Autonomic and emotional responses after transdermal absorption of sweet orange oil in humans: Placebo controlled trial

Abstract

Essential oils are used increasingly for the improvement in quality of life and relief of various symptoms
in patients, but scientific validation is still rare. The aim of this study was to investigate the effect of sweet
orange oil (Citrus sinensis, Rutaceae) on human autonomic parameters and emotional responses in healthy
subjects after transdermal absorption. In order to exclude any olfactory stimulation, the inhalation of the
fragrances was prevented by breathing masks. Thirty nine healthy volunteers participated in the experiments.
Four autonomic parameters, i.e. blood pressure, breathing rate, pulse rate and skin temperature were
recorded. Emotional responses were assessed by means of rating scales. Compared to placebo, sweet
orange oil caused significant decreases of breathing rate and pulse rate which indicate a decrease of
autonomic arousal. At the emotional level, subjects in the sweet orange oil group rated themselves more
cheerful and more vigorous than subjects in the control group. This finding suggests an increase of arousal
in terms of self-evaluation

Full text

Introduction
The essential oil of sweet orange oil (Citrus sinensis,
Rutaceae) is widely used as a fragrance in food, perfumery,
and cosmetic industries. The oil has been associated with
antimicrobial activity [1, 2]. Insecticidal activity of sweet
orange oil has been demonstrated by Shalaby et al. [3].
During an in vitro study, the oil and its main component,
limonene, had a spasmogenic effect on guinea-pig ileum
smooth muscle [4]. Lehrner et al. [5] reported that ambient
odours of orange oil reduced anxiety and improved mood
in patients waiting for dental treatment. A mixture of citrus
oils helps to reduce the therapeutic doses of antidepressants
in depressive patients [6]. Aromatherapy massage using
sweet orange oil weekly for 4 weeks improves depressive
states in patients by increasing blood ow to the prefrontal
cortex [7]. Additionally, stress relieving properties could be
attributed to sweet orange oil measuring salivary cortisol
concentrations [8].
Presently, there are a variety of approaches to evaluate
the physiological and psychological effects of fragrances
such as measuring changes in autonomic parameters, e.g.
heart rate, breathing rate, blood pressure, eye-blinks, skin
temperature and skin conductance [9-14], changes in brain
wave activities, e.g. electroencephalogram, contingent
negative variation [15-18], changes in mood, cognitive
performances and emotion [19-23].
Although many researchers have attempted to prove the
scientic effects of aromatherapy, many aromatherapy
studies were not controlled and results are therefore
potentially biased. To date, no controlled experiments
on the effects of sweet orange oil on human autonomic
parameters and emotional measures after transdermal
administration have been carried out. Therefore, the main
objective of the present study was to investigate the effects
International Journal of
Essential Oil Therapeutics
www.ijeot.com
Autonomic and emotional responses after transdermal
absorption of sweet orange oil in humans: placebo
controlled trial
T. Hongratanaworakit a*, G. Buchbauer b
a Department of Pharmaceutical Chemistry, Faculty of Pharmacy, Srinakharinwirot University,
Rangsit-ongkharak Rd., Nakhon-nayok 26120, Thailand
b Department of Clinical Pharmacy and Diagnostics, Faculty of Life Sciences, University of Vienna,
Althanstrasse 14, A-1090 Vienna, Austria.
Abstract
Essential oils are used increasingly for the improvement in quality of life and relief of various symptoms
in patients, but scientic validation is still rare. The aim of this study was to investigate the effect of sweet
orange oil (Citrus sinensis, Rutaceae) on human autonomic parameters and emotional responses in healthy
subjects after transdermal absorption. In order to exclude any olfactory stimulation, the inhalation of the
fragrances was prevented by breathing masks. Thirty nine healthy volunteers participated in the experiments.
Four autonomic parameters, i.e. blood pressure, breathing rate, pulse rate and skin temperature were
recorded. Emotional responses were assessed by means of rating scales. Compared to placebo, sweet
orange oil caused signicant decreases of breathing rate and pulse rate which indicate a decrease of
autonomic arousal. At the emotional level, subjects in the sweet orange oil group rated themselves more
cheerful and more vigorous than subjects in the control group. This nding suggests an increase of arousal
in terms of self-evaluation.
Key words: Autonomic nervous system, massage aromatherapy, emotional evaluation, Citrus sinensis
EORC
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* Corresponding author.
E-mail address: tapanee@swu.ac.th
© Essential Oil Resource Consultants. All rights reserved.
29
International Journal of Essential Oil Therapeutics (2007) 1, 29-34

of this fragrance compound on autonomic nervous system
parameters as well as on mental and emotional condition
in healthy human volunteers following transdermal
absorption.
Materials and methods
Subjects and essential oil
Thirty nine healthy volunteers aged between 18 and 48
years (mean age 23.18 ± 1.01 years) took part in the
experiments. Demographic data for the control group
and the experimental group are presented in Table 1.
Subjects were tested in individual sessions and randomly
assigned to either the control group or the sweet orange
oil group according to random numbers. They were fully
briefed, gave written informed consent to all aspects of
the study (Srinakharinwirot University Ethic Committee)
and were free to withdraw at any time. Forty-eight hours
prior to testing subjects were asked to abstain from food,
beverages and toiletries containing the essential oil of
Citrus species or its constituents (e.g. limonene), i.e. citrus
fruits, apricots, peaches, fruit juices, basil, coriander, thyme,
cinnamon, geranium, and bergamot, as well as from any
stimulants (e.g. caffeine and nicotine).
Table 1. Demographic data for the control group and the
experimental sweet orange oil group.
parameters control experimental
N. of volunteers sex 20 19
sex (M:F) 12:8 11:8
height (mean±SD) cm M 172.75±6.01 172.72±4.98
F 159.91±4.81 161.13±7.53
weight (mean±SD) cm M 63.12±5.64 60.66±5.58
F 55.66±8.73 54.63±8.60
Sweet orange oil was extracted by pressing fresh peel from
the fruits of Citrus sinensis (L.) Osbeck. (available from FPI
Sale Ltd., Stamford England). The oil was analyzed by the gas
chromatography/ame ionization detector (GC/FID) and
the gas chromatography/mass spectrometry (GC/MS). GC/
FID was performed using a Perkin-Elmer AutoSystem gas
chromatograph tted with a fused-silca PB-WAX capillary
column (60 m, 0.25 mm, 0.32 µm lm thickness). Column
temperature was 90oC, 4 min and then was programmed
from 90-220oC at 10oC/min, held isothermal at this
temperature for 3 min. Injector and detector temperatures
were 190oC and 220oC, respectively. The carrier gas was
helium at 1.0 ml/min. The samples (1.5 µl) were injected
using a split ratio of 1:10. GC/MS was carried out on a
Trace GC Ultra /Trace DSG Finnigan gas chromatograph
tted with a fused-silca BPX5 capillary column (30 m, 0.25
mm, 0.25 µm lm thickness). Column temperature was
60oC, 1 min and then was programmed from 60-240oC
at 3.3oC/min, held isothermal at this temperature for 5
min. Injector and detector temperatures were 180oC and
220oC, respectively. The carrier gas was helium at 1.0 ml/
min. A split ratio was at 1:100. The oil mainly contains d-
limonene (96.27%). The minor components are b-myrcene
(1.21%), limonene oxide (0.81%), a-pinene (0.51%), b-
linalool (0.33%) and carvone (0.19%).
Essential oil administration
In the experimental group, 1 ml of a 20% (w/w) solution
of sweet orange oil in sweet almond oil was applied to the
skin of the lower abdomen of each subject and the subjects
self-massaged the oil into the skin for 5 min. Afterwards
the massage area was covered with a plastic lm in order
to prevent evaporation of the oil. In the control group, 1 ml
of the placebo oil, pure sweet almond oil, was used. In both
groups subjects were supplied with pure air by breathing
masks (inhalation set for adult, product no.1500004020,
B+P Beatmungsprodukte GmbH, Neunkirchen, Germany)
in order to eliminate any olfactory stimulation by nose or
mouth.
Experimental protocol
The experimental protocol has been previously described
by our group [24-28]. One session consisted of two
trials of 20 min each. At the beginning and at the end of
each trial, emotional responses were assessed by visual
analogue scales (VAS). VAS consisted of 100 mm lines for
six items: relaxation, vigour, calmness, attentiveness, mood
and alertness. Each subject was asked to mark his or her
feeling for each item between the two possible extremes:
relaxed (on the left) and tense (on the right) for the
item ‘relaxation’
vigorous (on the left) and feeble (on the right) for the
item ‘vigour’
calm (on the left) and restless (on the right) for the
item ‘calmness’
attentive (on the left) and inattentive (on the right) for
the item ‘attentiveness’
cheerful (on the left) and bad tempered (on the right)
for the item ‘mood’
alert (on the left) and tired (on the right) for the item
‘alertness’.
Autonomic parameters i.e., breathing rate (BR), pulse rate
(PR), skin temperature (ST), systolic and diastolic blood
pressure (SBP and DBP) were recorded continuously
during each trial. In the rst trial, which served as a control
for inuences of the experimental setup, the placebo
substance was administered to all subjects. In the second
trial the placebo was again administered to the control
group, whereas in the experimental group the essential oil
was administered.
Procedure
All experiments were conducted in a bright and quiet
room. Ambient temperature was 24-26oC. Upon arrival,
the volunteers were interviewed about their personal
data, e.g. sex, age, height, weight. In addition, they were
asked about the rating of emotional responses. After
completion of the interview and the rating scales, SBP and
DBP were measured. Subsequently, subjects were seated
in a semi-reclined position, providing easy access to attach
the ANS electrodes or probes. BR was measured using
a MLT415 surface temperature thermistor probe which
registers breathing cycles on the basis of the difference in
temperature between inhaled and exhaled air. The probe
was placed at the entrance of the left nostril with non-
caustic adhesive tape. PR was measured using a MLT1010
pulse transducer. The non-invasive pulse transducer was
placed on the rst phalanx of the ring nger with non-
•
•
•
•
•
•
30 International Journal of Essential Oil Therapeutics (2007) 1, 29-34

caustic adhesive tape. ST was measured using a MLT409
fast response thermistor. The sensor was placed on the
middle of the back of the hand with non-caustic adhesive
tape. The breathing mask was tted to the volunteer’s
face to cover the nose and mouth. The oxygen was then
supplied directly. The oil or the placebo was administered
as described together with recording of the autonomic
parameters. After completion of the rst trial, the subjects
were asked to rate the VAS. SBP and DBP were also
measured at the end of the rst trial. This procedure
was repeated in the second trial. At the end of each trial,
the subjects were asked if they had perceived any odour
during the experiment. All subjects stated that they did not
perceive any odour during the experiment.
Acquisition of autonomic parameters and statistical analysis
BR, PR and ST were measured using Power Lab/4SP
hardware (ADInstruments, Inc., NSW, Australia). Sampling
rate was 100 Hz. SBP and DBP were determined by
sphygmomanometry using an automated system (Digital
Electronic Model DS-155E, Japan). Details of the recording
system and procedure have been described elsewhere
[24-28]. VAS, i.e., relaxation, vigour, calmness, attentiveness,
mood and alertness, were used to assess emotional
responses. All statistical calculations and data analyses
were performed with the Statistical Package for the Social
Sciences (SPSS version 11.5). The effects of fragrances on
autonomic parameters and ratings of emotional responses
were determined by Mann-Whitney-U-Test analysis of
variances. Correlational analyses between ratings of
emotional responses and autonomic parameters were
performed by means of Spearman rank-order correlation
coefcient.
Results
Autonomic parameters
The mean difference scores and standard error mean
(SEM) of breathing rate between the second trial and the
rst trial for the control group and the sweet orange oil
group are shown in Figure 1.
-1.5
-1
-0.5
0
0.5
1
1.5
Breathing rate (difference score
)
control sweet orange oil
Fig. 1. The mean difference scores and SEM of breathing
rate for the control group and the orange oil group.
The breathing rate of subjects in the control group
increased in the second trial compared with the rst trial.
In contrast, the breathing rate of subjects in the sweet
orange oil group decreased in second trial compared
with the rst trial. Comparison of these difference scores
revealed a signicantly larger decrease of breathing rate in
the sweet orange oil group than in the control group (p
= 0.038).
The mean difference scores and SEM of pulse rate between
the second trial and the rst trial for the control group
and the sweet orange oil group are shown in Figure 2. The
pulse rate of subjects in the control group only changed
marginally in the second trial compared with the rst trial.
In contrast, the pulse rate of subjects in the sweet orange
oil group decreased in second trial compared with the
rst trial. Comparison of these difference scores revealed
a signicantly larger decrease of pulse rate in the sweet
orange oil group than in the control group (p = 0.036).
-1
0
1
2
3
4
5
P ulse rate (difference score)
control sweet orange oil
Fig. 2. The mean difference scores and SEM of pulse rate
for the control group and the sweet orange oil group.
No signicant effects of the sweet orange oil on systolic
blood pressure, diastolic blood pressure and skin
temperature were found (p > 0.05 for all).
Emotional responses
The mean difference scores and SEM of subjective mood
between the second trial and the rst trial for the control
group and the sweet orange oil group are shown in Figure
3. Subjects in the control group felt less cheerful at the end
of the second trial compared with the end of the rst trial.
In contrast, subjects in the sweet orange oil group judged
themselves more cheerful at the end of the second trial
compared with the end of the rst trial. Comparison of
these difference scores revealed a signicant increase of
subjective mood in the sweet orange oil group compared
with the control group (p = 0.012).
In addition, subjects in the control group and the sweet
orange oil group felt more vigorous at the end of the
second trial compared with the end of the rst trial. The
31
International Journal of Essential Oil Therapeutics (2007) 1, 29-34

mean difference scores and SEM of subjective vigour
between the second trial and the rst trial for the control
group and the sweet orange oil group are shown in Figure
4. Comparison of these difference scores revealed a
signicant increase of subjective vigour in the sweet orange
oil group as compared to the control group (p = 0.035).
-6
-4
-2
0
2
4
6
8
10
Mood (differenc e score)
control sweet orange oil
Fig. 3. The mean difference scores and SEM of subjective
mood for the control group and the sweet orange oil
group.
-2
0
2
4
6
8
10
12
Vigor (difference score)
control sweet orange oil
Fig. 4. The mean difference scores and SEM of subjective
vigour for the control group and the sweet orange oil
group.
No signicant effects of the sweet orange oil on subjective
attentiveness, alertness, calmness, and relaxation were
found (p > 0.05 for all).
Correlations
The Spearman rank-order correlation coefcient (ρ) was
used to analyze interaction between ratings of emotional
responses and autonomic parameters. With a sample
size of n = 20, ρ ≥ |0.379| is considered to be statistically
signicant at the 0.05 level [29]. In the sweet orange oil
group, changes of subjective mood were correlated with
changes of pulse rate: the more cheerful subjects rated
themselves, the less the pulse rate increased (ρ = +0.631).
Additionally, interactions between changes of subjective
vigour and pulse rate were found: the more vigorous
subjects judged themselves, the more the pulse rate
decreased (ρ = +0.566).
Discussion
In the present investigation essential sweet orange oil
was administered to healthy young adult volunteers by
transdermal absorption. Autonomic parameters, i.e. blood
pressure, pulse rate, breathing rate, and skin temperature,
were recorded as indicators of the arousal level of the
autonomic nervous system (ANS). In addition, subjects
had to rate their mental and emotional condition in terms
of relaxation, vigour, calmness, attentiveness, mood, and
alertness in order to assess subjective emotional arousal.
Transdermal absorption of sweet orange oil affected
breathing rate and pulse rate. Transdermal absorption
of sweet orange oil led to a signicant decrease of
pulse rate. Since pulse rate is mainly controlled by the
autonomic nervous system, the decrease of pulse rate
after transdermal absorption of sweet orange oil is likely
to show an increase in vagal tone, i.e., a decrease of ANS
arousal. The change in the cardiovascular parameters, i.e.
pulse rate, was consistent with a decrease of peripheral
autonomic nervous activity.
In addition, transdermal absorption of sweet orange oil
led to a signicant decrease of breathing rate. In general,
the cardiovascular system has a relationship with the
respiratory system. Muscle sympathetic nerve activity was
associated with respiratory function, namely, reduction in
respiratory rate leads to a decrease of muscle sympathetic
activity [30]. Furthermore, a decrease of breathing rate
may cause an increase of baroreceptor sensitivity and a
decrease of pulse rate [31].
At the emotional level, transdermal absorption of sweet
orange oil led to changes in subjective mood and vigour.
Subjects in the sweet orange oil group rated themselves
more cheerful and more vigorous than subjects in the
control group. These ndings show an increase of arousal
in terms of self-evaluation. Correlational analyses showed
that changes of subjective mood and vigour were correlated
with changes of pulse rate in sweet orange oil group. The
more pulse rate decreased in subjects in the sweet orange
oil group, the more cheerful and the more vigorous they
judged themselves. Obviously, a decrease of autonomic
activation, i.e. a decrease of pulse rate, was correlated with
an increase of arousal at the subjective level, i.e. increases
of subjective mood and vigour.
The observed effects of essential sweet orange oil are not
precisely characterized by concepts such as relaxation or
sedation, since deactivation on both the autonomic level
and on the level of self-evaluation is associated with these
concepts. Transdermal absorption of sweet orange oil,
however, reduced the level of arousal of the autonomic
32 International Journal of Essential Oil Therapeutics (2007) 1, 29-34

nervous system but did not lead to deactivation at the
behavioural level, i.e. after the administration of the oil
subjects did not feel more relaxed or calm, but in contrast
reported to feel more cheerful and more vigorous than
before the administration of the oil. Thus, the effects
of essential sweet orange oil may be characterized by
the concept of ‘harmonization’ rather than relaxation/
sedation which has also been described for the essential
oils of lavender [32], sandalwood [27] and ylang ylang [28].
This harmonization is also in line with the stress relieving
effect of sweet orange oil as recently shown by decrease of
cortisol in saliva samples [8]. The decrease of breathing rate
was not correlated with changes in emotional responses.
These ndings suggest the effectiveness of pharmacological
mechanisms, e.g. direct interactions between fragrance
molecules and receptor sites that are involved in the
regulation of ANS arousal. Due to their high lipophilicity,
fragrance molecules easily penetrate the blood brain
barrier and enter the brain following massage [33].
Therefore, one possibility that explains the effect of the
sweet orange oil could be that the oil possibly deactivates
the locus ceruleus in the brain into releasing noradrenalin,
a neurotransmitter that creates a stimulating/ activating
effect. The locus ceruleus is also involved in arousal and
activation [34]. Another possibility that explains its effect
could be that sweet orange oil exerts its effects by an
interaction with central (e.g. hypothalamic, limbic, thalamic)
structures that control the level of autonomic and/ or
behavioural arousal.
However, our previous studies reported that inhalation
of sweet orange oil and its main component, limonene,
increased both the level of autonomic arousal and the
level of emotional arousal which are likely to represent a
stimulating effect of the oil [26, 35]. All our ndings indicate
that differential effects of the essential oils depend on
mode/route of administration. Both pharmacological and
psychological effects are active simultaneously when the
oils are administered by means of inhalation and olfactory
processing occurs. In contrast, percutaneous administration
gives evidence for a primarily pharmacological effect and
exclusion of olfactory processing. Therefore, in order to
differentiate between pharmacological and psychological
effects of fragrances, subjective evaluation of the odours
must be prevented [21, 24-28, 35].
In conclusion, transdermal absorption of sweet orange
oil led to deactivation at the level of ANS arousal but did
not lead to deactivation at the behavioural level, i.e. after
the administration of the oil, subjects felt more cheerful
and more vigorous than before the administration of
the oil. Therefore, the effects of sweet orange oil may be
characterized by the concept of ‘harmonization’. These
ndings also furnish further scientic proof for the use
of the sweet orange oil in aromatherapy for the relief of
depression and stress in humans.
Acknowledgements
This work was supported by grants from Srinakharinwirot
University, Thailand. The author is grateful to Dr. E.
Heuberger, University of Vienna, Austria, for experimental
design suggestion.
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