The Influence of Urban Natural and Built Environments on Physiological and Psychological Measures of Stress—A Pilot Study

Abstract

Environments shape health and well-being, yet little research has investigated how different real-world environmental settings influence the well-known determinant of health known as stress. Using a cross-over experimental design; this pilot study investigated the effect of four urban environments on physiological and psychological stress measures. Participants (N = 15) were exposed on separate days to one of the four settings for 20 min. These settings were designated as Very Natural; Mostly Natural; Mostly Built and Very Built. Visitation order to the four settings was individually randomized. Salivary cortisol and alpha-amylase; as well as self-report measures of stress; were collected before and after exposure to each setting. Gender was included as a variable in analysis; and additional data about environmental self-identity, pre-existing stress, and perceived restorativeness of settings were collected as measures of covariance. Differences between environmental settings showed greater benefit from exposure to natural settings relative to built settings; as measured by pre-to-post changes in salivary amylase and self-reported stress; differences were more significant for females than for males. Inclusion of covariates in a regression analysis demonstrated significant predictive value of perceived restorativeness on these stress measures, suggesting some potential level of mediation. These data suggest that exposure to natural environments may warrant further investigation as a health promotion method for reducing stress.

Full text

Int. J. Environ. Res. Public Health
2013,
10
, 1250-1267; doi:10.3390/ijerph10041250
International Journal of
Environmental Resea rch and
Public H ealth
ISSN 1660-4601
www.mdpi.com/journal/ijerph
Article
The Influence of U rban Natural and Built E nvironments on
Physiological and Psychological Measures of Stress²
A Pilot Study
K urt Beil * and Douglas H anes
Helfgott Research Institute, National College of Natural Medicine, Portland, OR 97201, USA;
E-Mail: dhanes@ncnm.edu
* Author to whom correspondence should be addressed; E-Mail: kbeil@ncnm.edu;
Tel.: +1-503-552-1804; Fax: +1-503-227-3750.
Received: 15 F ebruary 2013; in revised for
m
: 18 March 2013 / Accepted: 18 March 2013 /
Published: 26 March 2013
Abstract: Environments shape health and well-being, yet little research has investigated
how different real-world environmental settings influence the well-known determinant of
health known as stress. Using a cross-over experimental design; this pilot study investigated
the effect of four urban environments on physiological and psychological stress measures.
Participants (N = 15) were exposed on separate days to one of the four settings for 20 min.
These settings were designated as Very Natural; Mostly Natural; Mostly Built and Very
Built. Visitation order to the four settings was individually randomized. Salivary cortisol
and alpha-amylase; as well as self-report measures of stress; were collected before and
after exposure to each setting. Gender was included as a variable in analysis; and additional
data about environmental self-identity, pre-existing stress, and perceived restorativeness of
settings were collected as measures of covariance. Differences between environmental
settings showed greater benefit from exposure to natural settings relative to built settings;
as measured by pre-to-post changes in salivary amylase and self-reported stress;
differences were more significant for females than for males. Inclusion of covariates in a
regression analysis demonstrated significant predictive value of perceived restorativeness
on these stress measures, suggesting some potential level of mediation. These data suggest
that exposure to natural environments may warrant further investigation as a health
promotion method for reducing stress.
OP E N A C C ESS

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Keywords: stress; cortisol; amylase; natural environment; built environment; green space;
biophilia; psychological restoration
1. I nt roduction
7KH³VHWWLQJV DSSURDFK´WR SXEOLF KHDOWK XVHV D holistic, multi-component model to describe how
environments shape health and well-being [1]. This systems-based approach, established by the 1986
WHO Ottawa Charter for Health Promotion, lays the groundwork for the inclusion of healthy,
supportive environments as part of the health promotion agenda [2]. The optimal design of physical
environmental features is one component of this approach that contributes WR D VHWWLQJ¶V FDSDFLW\ WR
influence health [3]. The tangible infrastructure and environmental features of a place affect numerous
health-determining processes. This is particularly true in urban settings, as initiatives such as the
:+2(XURSH¶V +HDOWK\ &LWLHV SURMHFW [4] DQG WKH &'&¶V +HDOWK\ 3ODFHV SURJUDP [5] have
demonstrated. The consideration and adoption of a health-promoting approach to urban design is
increasingly necessary as cities grow and the global population continues to surpass the 50% urban
threshold [6]. The importance of these perspectives is reflected in the difference in prevalence of
multiple physical and mental health conditions that exist between urban and rural areas [7±9].
One element of healthy supportive environments and urban design QRWHG IRUDQ ³XSVWUHDPKHDOWK
SURPRWLRQ´ FDSDFLW\ LVWKH SUHVHQFH RI WUHHVSDUNV DQG RWKHU QDWXUDO DUHDV [10±12]. Epidemiological
research has shown that residential proximity to these natural green spaces is associated with lower rates
of morbidity and mortality in some [13,14] but not all [15] cases. Evidence suggests that one mechanism
for contact with nature to positively influence health may be via their ability to facilitate stress
reduction [16,17]. Exposure to natural stimuli has been shown to reduce physiological and psychological
stress-related health measures in workplace environments [18±20], hospital settings [21±23]
and artificial simulations [24,25]. It is hypothesized that this reaction is the result of an evolutionary
adaptation known as biophiOLD WKH ³LQQDWH WHQGHQF\ WR IRFXV RQ OLIH DQG OLIH-OLNH SURFHVVHV´ [26].
7KLV ³SV\FKR-HYROXWLRQDU\ VWUHVV´ 3(6 theory [24] is widely regarded and many studies have
supported its premise that nature has the ability to increase health and well-being by reducing stress [27].
Stress is an epidemic public health concern that negatively impacts physical and mental health,
including cardiovascular, gastroenterological, immunological, neurological, endocrine and mental/
emotional health status [28,29]. The complex psychophysiological pathways of stress make
measurement via one single marker impossible. Most stress research utilizes a holistic approach of
collecting subjective psychological and objective physiological data to assess stress status.
Psychological stress is measured via subjective rating scales. Physiological stress is often measured by
salivary analysis due to the validity, reliability and ease of collection of salivary data. Salivary
collection also permits simultaneous measurement of the two principal SDWKZD\VRI WKH ERG\¶VVWUHVV
response: (1) the delayed-response, endocrine-mediated Hypothalamic-Pituitary-Adrenal (HPA)
pathway, measured by concentration of salivary cortisol (sCort), and (2) the immediate-response,
neuro-endocrine mediated Sympatho-Adreno-Medullary (SAM) pathway, measured by activity of
salivary alpha-amylase (sAA) [30]. These methods have been used to measure psychological and

Int. J. Environ. Res. Public Health
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physiological stress response after short- and long-term exposures to different environmental
settings [16,31,32].
Few real-world experimental field studies have been conducted examining the relationship between
stress and
urban natural and built environmental settings. Of those that have, the vast majority utilize
an initiating stressor to elevate baseline stress and facilitate measurement of stress
recovery
[24,33,34].
7RWKH DXWKRUV¶NQRZOHGJH QR VWXGLHV KDYH LQYHVWLJDWHGXUEDQ HQYLURQPHQWV¶ HIIHFWRQ XQSURYRNHG
de novo
stress status. The purpose of this study was two-fold: (1) To test a method for collecting
information from participants about the effects of environments on stress using a 4-arm cross-over
design, and (2) To detect the differences that natural and built urban settings have on physiological and
psychological measures of unprovoked,
de novo
stress. In addition, factors such as pre-existing stress,
perceived restorativeness of a setting, and gender have been suggested as influential determinants of
stress response to environments, and were therefore included in this pilot study.
2. Methods
2.1. Participants
Participants were recruited from the local community via printed and internet-based methods.
Anyone with a current or recent history of endocrine, neuro/psychiatric, salivary gland or acute/chronic
pain disorder, or that was using certain disqualifying medications, was excluded from participating.
To be eligible for enrollment, interested participants also agreed to do the following prior to each study
visit: Refrain from using alcohol, tobacco and recreational drugs for at least 24 h; get a good night¶s
sleep; avoid strenuous activity or caffeine for 12 h; and not consume any food or liquid (except water)
for one hour. Participants were given a $30 USD gift-card to a local hypermarket chain for each study
visit attended, and an additional $30 gift-card if all four visits were attended (Total = $150 USD).
A total of fifteen people (eight male, seven female) were enrolled and participated in the study.
All participants completed all four study visits except for one male participant who missed one visit
due to a scheduling error. Participants reported an average age of 42.3 years (range 20±61 years) and
homogenous ³Non-Hispanic White´ racial/ethnic background. Education and income levels of the
group reflected regional mean and distribution values, with a median annual income of $30,000 USD.
This study was approved by the Institutional Review Board of the National College of Natural
Medicine, Portland, OR USA (IRB#061912A).
2.2. Experi
m
ental Design
Interested participants contacted study personnel and were briefly screened for eligibility. Eligible
participants reported to the study lab to sign consent forms and complete questionnaires about their
health status and self-identity regarding the environment. They were asked to return for all scheduled
study visits, which occurred on four separate non-consecutive weekday mornings in August 2012.
The study used a four-arm cross-over design with identical visits as follows (see Figure 1): participants
arrived at the study lab by 9 a.m. and were asked to turn off their cell phones and not use any
electronic media or converse with other participants for the remainder of the visit. They were then
asked to complete a brief health check-in form, a measure of stress experienced in the last week, and a

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subjective measure of current stress level (Time1). Participants were then transported in groups of
three or four via passenger van to the environmental settings. Setting visitation order was individually
randomized so that no participants visited the four settings in the same order. Upon arrival at the
setting, participants provided a pre-exposure saliva sample and repeated the subjective stress scale
(Time2). They were then instructed to sit comfortably and observe their surroundings without
engaging in any activity for 20 min. After 20 min, post-exposure salivary and subjective stress data
were collected (Time3). Individual on-site subjective rating scales and a focus-group debriefing back
DWWKHVWXG\ODESURYLGHGLQIRUPDWLRQDERXWSDUWLFLSDQWV¶H[SHULHQFHVZLWKWKHLQGLYLGXDOVHWWLQJV
Figur e 1. Flow diagram for each visit (×4). (PSS²Perceived Stress Scale, Stress²
Subjective Stress Scale, PRS²Perceived Restorativeness Scale).
Environmental Settings
All settings were located within 15km of the study lab, and selected on the basis of: (1) proximity to
the study lab, (2) availability during the dates of the study visits, (3) presence of overhead covering to
minimize sun & rain exposure, and (4) sufficient level of safety, as perceived by the study authors.
7KHVHWWLQJVZHUHFDWHJRUL]HGRQD RUGLQDOVFDOHIURP³9HU\1DWXUDO´ WR³9HU\ %XLOW´ (Figure 2(a±d)),
following the method used by Matsuoka [35] as follows:

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9 Very Natural: Trees, shrubs, and other natural elements with minimal evidence of human
influence. Study setting was a 187-acre forested urban nature reserve
9 Mostly Natural: Presence of significant amounts of vegetation and some human influence such
as walkways and buildings. Study setting was a 8.76-acre tree-lined urban park
9 Mostly Built: Majority of viewable landscape is due to human influence, with some natural
elements such as trees. Study setting was a 0.92-acre urban plaza
9 Very Built: Entirety of viewable landscape is due to human influence, with minimal presence of
natural elements. Study settings was a 3.46-acre outdoor shopping mall
Figur e 2. Photos depicting each of the four environmental settings experienced by
participants. (a) Very Natural; (b) Mostly Natural; (c) Mostly Built; (d) Very Built.
(a)
(b)
(c)
(d)
Setting category labels were not shared with study participants at any time. Transportation to and
from each setting occurred via identical rented minivans and took no longer than 15 min one-way.
All settings were within 50 m of the roadway, thus minimizing the amount of walking required from
setting parking areas. Visitation to the settings occurred between 9:30 and 10:30 a.m. on weekday
mornings in order to minimize the presence of foot traffic and possible disruption.

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2.3. Measures
2.3.1. Outcome Measures
S
aliva (sCort and sAA)
Collection of saliva occurred before and after 20 min of environmental exposure at Time2 and
Time3 respectively. All saliva samples were collected using Saliva Oral Swabs® from Salimetrics,
LLC (State College, PA, USA). Participants placed inert polymer oral collection swabs under their
tongue for 2 min of passive retention before storing them in a provided swab storage tube. At the end
of each study visit, samples were centrifuged for 10 min at 1,500 g, separated, and stored at í80 °C
until assay. Salivary cortisol samples were analyzed in duplicate by ZRT labs (Beaverton, OR, USA)
using standard ELISA. Salivary alpha-amylase was analyzed by Salimetrics LLC using a Tecan Sunrise
plate reader to assess kinetic activity of 1:200 dilution at 37 °C with readings at 1 and 3 min.
S
ubjec tive
S
tress
S
cale (
S
tress)
A one-item, 0±10 rating scale was used to collect participants' perceived levels of stress, in a
manner similar to that used by Nater
et al
. [36]. This instrument was administered at three times during
each study visit: (1) upon initial check-in (Time1); (2) upon arrival to the environmental settings at
(Time2), and (3) after 20 min of the exposure to each setting (Time3).
2.3.2. Exploratory Co-Variates (Pre-Exposure)
Environ
m
ental Identity (EID)
S
cale
The EID scale is a validated, 28-item questionnaire that measures self-identification with the natural
environment and natural causes [37]. Previous research has demonstrated that EID is related to
affective connection to an environment and environmental behaviors [38], but tR WKH DXWKRUV¶
knowledge no studies have been conducted establishing a relationship between EID score and health
status or stress response to environmental settings.
Perce ived
S
tress
S
cale (P
SS
)
The PSS is a validated 10-item self-report questionnaire that measures an individual¶s response to
stressful events that have occurred during a given period of time [39], in this case during the seven
days prior to each study visit. To determine if pre-existing stress influenced study outcome measures,
the PSS was completed during visit check-in at Time1.
2.3.3. Exploratory Co-Variates (Post-Exposure)
Perce ived Restorativeness
S
cale (PR
S
)
The PRS is a validated 16-item scale that asks participants to rate their agreement with
opinion-based statements related to environmental features [40]. It was originally developed as an

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instrument to test the validity of .DSODQ¶V neuro-cognitive model of biophilia known as Attention
Restoration Theory (ART) [41], but has been used to adequately measure psychophysiological stress
UHVSRQVHV WR QDWXUDO DQG EXLOW VHWWLQJV DFFRUGLQJ WR 8OULFK¶V 3(6 PRGHO [42]. It has been used to
demonstrate the relationship between subjective environmental assessment and psychophysiological
changes [42,43]. To account for participants¶ subjective assessment of environmental settings, the PRS
was completed at the conclusion of each period of exposure at Time3.
2.4.
S
tatistical Analysis
For each of the primary and secondary outcome measures, the following plan was followed: First,
the effect of Visit Order on the outcome was tested to exclude it as a significant factor. Second, it was
noticed that there was significant regression to the mean for almost all outcomes, so baseline values
were included as covariates in all main analyses. Third, between-setting outcomes were compared
using baseline values as a covariate. Where possible, mixed-model ANCOVAs were used with Setting
as a within-subjects factor. Both sCort and sAA measurements were log-transformed. For some
self-report outcomes, responses were distributed in a way that required non-parametric analysis, via
)ULHGPDQ¶VWHVW$VDIROORZ-up to the main analysis, tests were repeated with gender included in the
model to determine whether there were differences in outcomes between gender or interactions
between setting and gender effects. Correlations computed for some covariates and outcome measures
use all data points, including multiple measurements of individual subjects, and should therefore be
considered only as descriptive measures. This is likewise true of the regression of ǻStress on PRS
shown in Section 3.3.3.
3. R esults
Initial repeated-measures analyses for all outcome measures revealed no effect of either study visit
order (
i.e.
, Visit 1±4) or interaction between visit order and environmental setting. As a result, study
visit order was excluded from subsequent analyses. Comparison of primary outcome measures
revealed no significant correlations between sCort and sAA stress biomarkers or between these
physiological measures of stress and the main psychometric stress measure (all R2 < 0.04).
The presence of gender effects in similar studies [44±46] led to the decision that all outcome measure
data would be analyzed by gender, subsequent to the main analyses for each measure.
3.1.
S
alivary Measures
3.1.1. Cortisol (sCort)
All sCort data were subjected to a natural log transformation prior to analyses in order to normalize
outcome distributions. Analyses of logCort by setting demonstrated a mean Time3 decrease in logCort
relatLYH WR 7LPH EDVHOLQH ǻORJ&RUW) in all four settings, consistent with normal circadian rhythm
physiology. 6HWWLQJ GLG DSSHDU WR LQIOXHQFH ǻORJ&RUW LQ WKH K\SRWKHVL]HG GLUHFWLRQ
i.e.
, logCort
reductions were largest after exposure to the Very Natural and Mostly Natural settings, and were larger
for the Mostly Built setting than the Very Built setting. However, while these results are consistent
with the PES model, ANOVA was not able to detect sWDWLVWLFDOO\ VLJQLILFDQFH ǻORJ&RUW GLIIHUHQFHV

Int. J. Environ. Res. Public Health
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between settings (F3,38.4 = 0.675,
p
= 0.573). There were no gender differences detected for
measurements of sCort.
3.1.2. Amylase (sAA)
All sAA data was subjected to a natural log transformation prior to analysis in order to normalize
outcome distributions. Analysis of sAA by setting demonstrated a mean Time3 increase relative to
Time2 baseline in all four settings, though only the Very Built setting showed statistical significance
for the within-group change (
p
= 0.001; See Figure 3). The elevation in sAA indicates an activation of
the SAM pathway during exposure to the Very Built setting and suggests participants were highly
stressed in this locDWLRQDW 7LPH GDWDFROOHFWLRQ $ QHJDWLYHFRUUHODWLRQ EHWZHHQ ǻORJ$P\ODVH
i.e.
,
logTime3Amylase-logTime2Amylase) and logTime2Amylase (r = í0.369) was suggestive of a
regression to the mean and led to inclusion of logTime2Amylase as a covariate in subsequent analyses.
Repeated measures ANCOVA returned a non-VLJQLILFDQW RYHUDOO HIIHFW RI VHWWLQJ RQ ǻORJ$P\ODVH
(F3, 38.3 = 1.69,
p
= 0.186). However, post hoc t-tests did show unadjusted significance in comparison
of the Mostly Built and Very Built settings (ݔҧ = 6.31
vs.
45.05 U/mL, respectively;
p
= 0.033),
suggesting some difference in activation of the SAM pathway between these two built urban settings.
Participant reporting during the debriefing revealed strong dislike and feelings of unease in the Very
Built setting, which likely contributed to the elevation of sAA.
Figure 3. &KDQJHVLQVDOLYDU\DP\ODVH¨Amylase) after 20 min exposure to environmental settings.
Inclusion of gender in the analysis revealed that females had a mean increase in logAmylase across
all four settings, while males had an overall mean decrease in logAmylase. However, ANCOVA
analysis did not reveal statistical significance for the effects of either Gender (F1,11.8 = 3.13,
p
= 0.103)
or the interaction between gender and setting (F3,36.0 = 0.391,
p
= 0.76).
3.2.
S
ubjec tive
S
tress Measure
Analysis of subjective stress by setting demonstrated no between-settings difference for Time2
relative to Time1 baseline, ruling out any concern that the drive to each setting would influence
subjective stress response. Conversely, setting differences were detected for stress measured at Time3

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UHODWLYH WR 7LPH ǻ6WUHVV LQGLFDWLQJ VHWWLQJ H[SRVXUH GLG KDYH DQ LQIOXHQFH RQ VXEMHFWLYH VWUHVV
/DUJHU QHJDWLYH ǻ6WUHVV VFRUHV ZHUH GHWHFWHG IRU WKH QDWXUDO VHWWLQJV FRPSDUHG WR WKH EXLlt settings
(Figure 4); only the Very Natural setting showed a statistically significant within-group change
(
p
= 0.01 Wilcoxon signed rank).
Figur e 4. &KDQJHVLQVXEMHFWLYHVWUHVV¨Stress) after 20 min exposure to environmental settings.
Comparison between settings via non-SDUDPHWULF )ULHGPDQ¶s test failed to reveal a statistically
significant difference in the change in self-reported Stress (
p
= 0.140). Large negative correlations
EHWZHHQǻ6WUHVVDQG7LPH6WUHVVUs = í0.346) suggested possible regression to the mean. Inclusions
of Time2 stress as a covariate was therefore used in subsequent analyses; this inclusion also yielded
residual distributions suitable for parametric analysis. Parametric repeated-measures ANCOVA
analysis revealed a near-statistically significant Setting main effect (F3,40.84 = 2.670,
p
= 0.060),
after adjustment for baseline values.
Post hoc
JURXSFRPSDULVRQVGLGGHPRQVWUDWHVLJQLILFDQWǻ6WUHVV
differences between the Very Natural and Mostly Built settings (ݔҧ = í1.00
vs.
+0.07, respectively;
p
= 0.008), suggesting that while these two settings did have different effects on stress status, these
may have been obscured by the four-way design of this study. It is interesting to note that comments
made during debriefing were mixed for the Mostly Built setting, with many participants enjoying the
physical setting but disliking the noise and activity of some non-study personnel. Over-all these
comments were more positive than the negative comments about the Very Built setting in which there was
QRVWDWLVWLFDOHIIHFWRQǻ6WUHVV&RPPHQWVDERXWWKH9HU\1DWXUDOVHWWLQJZHUHRYHUZKHOPLQJO\SRVLWLYH
Subsequent inclusion of Gender as a factor revealed no main effect of Gender on subjective stress;
however, a near-significant Setting × Gender interaction was reported (F3,37.7 = 2.764,
p
= 0.055). This
is primarily the result of responses to the Mostly Built setting, to which only females had a positive
ǻ6WUHVVresponse (See Table 1). With gender included in the model, post hoc pair-wise comparisons
UHYHDOHG VLJQLILFDQW ǻ6WUHVV GLIIHUHQFHV EHWZHHQ WKH 9HU\ 1DWXUDO DQG ERWK WKH 0RVWO\ %XLOW
(
p
= 0.003) and Very Built (
p
= 0.039) settings.

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Table 1. Setting × *HQGHUDGMXVWHGPHDQVIRUǻ6WUHVV.
Setting
Gender
Mean ǻ6WUHVV
95% Con fidenc e Interval
Lower Bound
Upper Boun d
Very natural
Male
í0.88
í1.73
í0.04
Female
í1.26
í2.17
í0.34
Mostly Natural
Male
í0.33
í1.30
0.64
Female
í0.48
í1.41
0.46
Mostly Built
Male
í0.60
í1.48
0.28
Female
0.89
í0.07
1.84
Very Built
Male
í0.02
í0.87
0.83
Female
í0.47
í1.39
0.45
3.3. Co-Variate Measures
3.3.1. Environmental Identity Scale (EID)
Mean EID score for participants was 118.5 (SD = 10.1), in a possible range of 24±196 points; these
results are similar to other population means [37]. Correlations were detected between EID and both
ǻORJ&RUW U  
p
=  DQG ǻORJ$P\ODVH U  
p
= 0.033), indicating a potential
relationship between environmental identity and physiologic response. However, inclusion of EID in
ANCOVA analysis did not significantly influence the effect of Setting on these salivary measures
(F3,37.9 = 0.672,
p
= 0.575 & F3,37.1 = 1.672,
p
= 0.190, respectively). No correlation was detected
EHWZHHQ (,' DQG ǻ6WUHVV LQGLFDWLQJ WKDW HQYLURQPHQWDO self-LGHQWLW\ ZDV XQUHODWHG WR SDUWLFLSDQWV¶
subjective experience during the study. Inclusion of EID as a covariate RIǻ6WUHVVGLGQRWVLJQLILFDQWO\
influence the effect of Setting on subjective stress.
3.3.2. Perceived Stress Scale (PSS)
No PSS differences were detected either by setting or visit date, indicating that all groups had
statistically equivalent stress levels prior to study arrival. The mean PSS score across all four study
visits was 11.94 (SD = 4.96) out of a possible 40 points. This is less than the 2009 US National PSS
mean of 15.84 [47], suggesting participants had lower levels of pre-existing stress at the beginning of
each visit than the population average. Regarding relationship with outcome measures, PSS score was
not associated with either sCort or sAA biomarker outcomes. A large correlation was detected between
PSS and both Time1 (r = 0.663) and Time2 (r = 0.439) subjective stress, suggesting participants¶OHYHO
of experienced stress in the previous week was related to their level of current stress during the study.
+RZHYHU QR FRUUHODWLRQ ZDV GHWHFWHG EHWZHHQ 366 DQG ǻ6WUHVV VXJJHVWLQJ WKDW SUH-existing stress
was not a factor in determining changes in stress level during the experiment. Inclusion of PSS as a
FRYDULDWHRIǻ6WUHVVLQDPRGHOGLGKRZHYHUUHVXOWLQDQHDU-significant Setting effect (
p
= 0.053).

Int. J. Environ. Res. Public Health
2013,
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3.3.3. Perceived Restorativeness Scale (PRS)
Highly significant setting PRS differences were found (F3,40.97 = 12.526,
p
< 0.001) with
post-hoc
pair-wise comparisons demonstrating that the Very Natural setting was perceived as more restorative
than the other three settings (all
p
< 0.001; See Figure 5). Perceived restorativeness was not associated
with either sCort or sAA biomarker outcomes, but a significant correlation was detected between PRS
DQGǻ6WUHVVUs = í0.387). 6LPSOHOLQHDUUHJUHVVLRQWRGHWHUPLQHWKHHIIHFWRI356RQǻ6WUHVVSURGXFHG
a relatiRQVKLS ZLWK VORSH Į  í0.422 (R2 = 0.219) demonstrating a small but reliable effect on
subjective stress (See Figure 6). ,QFOXVLRQ RI 356 DV D FRYDULDWH LQ WKH SULRU DQDO\VLV RI ǻ6WUHVV E\
environmental setting showed a highly significant (
p
< 0.001) effecWRI356RQǻ6WUHVVEXWresulted in
a highly non-significant Setting effect (F3,41.77 = 0.140,
p
= 0.936), suggesting that PRS may be a
primary mediator of setting¶s effect on subjective stress.
Figur e 5. 3DUWLFLSDQW¶VUDWLQJVRIWKH3HUFHLYHGRestorativeness of Environmental Settings.
Figur e 6. Simple linear regression between Perceived Restorativeness (PRS) score and
FKDQJHLQ6XEMHFWLYH6WUHVVǻ6WUHVV.

Int. J. Environ. Res. Public Health
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10
1261
4. D iscussion
Trends suggest that differences in environmental settings did influence SDUWLFLSDQWV¶ OHYHOV RI
measureable stress. Salivary alpha-amylase elevation after exposure to the Very Built setting,
independent of any significant change in subjective stress, identifies a physiological response that is
separate from a conscious psychological component. Reductions in subjective stress after exposure to
the Very Natural setting relative to the Mostly Built settings are consistent with the stress-moderating
implications of PES suggested by Ulrich [24].
Data from analysis of the outcome measures was unable to support the hypotheses that natural
urban settings produce more beneficial changes in measures of physiological and psychological stress
relative to built urban settings. This was not unexpected considering the small sample size and low
statistical power of the study.
The low level of baseline stress among participants at Time2 (ݔҧ = 2.39, SD = 1.71; Scale 0±10)
indicates a near-floor effect regarding baseline stress level. The likelihood of detecting measurable
changes in stress, particularly after exposure to a mild and passive activity, was minimal. Therefore,
the common use of an initiating, pre-exposure stressor may be warranted in future studies so that more
robust physiological and psychological stress changes can be measured.
However, the presence of a statistically significant subjective stress difference between the Very
Natural and Mostly Built settings in this pilot study, despite a near-floor effect and low statistical
power, does suggest a potential environmental contribution to the moderation of stress. This evidence
suggests that natural environments have stress-reducing capacity beyond the restorative, therapeutic
action that occurs after exposure to an acute stressor. Natural urban settings may therefore be useful for
helping to create the supportive, upstream health-promotive environments that are the foundation for a
more sustainable urban living experience [11,48]. Further studies will be needed to determine the
VWUHQJWK DQG RU ³GRVH´ RI VXFK DQ H[SRVXUH WKH GXUDWLon of such effects, the effect of single
vs.
repeated exposures, and the repercussions on physical and mental health status and disease conditions.
The gender differences in outcome measures support previous evidence suggesting women and men
respond to environmental settings differently [44±46]. A greater decrease in subjective stress for
women after Very Natural setting exposure, but greater increase after Mostly Built exposure (when
men had a decrease) suggests that women may be more influenced by environmental conditions than
men, in either direction of the stress scale. Comments made by female and male participants during
debriefing did not demonstrate any gender differences in setting experiences, suggesting a
subconscious component may be involved. Future studies in this area may want to continue including
gender as a variable for analysis.
Mean EID score consistent with other sample means indicates participants were representative of
other populations regarding environmental self-identity. Correlation of EID with salivary outcome
measures suggests that individuals with greater personal environmental identification may be more
physiologically sensitive to their surroundings. However, this sensitivity may be generalized to all
environments and not specific to the setting content as evidenced by negligible changes in ANCOVA
models. Lack of correlation between EID and subjective stress markers suggests that physiologic
sensitivity may occur due to sensori-perceptual level processing independent of conscious awareness.
Further exploration of these mechanisms is warranted. Future studies investigating how environmental

Int. J. Environ. Res. Public Health
2013,
10
1262
setting differences influence healtK RXWFRPHV PD\ ZDQW WR LQFOXGH DQ LQGLYLGXDO¶V HQYLURQPHQWDO
self-identity in their analyses.
The mean PSS score below national average indicates a relatively relaxed sample population,
though this may reflect local or regional norms (data not available). Populations with different levels
of perceived baseline stress may experience different responses to setting exposures. Therefore,
the generalizability of study results is limited.
TKHPRGHUDWHO\VWURQJFRUUHODWLRQEHWZHHQ356DQGǻ6WUHVV suggests it is likely that restorativeness
LV D GLUHFW PHDVXUH RI D VHWWLQJ¶V SRWHQWLDO LPSDFW RQ VXEMHFWLYH VWUHVV UHJDUGOHVV RI D VHWWLQJ¶V
naturalness. ,W VKRXOG EH QRWHG WKDW D VHWWLQJ¶V UHVWRUDWLYHQHVV PD\ EH LQGHSHQGHQW IURP LWV
categorization along a natural/built continuum [49]. As such, perceived restorativeness can differ for
two settings of comparable naturalness [50,51]. For these reasons, future studies hoping to measure
outcome differences between exposures to natural and built settings may want to include PRS or other
subjective environmental setting measures in covariate analyses.
It is unsurprising that there was little overlap between the salivary measures sCort and sAA. A lag
of up to 18 min have been reported between the immediate-timed response of sAA and the delay-timed
response of sCort after exposure to an acute stressor [52]. The limited number of salivary data
collection points in this study does not allow for a full temporal correlation comparison between
measures. In addition, the collection of Time3 saliva after only 20 min of setting exposure may not
have been sufficient to capture the full cortisol response, given a potential 18 min delay. Lack of
congruent findings between the physiological and psychological measures reflects stress response
complexity, and demonstrates how a holistic approach to environmental stress research is necessary.
Li
m
itations
As mentioned, this pilot study was limited in its statistical power by a small sample size due to
budgetary and logistical constraints. Future studies seeking to explore this area of research should
consider including more participants. In addition, the recruitment of participants from the local
geographic area of a mid-sized city in the Pacific Northwest of the United States limits the
generalizability of this study.
Conducting an experimental field study introduces the potential for exposure to non-extraneous
variables, preventing attribution of study findings to the dependant variable and making it impossible
to empirically assess the validity of PES. These variables fluctuate within and between settings, as well
as within and between setting visits. This variability includes both a normal range (e.g., background
traffic noise of ~60 dB at the Mostly Built setting) and unforeseen outlier events (e.g., infrastructure
construction noise of ~80 dB at the Very Natural setting). 3DUWLFLSDQWV¶ FRPPHQWV PDGH GXULQJ
debriefing shows these extraneous variables influenced conscious experience of setting exposures and
directly influenced subjective stress measures. It is likely that salivary measures were also influenced
by these variables [53]. A list of variables mentioned by participants includes: noise, presence of
non-study personnel, past memories of setting visits, physical discomfort, air temperature, and odors.
Future field studies seeking to validate environmentally-moderated stress measures should control for
these factors by capturing relevant data to incorporate into data analysis models. Attempts at such
exploratory data capture methods were made with the current study for the acoustic environment,

Int. J. Environ. Res. Public Health
2013,
10
1263
but logistical issues prevented inclusion of useable data. Audio monitoring of setting decibel levels
was attempted, but the equipment used was only capable of recording isolated data at prescribed
time-points (
i.e.
, at Time2 and Time3). This proved to be insufficient for representing the actual
experience of participants in settings with greatly fluctuating soundscapes.
The collection of only two salivary data points provides minimal data for analysis. Collection of
multiple salivary data points before and after exposure would permit incorporation of highly variable
individualized daily cortisol patterns known [54,55] into data analysis while also extending the
post-exposure window of extended or delayed cortisol effects, as mentioned above.
The PRS was validated XVLQJ .DSODQ¶V $57 PRGHO and the relationship between this type of
restoration and stress has not been firmly established in the research literature. A more appropriate
instrument might include assessments of the attractiveness and/or aesthetics of an environment, which
are constructs XVHG LQ8OULFK¶V 3(6 PRGHOSuch instruments have been used by Dijkstra
et al
., [56]
and Karmanov and Hamel [49]. Use of the latter instrument may be particularly appropriate, as it
includes a bipolar scale for rating WKH ³QDWXUDOQHVV´ RI D VHWWLQJ The individualized data of
SDUWLFLSDQWV¶VXEMHFWLYHUDWLQJfrom this instrument would be more informative than the categorizations
assigned by study personnel, and could be incorporated into co-variate analyses. It should be noted
that, to the authors knowledge, neither of these instruments have been validated.
5. Conclusions
The purpose of this pilot study was to test a within-subjects methodology for measuring urban
HQYLURQPHQWDOVHWWLQJV¶ HIIHFWRQOHYHOVRIVWUHVV7KLVLQIRUPDWLRQLVLPSRUWDQWWRXQGHUVWDQGLQJKRZ
environments contribute to the accumulation of stress and how this information can be used to
positively affect health status in individuals and populations.
Though this study was not able to validate the hypothesis that natural urban environments have a
greater ability to positively affect unprovoked
de novo
levels of stress than built urban environments,
the presence of multiple extraneous variables cannot rule-out the possibility that such an effect occur.
Future studies looking to utilize an experimental field study design should control for these variables
(e.g., noise, past exposures, non-study personnel,
etc
.). Consideration of environmental self-identity,
perceived restorativeness and pre-existing levels of stress should be included as co-variates, and data
should be analyzed by gender. Further studies are needed to determine what the effects on chronic or
repeat exposures to environments might be, and if measuring the effect of these repeat exposure visits
supports the epidemiological evidence.
Acknowledgements
This project was sponsored by NIH NCCAM Award 2R25AT002878-05A1. Thanks to the Helfgott
Research Institute of the National College of Natural Medicine, including Heather Zwickey, Mayen
Dada, Amy Goldfeder, Eric Jorgenson, Corey McAuliffe, Lindsay Rogers and Bethany Tennant.
Thanks also to Portland Parks and Recreation Department for use of Hoyt Arboretum-Stevens Pavilion
Picnic Shelter, and to ZRT Laboratory for providing cortisol analysis of saliva samples.

Int. J. Environ. Res. Public Health
2013,
10
1264
Conflict of I nterest
The authors declare no conflict of interest.
References
1. Dooris, M. Expert voices for change: Bridging the silos-towards healthy and sustainable settings
for the 21st century.
Health Place
2013,
20
, 39±50.
2. WHO Ottawa Charter for Health Promotion.
First International Conference on Health
Pro
m
otion
; World Health Organization: Ottawa, Canada,
1986; pp. 1±4.
3. Dannenberg, A.L.; Jackson, R.; Frumkin, H.; Schieber, R.A.; Pratt, M.; Kochtitzky, C.;
Tilson, H.H. The impact of community design and land-use choices on public health: A scientific
research agenda.
A
m
. J. Public Health
2003,
93
, 1500±1508.
4. Hancock, D.; Duhl, L.
WH O Healthy C ities Project: Pro
m
oting Health in the Urban Context
;
World Health Organization: Geneva, Switzerland, 1988; pp. 1±54.
5. CDC Designing and Building Healthy Places. Available online: http://www.cdc.gov/
healthyplaces/default.htm (accessed on 29 October 2012).
6. State of World Population 2007: Unleashing the Potential of Urban Growth; United Nations
Population Fund (UNFPA): New York, NY, USA, 2007.
7. Peen, J.; Schoevers, R.A.; Beekman, A.T.; Dekker, J. The current status of urban-rural differences
in psychiatric disorders.
Acta Psychiatr.
S
cand.
2010,
121
, 84±93.
8. Dhingra, S.S.; Strine, T.W.; Holt, J.B.; Berry, J.T.; Mokdad, A.H. Rural-urban variations in
psychological distress: Findings from the behavioral risk factor surveillance system, 2007.
Int. J.
Public Health
2009,
54
, 16±22.
9. Verheij, R.A.; Maas, J.; Groenewegen, P.P. Urban-rural health differences and the availability of
green space.
Eur. U rban Reg.
S
tud.
2008,
15
, 307±316.
10. Kuo, F.E. Parks and other green environments: Essential components of a healthy human habitat.
Australas. Parks Leisure
2010,
14
, 1±48.
11. Maller, C.; Townsend, M.; Pryor, A.; Brown, P.; St Leger, L. Healthy nature healthy people:
³Contact with nature´ as an upstream health promotion intervention for populations.
Health Pro
m
ot. Int.
2006,
21
, 45±54.
12. Frumkin, H. Beyond toxicity: Human health and the natural environment.
A
m
. J. Prev. Med.
2001,
20
, 234±240.
13. Maas, J.; Verheij, R.A.; De Vries, S.; Spreeuwenberg, P.; Schellevis, F.G.; Groenewegen, P.P.
Morbidity is related to a green living environment.
J. Epide
m
iol. Co
mm
unity Health
2009,
63
,
967±973.
14. Mitchell, R.J.; Popham, F. Effect of exposure to natural environment on health inequalities:
An observational population study.
Lancet
2008,
372
, 1655±1660.
15. Richardson, E.A.; Mitchell, R.J.; Hartig, T.; de Vries, S.; Astell-Burt, T.; Frumkin, H. Green cities
and health: A question of scale?
J. Epide
m
iol. Co
mm
unity Health
2012,
66
, 160±165.

Int. J. Environ. Res. Public Health
2013,
10
1265
16. Thompson, C.W.; Roe, J.J.; Aspinall, P.; Mitchell, R.J.; Clow, A.; Miller, D. More green space is
linked to less stress in deprived communities: Evidence from salivary cortisol patterns.
Landsc.
Urban Plan.
2012,
105
, 221±229.
17. Van den Berg, A.E.; Maas, J.; Verheij, R.A.; Groenewegen, P.P. Green space as a buffer between
stressful life events and health.
S
oc.
S
ci. Med.
2010,
70
, 1203±1210.
18. Lottrup, L.; Grahn, P.; Stigsdotter, U.K. Workplace greenery and perceived level of stress:
Benefits of access to a green outdoor environment at the workplace.
Landsc. Urban Plan.
2013,
110
, 5±11.
19. Largo-Wight, E.; Chen, W.W.; Dodd, V.; Weiler, R. Healthy workplaces: The effects of nature
contact at work on employee stress and health.
Public Health Rep.
2011,
126
, 124±130.
20. Lohr, V.I.; Pearson-Mims, C.H.; Goodwin, G.K. Interior plants may improve worker productivity
and reduce stress in a windowless environment.
J. Environ. Hortic.
1996,
14
, 97±100.
21. Beukeboom, C.J.; Langeveld, D.; Tanja-Dijkstra, K. Stress-reducing effects of real and artificial
nature in a hospital waiting room.
J. Altern. Co
m
ple
m
ent. Med.
2012,
18
, 329±333.
22. Alvarsson, J.; Wiens, S.; Nilsson, M.E. Stress recovery during exposure to nature sound and
environmental noise.
Int. J. Environ. Res. Public Health
2010,
7
, 1036±1046.
23. Ulrich, R.S. View through a window may help recovery from surgery.
S
cience
1984,
224
,
420±421.
24. Ulrich, R.S.; Simons, R.F.; Losito, B.D.; Fiorito, E.; Miles, M.A.; Zelson, M. Stress recovery
during exposure to natural and urban environments.
J. Environ. Psychol.
1991,
11
, 201±230.
25. Ulrich, R.S. Natural versus urban scenes: Some psychophysiological effects.
Environ. Behav.
1981,
13
, 523±556.
26. Wilson, E.O.
Biophilia
; Harvard University Press: Cambridge, MA, USA, 1984.
27. Grinde, B.; Patil, G.G. Biophilia: Does visual contact with nature impact on health and
well-being?
Int. J. Environ. Res. Public Health
2009,
6
, 2332±2343.
28.
S
tress in A
m
erica: Our Health at Risk
; American Psychological Association: Washington, DC,
USA, 2012; pp. 1±78.
29. Larzelere, M.M.; Jones, G.N. Stress and health.
Pri
m
. C are
2008,
35
, 839±856.
30. Engert, V.; Vogel, S.; Efanov, S.I.; Duchesne, A.; Corbo, V.; Ali, N.; Pruessner, J.C. Investigation
into the cross-correlation of salivary cortisol and alpha-amylase responses to psychological stress.
Psychoneuroendocrinology
2011,
9
, 1294±1302.
31. Park, B.-J.; Tsunetsugu, Y.; Kasetani, T.; Kagawa, T.; Miyazaki, Y. The physiological effects of
Shinrin-Yoku (taking in the forest atmosphere or forest bathing): Evidence from field experiments
in 24 forests across Japan.
Environ. Health Prev. Med.
2010,
15
, 18±26.
32. Yamaguchi, M.; Deguchi, M.; Miyazaki, Y. The effects of exercise in forest and urban
environments on sympathetic nervous activity of normal young adults.
J. Int. Med. Res.
2006,
34
,
152±159.
33. Van den Berg, A.E.; Custers, M.H.G. Gardening promotes neuroendocrine and affective
restoration from stress.
J. H ealth Psychol.
2010,
16
, 3±11.
34. Hartig, T.; Evans, G.W.; Jamner, L.D.; Davis, D.S.; Gärling, T. Tracking restoration in natural
and urban field settings.
J. Environ. Psychol.
2003,
23
, 109±123.

Int. J. Environ. Res. Public Health
2013,
10
1266
35. Matsuoka, R.H. Student performance and high school landscapes: Examining the links.
Landsc. Urban Plan.
2010,
97
, 273±282.
36. Nater, U.M.; Rohleder, N.; Gaab, J.; Berger, S.; Jud, A.; Kirschbaum, C.; Ehlert, U. Human
salivary alpha-amylase reactivity in a psychosocial stress paradigm.
Int. J. Psychophysiol. Off. J.
Int. Organ. Psychophysiol.
2005,
55
, 333±342.
37. Clayton, S. Environmental identity: A conceptual and an operational definition. In
Identity and
the Natural Environ
m
ent: The Psychological
S
ignificance of Nature
; Clayton, S., Opotow, S.,
Eds.; MIT Press: Cambridge, MA, USA, 2003; pp. 45±65.
38. Hinds, J.; Sparks, P. Engaging with the natural environment: The role of affective connection and
identity.
J. Environ. Psychol.
2008,
28
, 109±120.
39. Cohen, S.; Kamarck, T.; Mermelstein, R. A global measure of perceived stress.
J. Health
S
oc.
Behav.
1983,
24
, 385±396.
40. Hartig, T.; Korpela, K.M.; Evans, G.W.; Garling, T. A measure of restorative quality in
environments.
S
cand. Hous. Plan. Res.
1997,
14
, 175±194.
41. Kaplan, S. The restorative benefits of nature: Toward an integrative framework.
J. Environ.
Psychol.
1995,
15
, 169±182.
42. Chang, C.Y.; Hammitt, W.E.; Chen, P.; Machnik, L.; Su, W. Psychophysiological responses and
restorative values of natural environments in Taiwan.
Landsc. Urban Plan.
2008,
85
, 79±84.
43. Berto, R. Exposure to restorative environments helps restore attentional capacity.
J. Environ.
Psychol.
2005,
25
, 249±259.
44. Richardson, E.A.; Mitchell, R.J. Gender differences in relationships between urban green space
and health in the United Kingdom.
S
oc.
S
ci. Med.
2010,
71
, 568±575.
45. Mair, C.; Cutchin, M.; Peek, M.K. Allostatic load in an environmental riskscape: The role of
stressors and gender.
Health Place
2011,
17
, 978±987.
46. Takai, N.; Yamaguchi, M.; Aragaki, T.; Eto, K.; Uchihashi, K.; Nishikawa, Y. Gender-specific
differences in salivary biomarker responses to acute psychological stress.
Ann. New York Acad.
S
ci.
2007,
1098
, 510±515.
47. Cohen, S.; Janicki-'HYHUWV ' :KR¶V stressed? Distributions of psychological stress in the
United States in probability samples from 1983, 2006, and 2009.
J. Appl.
S
oc. Psychol.
2012,
42
,
1320±1334.
48. Van den Berg, A.E.; Hartig, T.; Staats, H. Preference for nature in urbanized societies: Stress,
restoration, and the pursuit of sustainability.
J.
S
oc. Issues
2007,
63
, 79±96.
49. Karmanov, D.; Hamel, R. Assessing the restorative potential of contemporary urban
environment(s): Beyond the nature versus urban dicotomy.
Landsc. Urban Plan.
2008,
86
,
115±125.
50. Hauru, K.; Lehvävirta, S.; Korpela, K.M.; Kotze, D.J. Closure of view to the urban matrix has
positive effects on perceived restorativeness in urban forests in Helsinki, Finland.
Landsc. U rban
Plan.
2012,
107
, 361±369.
51. Tenngart Ivarsson, C.; Hagerhall, C.M. The perceived restorativeness of gardens-assessing
the restorativeness of a mixed built and natural scene type.
Urban Forest Urban Green.
2008,
7
,
107±118.

Int. J. Environ. Res. Public Health
2013,
10
1267
52. Takai, N.; Yamaguchi, M.; Aragaki, T.; Eto, K.; Uchihashi, K.; Nishikawa, Y. Effect of
psychological stress on the salivary cortisol and amylase levels in healthy young adults.
Arch.
Oral Biol.
2004,
49
, 963±968.
53. Martimportugués-Goyenechea, C.; Gómez-Jacinto, L. Simultaneous multiple stressors in the
environment: Physiological stress reactions, performance, and stress evaluationitle.
Psychol. Rep.
2005,
97
, 867±874.
54. Stone, A.A.; Schwartz, J.E.; Smyth, J.; Kirschbaum, C.; Cohen, S.; Hellhammer, D.; Grossman, S.
Individual differences in the diurnal cycle of salivary free cortisol: A replication of flattened
cycles for some individuals.
Psychoneuroendocrinology
2001,
26
, 295±306.
55. Fries, E.; Dettenborn, L.; Kirschbaum, C. The cortisol awakening response (CAR): Facts and
future directions.
Int. J. Psychophysiol.
2009,
72
, 67±73.
56. Dijkstra, K.; Pieterse, M.E.; Pruyn, A.T.H. Stress-reducing effects of indoor plants in the built
healthcare environment: The mediating role of perceived attractiveness.
Prev. Med.
2008,
47
,
279±283.
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