the forest bathing trip on the percentage of T cells.
Data are presented as the mean ±SE (n=13). *P\0.05,
**P\0.01, significantly different from before the trip by paired
ttest. Cited from Li et al. [4]
14 Environ Health Prev Med (2010) 15:9–17
123
anticipation, unpredictability, and general emotional arou-
sal. Noradrenaline is the predominant neurotransmitter
released by the sympathetic system, and some of this enters
the blood; the level of noradrenaline increases during
increased physical activity [27]. The measurement of free
adrenaline and noradrenaline in urine provides a reliable
measure of the circulating concentration of adrenaline and
noradrenaline in the bloodstream and, is, therefore, is a
measure of sympathoadrenal medulla activity [28]. The
concentrations of adrenaline and noradrenaline in urine
have been used to evaluate work-related stress in nurses
[29] and truck drivers [30], and the subjects were found to
show decreases in adrenaline and/or noradrenaline in urine
with lower stress. Forest bathing trips were found to sig-
nificantly decrease urine adrenaline and noradrenaline
concentrations in both male (Fig. 9a) [3] and female
subjects (Fig. 9c, d) [4], while a city tourist visit had no
effect (Fig. 9b) [3]. This result suggests that the subjects
were under lower stress during the forest bathing trips [3,
4]. Garland et al. reported that adrenaline inhibits human
NK activity [31]. The addition of noradrenaline to intra-
thecal morphine augments the postoperative suppression of
NK cell activity [32], suggesting that noradrenaline also
inhibits human NK activity. Li et al. [33] reported that
physical and/or psychological stress decreases NK activity,
NK receptor levels, and mRNA transcription levels of
granzymes and perforin in mice. The increase in NK
activity during forest bathing trips may be related to an
attenuated stress hormone response (adrenaline, noradren-
aline) associated with the forest bathing trip, whereas
increased sympathetic activity may have an immunosup-
pressive effect through the release of adrenaline [34]. Other
studies have reported that forest bathing trips reduce saliva
cortisol levels, prefrontal cerebral activity, and blood
pressure in humans, as well as stabilize autonomic nervous
activity [3537]. In addition, in studies using the POMS
test, forest bathing trips were found to significantly
increase the score for vigor and decrease the scores for
anxiety, depression, and anger, suggesting that the subjects
were physiologically relaxed during the forest bathing trips
[2,4]. One of these studies [2] also demonstrated that a
forest bathing trip significantly increased the proportions of
lymphocytes and monocytes and decreased the proportions
of granulocytes in WBC [2]. It has been reported that
dominance by the parasympathetic nervous system causes
an increase in circulating lymphocytes and decrease in
granulocytes in peripheral blood [38]. This mechanism
suggests indirectly that the parasympathetic nervous sys-
tem, which is associated with relaxation and decreased
stress, was dominant in the subjects during the forest
bathing trips.
Before Da
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Before Da
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y
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∗∗
AB
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1Da
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D
Fig. 9 Effect of a forest bathing trip on adrenaline and noradrenaline
concentrations in urine. aEffect of a forest bathing trip on urinary
adrenaline concentration in male subjects (n=12), beffect of a city
trip on urinary adrenaline concentration in male subjects (n=11),
ceffect of a forest bathing trip on urinary adrenaline concentration in
female subjects (n=13), deffect of a forest bathing trip on urinary
noradrenaline concentration in female subjects (n=13). Data are
presented as the mean ±SE. *P\0.05, **P\0.01, significantly
different from before the trip by paired ttest. Cited from Li et al. [3]
and [4]
Fig. 10 Mechanism of forest bathing-induced induction in NK
activity. AIF Apoptosis-inducing factor, Cyto-c cytochrome c
Environ Health Prev Med (2010) 15:9–17 15
123
Conclusions
These findings indicate that forest bathing trips increase
NK activity, which was mediated by increases in the
number of NK cells and the levels of intracellular anti-
cancer proteins (Fig. 10). Phytoncides released from trees
and the decreased production of stress hormones may
partially contribute to the increased NK activity.
Because NK cells can kill tumor cells by releasing anti-
cancer proteins, such as perforin, GRN, and GrA/B, and
forest bathing trips increase NK activity and the intracel-
lular level of anti-cancer proteins, the above findings
suggest that forest bathing trips may have a preventive
effect on cancer generation and development.
Acknowledgments Parts of the experimental data shown in this
review and performed by author were supported by a grant from the
Ministry of Education, Culture, Sports, Science, and Technology of
Japan (No. 16107007). This project is a collaboration with Professor
Yoshifumi Miyazaki at Chiba University, Professor Kanehisa
Morimoto at Osaka University, Mr. Takahide Kagawa, Forestry and
Forest Products Research Institute, and Dr. Tomoyuki Kawada,
Department of Hygiene and Public Health, Nippon Medical School
(Professor and Chief). The author is grateful to the staff of Depart-
ment of Hygiene and Public Health, Nippon Medical School for their
technical assistance in the experiments.
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... Several European countries are interested in integrating nature into children's education [52]; diverse outdoor activities and school field trips are thus available for students to engage in outside the classroom. Some programs might be geared toward building self-esteem and confidence, while others emphasize communication and teamwork [5,52]. ...
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... Alpine forests. Reported health benefits from forest therapy studies include impacts on humans' immune system, boosting natural killer cells and anticancer proteins, reduced stress, improved mood, sleep, and well-being, reduced blood pressure, accelerated recovery from illness, and increased ability to concentrate [97][98][99][100]. Based on these results, more than 50 Forest Therapy Trails were developed in Japan with millions of annual visitors, and forest therapy has become a cornerstone of preventive health care and healing in Japanese medicine. ...
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Alpine regions are characterized by exceptional natural resources, cultural heritage, healthy climate, and long tourism tradition. Tourism is a major component of economic growth, with several employment opportunities, and of great importance for the Alpine regions, with many positive effects on the local and regional population. Natural resources can determine the development of competitive tourism destinations and drive the development of nature-based value chains aimed at enhancing tourists’ health and well-being. Historically, the small size of most enterprises, the difficulties in establishing collaborative relationships between industry operators, and the lack of strategic projects aimed at the use and exploitation of natural resources, have hindered a systematic development of a nature-based health tourism (NHT) value chain. Nowadays, tourist market segments are changing the industry competitiveness with the request for more nature-based experiential programs, integrating both rewarding elements of beauty, relaxation, and regeneration, and more demanding elements such as preventative activities and sports. There is an increasing consciousness of the importance of local environmental and cultural preservation, the search for relax and stress-relieving products, and the overall authenticity of the vacation experience. Beyond lifestyle changes, key trends reshaping the health tourism landscape in Alpine regions include population ageing, climate change, and consequences of the COVID-19 pandemic both in terms of business losses and the need for natural remedies against these virus’s long-term effects. This background challenges health tourism operators to rethink the industry dynamics with a more innovation-driven strategy and business development, as well as facilitation of transnational cooperation among all kinds of actors. These include sectoral and specialized agencies such as destination management organizations, business support organizations, and tourism organizations; regional councils and municipalities in charge of policy-making and tourism strategy development; tourism facilities and companies (especially small- and medium-sized enterprises); universities and research centres that conduct applied research and development within the health tourism sector and related sectors, based on natural resources or health-related issues; interest groups and networks supporting nature-based and sustainable health tourism. Despite the richness of natural resources and health-promoting activities that spread among Alpine regions, the NHT landscape is characterized by innovation spatial fragmentation, lack of access to knowledge, and little transversal cooperation for value creation and sharing. Aimed to address these key territorial challenges, the HEALPS2 project “Healing Alps: Tourism based on natural health resources as strategic innovation for the development of Alpine regions” was funded in the Priority “Innovative Alpine Space” of the Interreg Alpine Space program. The key objective of the project was to improve the framework conditions for utilizing the Alpine natural health resources by leveraging existing and newly developed NHT products and service chains to enhance access to knowledge and sharing of experiences at a transnational level. The main project activities took place from October 2019 to June 2022 and involved 11 organizations from 6 countries, i.e. Austria, Italy, Slovenia, Germany, France, and Switzerland. The collaboration between the project partners led to the development of a set of innovation practices and digital solutions, properly combined with the latest research results in tourism and health-related issues and the requirements of health tourism stakeholders collected in several events organized at the local and regional level. The vision of the project is to contribute to the positioning of the Alpine Space as a globally attractive health-promoting place, with a virtuous process of value generation and sharing among Alpine assets, actors, and territories. This book incorporates the key knowledge and experiences, in terms of concepts, tools, and practices, developed within the HEALPS2 project, here organized into eight chapters. The content was purposefully organized to dedicate to the core assets for an Alpine NHT industry excellence, i.e. the natural resources and their healing effects; the digital tools enhancing the collection, advanced analytics and spread of data on NHT industry for supporting strategic decision-making; the innovation practices and communication strategies to properly engage the industry stakeholders.
... Alpine forests. Reported health benefits from forest therapy studies include impacts on humans' immune system, boosting natural killer cells and anticancer proteins, reduced stress, improved mood, sleep, and well-being, reduced blood pressure, accelerated recovery from illness, and increased ability to concentrate [97][98][99][100]. Based on these results, more than 50 Forest Therapy Trails were developed in Japan with millions of annual visitors, and forest therapy has become a cornerstone of preventive health care and healing in Japanese medicine. ...
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... Alpine forests. Reported health benefits from forest therapy studies include impacts on humans' immune system, boosting natural killer cells and anticancer proteins, reduced stress, improved mood, sleep, and well-being, reduced blood pressure, accelerated recovery from illness, and increased ability to concentrate [97][98][99][100]. Based on these results, more than 50 Forest Therapy Trails were developed in Japan with millions of annual visitors, and forest therapy has become a cornerstone of preventive health care and healing in Japanese medicine. ...
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... Alpine forests. Reported health benefits from forest therapy studies include impacts on humans' immune system, boosting natural killer cells and anticancer proteins, reduced stress, improved mood, sleep, and well-being, reduced blood pressure, accelerated recovery from illness, and increased ability to concentrate [97][98][99][100]. Based on these results, more than 50 Forest Therapy Trails were developed in Japan with millions of annual visitors, and forest therapy has become a cornerstone of preventive health care and healing in Japanese medicine. ...
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Full-text available
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... Alpine forests. Reported health benefits from forest therapy studies include impacts on humans' immune system, boosting natural killer cells and anticancer proteins, reduced stress, improved mood, sleep, and well-being, reduced blood pressure, accelerated recovery from illness, and increased ability to concentrate [97][98][99][100]. Based on these results, more than 50 Forest Therapy Trails were developed in Japan with millions of annual visitors, and forest therapy has become a cornerstone of preventive health care and healing in Japanese medicine. ...
Chapter
Full-text available
Communication activities play a pivotal role in the management of research projects, especially those involving several partners and stakeholders from different countries. The Interreg Alpine Space HEALPS2 project relies on a transnational and transversal approach to improve the framework conditions and tools for alpine health tourism, and therefore proposes a communication strategy based on specific objectives. These objectives guide the communication activities at an internal and external level, with the latter being declined for different targets and stakeholders. In this Chapter, the communication activities are described, starting from the general and specific objectives-oriented approach, to the local realization. The general strategy and the analysis are illustrated, then are demonstrated through a regional use case—the Parco Regionale Alpe Veglia-Alpe Devero and Parco Regionale Alta Valle Antrona.
... Alpine forests. Reported health benefits from forest therapy studies include impacts on humans' immune system, boosting natural killer cells and anticancer proteins, reduced stress, improved mood, sleep, and well-being, reduced blood pressure, accelerated recovery from illness, and increased ability to concentrate [97][98][99][100]. Based on these results, more than 50 Forest Therapy Trails were developed in Japan with millions of annual visitors, and forest therapy has become a cornerstone of preventive health care and healing in Japanese medicine. ...
Chapter
Full-text available
Innovation is considered essential to the growth and long-term sustainability of health tourism companies and destinations. Continuous innovation takes place to improve the industry competitiveness, but especially the tourists’ experience and wellness with new product offerings. This Chapter collects and describes the innovation practices proposed and developed in some pilot regions of the HEALPS2 project consortium. The innovation practices identified in the project can be subdivided into three types, i.e., innovation techniques, innovation supporting tools, and innovative product offerings. All the practices were designed to target several operators of the Nature-based Health Tourism (NHT) industry, from tourism facilities and companies (especially small- and medium-sized enterprises) to regional councils and municipalities in charge of policy-making and tourism strategy development. HEALPS 2 innovation practices and techniques can be purposefully integrated at the regional and local level for a more innovation-driven industry strategy and business development, as well as facilitation of transnational cooperation among key actors, also beyond Alpine regions and NHT destinations.
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