THE JOURNAL OF ALTERNATIVE AND COMPLEMENTARY MEDICINE Volume 20,Number 9,2014,pp.727-731 Mary Ann Liebert,Inc. D0l10.1089/acm.2014.0029 Effect of Olfactory Stimulation by Fresh Rose Flowers on Autonomic Nervous Activity Miho Igarashi,MPhil,*Chorong Song.MAgr:Harumi lkei,BAgr, Tatsuro Ohira,PhD,2 and Yoshifumi Miyazaki,PhD1 Abstract Objective:To clarify the effect of olfactory stimulation by fresh rose flowers,which exude a strong fragrance, on heart rate variability. Settings:A chamber with an artificial climate maintained at 25C with 50%relative humidity and 230 lux illumination at the Center for Environment,Health,and Field Sciences,Chiba University,Japan. Participants:Nineteen female university and graduate students(mean age,21.6+1.5 years;age range,19.0-26.0 years). Interventions:Fresh rose flowers as an olfactory stimulant,with air as a control. Outcome measures:Heart rate variability and subjective evaluations.The power levels of the high-frequency (HF)(0.15-0.40 Hz)and low-frequency (LF)(0.04-0.15Hz)components of heart rate variability were calcu- lated by the maximum-entropy method.The HF power was considered to reflect parasympathetic nervous activity.The LF/HF power ratio was determined to reflect the sympathetic nervous activity.A modified semantic differential method was used to perform subjective evaluations. Results:Fresh rose flowers induced (1)a significant increase in parasympathetic nervous activities and(2)an increase in“comfortable”and“natural'feelings. Conclusion:The findings indicated that olfactory stimulation by fresh rose flowers induced physiological and psychological relaxation. Introduction untreated migraine attacks.In addition,Fukui et al.reported that rose odor (essential oil of Rosa alba)inhalation de- N MODERN SOCIETIES,individuals are exposed to many creases cortisol levels in healthy volunteers.3 Fukada et al. stressors in daily life,-4 and consequently,many indi- showed that inhaling odor of rose essential oil (R.alba) viduals seek contact with nature to relax.One means of inhibits increases in salivary cortisol and skin-barrier dis- achieving contact with nature is viewing fresh flowers,such ruption in humans exposed to stress.Regarding subjec- as roses.Roses are among the most popular flowers,are a tive evaluations of effects,Ayan et al.used a visual analog common gift for women,and are used to decorate rooms. scale of pain scores ranging from"no pain"to "very severe The authors'earlier study showed that visual stimulation pain''to demonstrate that inhalation of odor of rose essential by fresh rose flowers (Rosa "Dekora")induces physiolog- oil (R.damascena)is a useful supplementary and adjunctive ical relaxation in female medical staff.To date.few studies therapy for relieving renal colic.Thus,the effects of o have evaluated the physiological effects of the odor of roses factory stimulation by rose extracts,including rose essential on humans.Inhalation of the odor of rose essential oil (Rosa oil,have been investigated using both physiological and damascena MILL.)decreases relative sympathetic activity subjective evaluations. and adrenaline concentration in healthy adults.Moreover. The present study is novel in many respects.First,no Stankewitz et al.explored neuronal processing in response previous study has been performed using fresh rose flowers to olfactory stimulation with rose oil in patients with mi- Second,no other study has evaluated the physiological ef- graine by using event-related functional magnetic reso- fects of olfactory stimulation by fresh rose flowers on wo- nance imaging and found that the odor of rose oil induces men from the perspective of autonomic nervous activity, significantly higher blood oxygen level-dependent signal particularly by assessing heart rate variability(HRV),which intensities in several brain areas during spontaneous and is a measure of sympathetic and parasympathetic nervous Center for Environment,Health,and Field Sciences,Chiba University,Chiba,Japan. Forestry and Forest Products Research Institute,Ibaraki,Japan. *Co-first authors. 727
Effect of Olfactory Stimulation by Fresh Rose Flowers on Autonomic Nervous Activity Miho Igarashi, MPhil,1,* Chorong Song, MAgr,1,* Harumi Ikei, BAgr,1 Tatsuro Ohira, PhD,2 and Yoshifumi Miyazaki, PhD1 Abstract Objective: To clarify the effect of olfactory stimulation by fresh rose flowers, which exude a strong fragrance, on heart rate variability. Settings: A chamber with an artificial climate maintained at 25C with 50% relative humidity and 230 lux illumination at the Center for Environment, Health, and Field Sciences, Chiba University, Japan. Participants: Nineteen female university and graduate students (mean age, 21.6 – 1.5 years; age range, 19.0–26.0 years). Interventions: Fresh rose flowers as an olfactory stimulant, with air as a control. Outcome measures: Heart rate variability and subjective evaluations. The power levels of the high-frequency (HF) (0.15–0.40 Hz) and low-frequency (LF) (0.04–0.15 Hz) components of heart rate variability were calculated by the maximum-entropy method. The HF power was considered to reflect parasympathetic nervous activity. The LF/HF power ratio was determined to reflect the sympathetic nervous activity. A modified semantic differential method was used to perform subjective evaluations. Results: Fresh rose flowers induced (1) a significant increase in parasympathetic nervous activities and (2) an increase in ‘‘comfortable’’ and ‘‘natural’’ feelings. Conclusion: The findings indicated that olfactory stimulation by fresh rose flowers induced physiological and psychological relaxation. Introduction In modern societies, individuals are exposed to many stressors in daily life,1–4 and consequently, many individuals seek contact with nature to relax. One means of achieving contact with nature is viewing fresh flowers, such as roses. Roses are among the most popular flowers, are a common gift for women, and are used to decorate rooms. The authors’ earlier study showed that visual stimulation by fresh rose flowers (Rosa ‘‘Dekora’’) induces physiological relaxation in female medical staff.5 To date, few studies have evaluated the physiological effects of the odor of roses on humans. Inhalation of the odor of rose essential oil (Rosa damascena MILL.) decreases relative sympathetic activity and adrenaline concentration in healthy adults.6 Moreover, Stankewitz et al. explored neuronal processing in response to olfactory stimulation with rose oil in patients with migraine by using event-related functional magnetic resonance imaging and found that the odor of rose oil induces significantly higher blood oxygen level–dependent signal intensities in several brain areas during spontaneous and untreated migraine attacks.7 In addition, Fukui et al. reported that rose odor (essential oil of Rosa alba) inhalation decreases cortisol levels in healthy volunteers.8 Fukada et al. showed that inhaling odor of rose essential oil (R. alba) inhibits increases in salivary cortisol and skin-barrier disruption in humans exposed to stress.9 Regarding subjective evaluations of effects, Ayan et al. used a visual analog scale of pain scores ranging from ‘‘no pain’’ to ‘‘very severe pain’’ to demonstrate that inhalation of odor of rose essential oil (R. damascena) is a useful supplementary and adjunctive therapy for relieving renal colic.10 Thus, the effects of olfactory stimulation by rose extracts, including rose essential oil, have been investigated using both physiological and subjective evaluations. The present study is novel in many respects. First, no previous study has been performed using fresh rose flowers. Second, no other study has evaluated the physiological effects of olfactory stimulation by fresh rose flowers on women from the perspective of autonomic nervous activity, particularly by assessing heart rate variability (HRV), which is a measure of sympathetic and parasympathetic nervous 1 Center for Environment, Health, and Field Sciences, Chiba University, Chiba, Japan. 2 Forestry and Forest Products Research Institute, Ibaraki, Japan. *Co-first authors. THE JOURNAL OF ALTERNATIVE AND COMPLEMENTARY MEDICINE Volume 20, Number 9, 2014, pp. 727–731 ª Mary Ann Liebert, Inc. DOI: 10.1089/acm.2014.0029 727
728 IGARASHI ET AL. activity.Finally,this study included a qualitative analysis Royale,from Enomoto Rose Garden,Japan)were used as of the characteristic odor of R.hybrida "Meikarouz,"also an olfactory stimulant and air was used as a control.Four known as Rouge Royale.11 flowers were put into a 24-L odor bag (polyethylene tere- As mentioned earlier.HRV has been used as a measure of phthalate film heat seal bag;NS-KOKEN Co.,Ltd.Kyoto, autonomic nervous activity.The maximum-entropy method Japan),and the odors were presented to each participant by (MemCalc/Win;GMS,Tokyo,Japan)was used to calculate means of a device fixed on the chest and situated approxi- the power levels of high-frequency (HF,0.15-0.40 Hz)and mately 10cm under the nose (Fig.1).The flow rate of the low-frequency (LF,0.04-0.15Hz)components.The HF odor was set at 3.0 L/min.Preliminary investigations de- power was considered to reflect parasympathetic nervous termined the subjective sensitivity to odor as.for example. activity,and the LF/HF power ratio was considered to reflect weak or easily sensed.The odor was administered for 90 sympathetic nervous activity.Physiological relaxation seconds while the participants sat with their eyes closed. effects were evaluated by using various previously described A within-subject experiment was performed.To eliminate stimuli.14-19 the effect of the order of olfactory stimulation,approxima- The aim of the present study was to clarify the effect of tely half the participants were administrated stimuli in the olfactory stimulation by fresh rose flowers,which exude a following order:control,then rose.The remaining partici- strong fragrance,on HRV. pants were then presented with the rose first,then control. Materials and Methods HRV Participants As a physiological measurement,HRV was analyzed for In this experiment,19 healthy female volunteers were re- the periods between consecutive R waves in the electro- cruited from approximately 500 students at the authors" university and graduate school (mean age+standard devia- o CaNs)vic tion,21.6+1.5 years;age range,19.0-26.0 years).Women performs measurements using a 3-lead electrocardiogram with breathing disorders,such as colds and nasal inflamma- (lead ID).The power levels of the HF (0.15-0.4 Hz)and the tion,were excluded.Participants were requested to get suf- LF (0.04-0.15 Hz)components of HRV were calculated ficient sleep the day before the experiment,to avoid drinking by the maximum-entropy method(MemCalc/Win).The HF alcohol,and to control their conditions.All were informed of power was considered to reflect parasympathetic nervous the aims and procedures involved in the experiment and activity.Furthermore,the LF/HF power ratio was determined provided written informed consent to participate.This study to reflect the sympathetic nervous activity.The means of data was performed in accordance with the regulations of the acquired for 90 seconds were analyzed. Ethics Committee of the Center for Environment.Health,and Field Sciences,Chiba University,Japan. Semantic differential method Study protocol Regarding psychological measurements,to subjectively evaluate the emotional effect of the odors,participants were Physiological measurements were performed in a cham- tested by the modified semantic differential method.23 The ber with an artificial climate maintained at 25C with 50% modified semantic differential method used two pairs of relative humidity and 230 lux illumination.20 Fresh rose adjectives assessed on 13 scales,including "comfortable- flowers (R.hrybrida "Meikarouz,"also known as Rouge uncomfortable,”and“natural--artificial..' FIG.1.The scene during olfactory stimulation and the device used to administer the odors
activity. Finally, this study included a qualitative analysis of the characteristic odor of R. hybrida ‘‘Meikarouz,’’ also known as Rouge Royale.11 As mentioned earlier, HRV has been used as a measure of autonomic nervous activity. The maximum-entropy method (MemCalc/Win; GMS, Tokyo, Japan) was used to calculate the power levels of high-frequency (HF, 0.15–0.40 Hz) and low-frequency (LF, 0.04–0.15 Hz) components. The HF power was considered to reflect parasympathetic nervous activity, and the LF/HF power ratio was considered to reflect sympathetic nervous activity.12,13 Physiological relaxation effects were evaluated by using various previously described stimuli.14–19 The aim of the present study was to clarify the effect of olfactory stimulation by fresh rose flowers, which exude a strong fragrance, on HRV. Materials and Methods Participants In this experiment, 19 healthy female volunteers were recruited from approximately 500 students at the authors’ university and graduate school (mean age – standard deviation, 21.6 – 1.5 years; age range, 19.0–26.0 years). Women with breathing disorders, such as colds and nasal inflammation, were excluded. Participants were requested to get suf- ficient sleep the day before the experiment, to avoid drinking alcohol, and to control their conditions. All were informed of the aims and procedures involved in the experiment and provided written informed consent to participate. This study was performed in accordance with the regulations of the Ethics Committee of the Center for Environment, Health, and Field Sciences, Chiba University, Japan. Study protocol Physiological measurements were performed in a chamber with an artificial climate maintained at 25C with 50% relative humidity and 230 lux illumination.20 Fresh rose flowers (R. hybrida ‘‘Meikarouz,’’ also known as Rouge Royale,11 from Enomoto Rose Garden, Japan) were used as an olfactory stimulant and air was used as a control. Four flowers were put into a 24-L odor bag (polyethylene terephthalate film heat seal bag; NS-KOKEN Co., Ltd. Kyoto, Japan), and the odors were presented to each participant by means of a device fixed on the chest and situated approximately 10 cm under the nose (Fig. 1). The flow rate of the odor was set at 3.0 L/min. Preliminary investigations determined the subjective sensitivity to odor as, for example, weak or easily sensed. The odor was administered for 90 seconds while the participants sat with their eyes closed. A within-subject experiment was performed. To eliminate the effect of the order of olfactory stimulation, approximately half the participants were administrated stimuli in the following order: control, then rose. The remaining participants were then presented with the rose first, then control. HRV As a physiological measurement, HRV was analyzed for the periods between consecutive R waves in the electrocardiogram (RR intervals) as measured by a portable electrocardiograph (Activtracer AC-301; GMS).21,22 This device performs measurements using a 3-lead electrocardiogram (lead II). The power levels of the HF (0.15–0.4 Hz) and the LF (0.04–0.15 Hz) components of HRV were calculated by the maximum-entropy method (MemCalc/Win). The HF power was considered to reflect parasympathetic nervous activity. Furthermore, the LF/HF power ratio was determined to reflect the sympathetic nervous activity. The means of data acquired for 90 seconds were analyzed. Semantic differential method Regarding psychological measurements, to subjectively evaluate the emotional effect of the odors, participants were tested by the modified semantic differential method.23 The modified semantic differential method used two pairs of adjectives assessed on 13 scales, including ‘‘comfortable– uncomfortable,’’ and ‘‘natural–artificial.’’ FIG. 1. The scene during olfactory stimulation and the device used to administer the odors. 728 IGARASHI ET AL.
ROSE ODOR EFFECT ON AUTONOMIC NERVOUS SYSTEM 729 Measurement of volatile organic compounds Very Volatile organic compounds emitted from the flowers were collected in PEJ-02 tubes (Supelco Inc.,Bellefonte, PA)by enclosing one weighed flower inside a 5.0-L Tedlar Moderately bag (GL Science Inc.,Tokyo,Japan).24 The air flow rate through the bag was approximately 80mL/min,and the Slightly temperature of the bag was 25.0+2.0C.The collected volatile compounds were removed from the PEJ-02 tube by heating the trap with an Automatic Thermal Desorption Indifferent System (ATD400,Perkin Elmer)at 280C for 15 minutes. Comfortable Natural The compounds were cryofocused in a cold trap (air mon- feeling feeling itoring trap)at 2C.By heating the cold trap,volatiles were Slightly transferred to a HP-5MS capillary column (30 mx0.25 mm i.d.x0.25-um film thickness,Agilent Technology)and ana- Moderately lyzed using gas chromatography-mass spectrometry(GC-MS ■：Roses ▣：Control Hewlett Packard GC type 6890,MSD 5973).25 The temper- ature program for GC-MS was 40C for 15 minutes,from Very 40℃to180Cat4Cmin,180°Cfor15 minutes,from 180C to 280C at 5C/min,and 280C for 15 minutes.All FIG.3.Subjective feeling measured by the modified se- mantic differential questionnaire after olfactory stimulation mass numbers between 15 and 550m/z were recorded(SCAN by fresh rose flowers or control.Data are expressed as technique).Individual compounds were identified by com- mean+standard deviation;n=19.*p<0.05 by Wilcoxon paring their mass spectra with the data from NIST Library. signed-rank test (one-sided). Literature values and nuclear magnetic resonance spectra were detailed as in a previous report.26 flowers and the control (p=0.0495).The HF power level of Statistical analysis fresh rose flowers(527.36+99.02 msec2)was 19.2%higher SPSS software,version,20.0(IBM Corp.,Armonk,NY, than that of the control (442.54+97.11 msec-).It was clear USA)was used for all statistical analyses.The HRV power that the olfactory stimulation by the fresh rose flowers in- level data were presented as means+SEM.A paired t-test duced a significant increase in parasympathetic nervous was used to compare physiological responses to the fresh rose activities,thereby inducing physiological relaxation.Fur- flowers and controls.Wilcoxon signed-rank test was applied thermore,the LF/HF power ratio of the fresh rose flowers to analyze differences in psychological indices between the (1.00+0.25)was 43.8%lower than that of the control responses to the fresh rose flowers and to the control.In both (1.78+0.59).The difference was not significant,but the re- cases,one-sided tests were used because of the hypothesis sults suggested that fresh rose flowers induced a trend to- that humans would be relaxed by fresh rose flowers. ward decreased sympathetic nervous activities (p=0.0595) (Fig.2B). Results Psychological effects Physiological effects Figure 2A shows the HF value associated with olfactory The modified semantic differential method was used to provide subjective reports of"comfortable"and"natural' stimulation by fresh rose flowers.When the results of the HRV power level data were compared,a significant differ- feelings(Fig.3).The subjective reports of feeling "com- fortable"/"natural"and "very comfortable"/"slightly nat- ence was found in the HF power level between the fresh rose ural"for fresh rose flowers but as"slightly comfortable"/ "indifferent"'for the control.The response to fresh rose 800 B3.0 p=0.0595 Howers was therefore perceived as being significantly more 700 comfortable and natural than to the control (p<0.05). 2.5 600 500 2.0 Volatile compounds 400 1.5 The volatile compounds from the fresh rose flowers are 300 shown in Table 1.The predominant compounds in the fresh 1.0 200 rose flowers were limonene,2-phenethyl acetate,and citral. 0.5 The physiological effects of these compounds remain un- 100 known,and further detailed studies are required. 0 0.0 Roses Control Roses Control Discussion FIG.2. Comparison of high-frequency (HF)power levels and low-frequency (LF)/HF power level ratios of heart rate This study measured the effects of olfactory stimulation by variability during olfactory stimulation by fresh rose flowers fresh rose flowers in humans.These results showed that this or control.Data are expressed as means+SEM;n=16. induced physiological and psychological effects.Some stud- *p<0.05 by paired t-test (one-sided). ies previously assessed the effects of olfactory stimulation by
Measurement of volatile organic compounds Volatile organic compounds emitted from the flowers were collected in PEJ-02 tubes (Supelco Inc., Bellefonte, PA) by enclosing one weighed flower inside a 5.0-L Tedlar bag (GL Science Inc., Tokyo, Japan).24 The air flow rate through the bag was approximately 80 mL/min, and the temperature of the bag was 25.0 – 2.0C. The collected volatile compounds were removed from the PEJ-02 tube by heating the trap with an Automatic Thermal Desorption System (ATD400, Perkin Elmer) at 280C for 15 minutes. The compounds were cryofocused in a cold trap (air monitoring trap) at 2C. By heating the cold trap, volatiles were transferred to a HP-5MS capillary column (30 m · 0.25 mm i.d. · 0.25-lm film thickness, Agilent Technology) and analyzed using gas chromatography-mass spectrometry (GC-MS, Hewlett Packard GC type 6890, MSD 5973).25 The temperature program for GC-MS was 40C for 15 minutes, from 40C to 180C at 4C/min, 180C for 15 minutes, from 180C to 280C at 5C/min, and 280C for 15 minutes. All mass numbers between 15 and 550 m/z were recorded (SCAN technique). Individual compounds were identified by comparing their mass spectra with the data from NIST Library. Literature values and nuclear magnetic resonance spectra were detailed as in a previous report.26 Statistical analysis SPSS software, version, 20.0 (IBM Corp., Armonk, NY, USA) was used for all statistical analyses. The HRV power level data were presented as means – SEM. A paired t-test was used to compare physiological responses to the fresh rose flowers and controls. Wilcoxon signed-rank test was applied to analyze differences in psychological indices between the responses to the fresh rose flowers and to the control. In both cases, one-sided tests were used because of the hypothesis that humans would be relaxed by fresh rose flowers. Results Physiological effects Figure 2A shows the HF value associated with olfactory stimulation by fresh rose flowers. When the results of the HRV power level data were compared, a significant difference was found in the HF power level between the fresh rose flowers and the control ( p = 0.0495). The HF power level of fresh rose flowers (527.36 – 99.02 msec2 ) was 19.2% higher than that of the control (442.54 – 97.11 msec2 ). It was clear that the olfactory stimulation by the fresh rose flowers induced a significant increase in parasympathetic nervous activities, thereby inducing physiological relaxation. Furthermore, the LF/HF power ratio of the fresh rose flowers (1.00 – 0.25) was 43.8% lower than that of the control (1.78 – 0.59). The difference was not significant, but the results suggested that fresh rose flowers induced a trend toward decreased sympathetic nervous activities ( p = 0.0595) (Fig. 2B). Psychological effects The modified semantic differential method was used to provide subjective reports of ‘‘comfortable’’ and ‘‘natural’’ feelings (Fig. 3). The subjective reports of feeling ‘‘comfortable’’/‘‘natural’’ and ‘‘very comfortable’’/‘‘slightly natural’’ for fresh rose flowers but as ‘‘slightly comfortable’’/ ‘‘indifferent’’ for the control. The response to fresh rose flowers was therefore perceived as being significantly more comfortable and natural than to the control ( p < 0.05). Volatile compounds The volatile compounds from the fresh rose flowers are shown in Table 1. The predominant compounds in the fresh rose flowers were limonene, 2-phenethyl acetate, and citral. The physiological effects of these compounds remain unknown, and further detailed studies are required. Discussion This study measured the effects of olfactory stimulation by fresh rose flowers in humans. These results showed that this induced physiological and psychological effects. Some studies previously assessed the effects of olfactory stimulation by FIG. 2. Comparison of high-frequency (HF) power levels and low-frequency (LF)/HF power level ratios of heart rate variability during olfactory stimulation by fresh rose flowers or control. Data are expressed as means – SEM; n = 16. *p < 0.05 by paired t-test (one-sided). FIG. 3. Subjective feeling measured by the modified semantic differential questionnaire after olfactory stimulation by fresh rose flowers or control. Data are expressed as mean – standard deviation; n = 19. *p < 0.05 by Wilcoxon signed-rank test (one-sided). ROSE ODOR EFFECT ON AUTONOMIC NERVOUS SYSTEM 729
730 IGARASHI ET AL. TABLE 1.VOLATILE COMPOUNDS EMITTED Acknowledgments FROM THE FRESH ROSE FLOWER The authors are grateful to Ms.Misako Komatsu and Identified compounds Relative area (% Ms.Mariko Aga for their valuable contributions during the data collection phase of this study.This study was sup- Ethanol 4.0 ported by a grant from the Policy Research Institute, Methoxy-benzene 3.6 Ministry of Agriculture,Forestry and Fisheries,Extramural Acetic acid 2.5 Research Program for Agricultural Forestry and Fishery g-Pinene 1.6 Camphene 1.4 Policy Research. B-Pinene 1.3 Methoxymethyl benzene 3.1 Author Disclosure Statement B-Terpinene 4.8 B-Myrcene 5.8 No competing financial relationships exist. Hexyl acetate 4.6 o-Ocimene 7.0 References Limonene 13.8 B-Ocimene 4.0 1.Krabbendam L,van Os J.Schizophrenia and urbanicity:a g-Ocimene 7.2 major environmental influence-conditional on genetic Terpinolene 1.8 risk.Schizophren Bull 2005;31:795-799. δ-2-Carene 1.8 2.Lederbogen F,Kirsch P,Haddad L,et al.City living and 4-g-Dimethylstyrene 4.5 urban upbringing affect neural social stress processing in Cyclofenchene 1.6 humans.Nature2011:474:498-501. 3,4-Dimethyl-2.4.6-octatriene 1.9 3.Pedersen CB.Mortensen PB.Evidence of a dose-response B-Citronellal 2.7 9.1 relationship between urbanicity during upbringing and 2-Phenethyl acetate Citral 9.0 schizophrenia risk.Arch Gen Psychiatry 2001:58:1039- 1046. δ-Cadinene 1.2 4.van Os J.Kenis G,Rutten BP.The environment and schizophrenia.Nature 2010:468:203-212. 5.Komatsu M.Matsunaga K.Lee J.et al.The physiological rose essential oils In addition,many studies focused on and psychological relaxing effects of viewing rose flowers the rose variety Rosa damascene, but none have evaluated in medical staff.Jpn J Physiol Anthropol 2013:18:1-7. the physiological effect and component analysis of Rouge 6.Haze S.Sakai K.Gozu Y.Effects of fragrance inhalation Royale,a relatively new rose created in the 2000s.11 The on sympathetic activity in normal adults.Jpn J Pharmacol 2002:90:247-253. current study is therefore novel in this regard. 7.Stankewitz A.May A.Increased limbic and brainstem ac- As in the current study,the authors previously studied the effects of nature on human physiology.They tivity during migraine attacks following olfactory stimula- tion.Neurology 2011:77:476-482. have also reported a decrease in sympathetic nervous ac- 8.Fukui H.Komaki R.Okui M.et al.The effects of odor on tivity,13.14.16-18 an increase in parasympathetic nervous cortisol and testosterone in healthy adults.Neuro En- activity,4a decrease in prefrontal cortex activity,s docrinol Lett 2007:28:433-437. and decreased concentrations of stress hormones in forest 9.Fukada M.Kano E.Miyoshi M.et al.Effect of "rose es- therapy studies.14-17.19.27.28 In the future,these indices sential oil"inhalation on stress-induced skin-barrier dis- should be comprehensively assessed to determine the ef- ruption in rats and humans.Chem Sense 2012:37:34-356. fects of olfactory stimulation by fresh rose flowers on 10.Ayan M,Tas U,Sogut E,et al.Investigating the effect of human physiological effects and feelings of relaxation.The aromatherapy in patients with renal colic.J Altern Com- current study used Rouge Royal,which has a strong fra- plement Med2013:19:329-333. grance.In the future,it will be necessary to clarify the 11.Alain A.Inventor.CP (Delaware).Inc.,Wilmington,DE different effects of other rose varieties.A previous report (US),assignee.Hybrid tea rose plant named 'Meikarouz'. showed that the main odor components differ between US patent US PP14,039 P3.Jul.29,2003,2003. varieties.29 Therefore,it is expected that physiological 12.Task Force of the European Society of Cardiology and the effects by every component should be clarified. North American Society of Pacing and Electrophysiology. The main limitation of the study is that it evaluated Heart rate variability standards of measurement,physio- sympathetic and parasympathetic nervous activity by HRV logical interpretation and clinical use.Circulation 1996:93: 1043-1065. only as indices of physiological relaxation.Other experi- 13.Pagani M,Lombardi F,Guzzetti S,et al.Power spectral mental indices,such as prefrontal cortex activity and stress analysis of heart rate and arterial pressure variabilities as a hormone concentrations,should also be assessed for a more marker of sympatho-vagal interaction in man and conscious comprehensive determination of the effect of olfactory dog.Circ Res1986,59:178-193. stimulation by fresh rose flowers on human physiology. 14.Lee J,Li Q,Tyrvainen L,et al.Nature Therapy and Pre- In conclusion,these results showed that olfactory stimu ventive Medicine.Croatia:InTech:2012. lation by fresh rose flowers induced (1)a significant increase 15.Lee J,Park BJ,Tsunetsugu Y,et al.Effect of forest bathing in parasympathetic nervous activities that are enhanced a on physiological and psychological responses in young relaxed state,(2)a trend toward decreased sympathetic Japanese male subjects.Public Health 2011;125:93-100. nervous activities,and (3)an increase in"comfortable'and 16.Park BJ,Tsunetsugu Y,Ishii H,et al.Physiological effects “natural'feelings. of Shinrin-yoku(taking in the atmosphere of the forest)in a
rose essential oils.6–10 In addition, many studies focused on the rose variety Rosa damascene, 6,10 but none have evaluated the physiological effect and component analysis of Rouge Royale, a relatively new rose created in the 2000s.11 The current study is therefore novel in this regard. As in the current study, the authors previously studied the effects of nature on human physiology.5,14–18,27,28 They have also reported a decrease in sympathetic nervous activity,13,14,16–18 an increase in parasympathetic nervous activity,5,14–19 a decrease in prefrontal cortex activity,28 and decreased concentrations of stress hormones in forest therapy studies.14–17,19,27,28 In the future, these indices should be comprehensively assessed to determine the effects of olfactory stimulation by fresh rose flowers on human physiological effects and feelings of relaxation. The current study used Rouge Royal, which has a strong fragrance. In the future, it will be necessary to clarify the different effects of other rose varieties. A previous report showed that the main odor components differ between varieties.29 Therefore, it is expected that physiological effects by every component should be clarified. The main limitation of the study is that it evaluated sympathetic and parasympathetic nervous activity by HRV only as indices of physiological relaxation. Other experimental indices, such as prefrontal cortex activity and stress hormone concentrations, should also be assessed for a more comprehensive determination of the effect of olfactory stimulation by fresh rose flowers on human physiology. In conclusion, these results showed that olfactory stimulation by fresh rose flowers induced (1) a significant increase in parasympathetic nervous activities that are enhanced a relaxed state, (2) a trend toward decreased sympathetic nervous activities, and (3) an increase in ‘‘comfortable’’ and ‘‘natural’’ feelings. Acknowledgments The authors are grateful to Ms. Misako Komatsu and Ms. Mariko Aga for their valuable contributions during the data collection phase of this study. This study was supported by a grant from the Policy Research Institute, Ministry of Agriculture, Forestry and Fisheries, Extramural Research Program for Agricultural Forestry and Fishery Policy Research. Author Disclosure Statement No competing financial relationships exist. References 1. Krabbendam L, van Os J. Schizophrenia and urbanicity: a major environmental influence—conditional on genetic risk. Schizophren Bull 2005;31:795–799. 2. Lederbogen F, Kirsch P, Haddad L, et al. City living and urban upbringing affect neural social stress processing in humans. Nature 2011;474:498–501. 3. Pedersen CB, Mortensen PB. Evidence of a dose-response relationship between urbanicity during upbringing and schizophrenia risk. Arch Gen Psychiatry 2001;58:1039– 1046. 4. van Os J, Kenis G, Rutten BP. The environment and schizophrenia. Nature 2010;468:203–212. 5. Komatsu M, Matsunaga K, Lee J, et al. The physiological and psychological relaxing effects of viewing rose flowers in medical staff. Jpn J Physiol Anthropol 2013;18:1–7. 6. Haze S, Sakai K, Gozu Y. Effects of fragrance inhalation on sympathetic activity in normal adults. Jpn J Pharmacol 2002;90:247–253. 7. Stankewitz A, May A. Increased limbic and brainstem activity during migraine attacks following olfactory stimulation. Neurology 2011;77:476–482. 8. Fukui H, Komaki R, Okui M, et al. The effects of odor on cortisol and testosterone in healthy adults. Neuro Endocrinol Lett 2007;28:433–437. 9. Fukada M, Kano E, Miyoshi M, et al. Effect of ‘‘rose essential oil’’ inhalation on stress-induced skin-barrier disruption in rats and humans. Chem Sense 2012;37:34–356. 10. Ayan M, Tas U, Sogut E, et al. Investigating the effect of aromatherapy in patients with renal colic. J Altern Complement Med 2013;19:329–333. 11. Alain A, Inventor. CP (Delaware), Inc., Wilmington, DE (US), assignee. Hybrid tea rose plant named ‘Meikarouz’. US patent US PP14,039 P3. Jul. 29, 2003, 2003. 12. Task Force of the European Society of Cardiology and the North American Society of Pacing and Electrophysiology. Heart rate variability standards of measurement, physiological interpretation and clinical use. Circulation 1996;93: 1043–1065. 13. Pagani M, Lombardi F, Guzzetti S, et al. Power spectral analysis of heart rate and arterial pressure variabilities as a marker of sympatho-vagal interaction in man and conscious dog. Circ Res 1986;59:178–193. 14. Lee J, Li Q, Tyrva¨inen L, et al. Nature Therapy and Preventive Medicine. Croatia: InTech; 2012. 15. Lee J, Park BJ, Tsunetsugu Y, et al. Effect of forest bathing on physiological and psychological responses in young Japanese male subjects. Public Health 2011;125:93–100. 16. Park BJ, Tsunetsugu Y, Ishii H, et al. Physiological effects of Shinrin-yoku (taking in the atmosphere of the forest) in a Table 1. Volatile Compounds Emitted from the Fresh Rose Flower Identified compounds Relative area (%) Ethanol 4.0 Methoxy-benzene 3.6 Acetic acid 2.5 a-Pinene 1.6 Camphene 1.4 b-Pinene 1.3 Methoxymethyl benzene 3.1 b-Terpinene 4.8 b-Myrcene 5.8 Hexyl acetate 4.6 o-Ocimene 7.0 Limonene 13.8 b-Ocimene 4.0 a-Ocimene 7.2 Terpinolene 1.8 d-2-Carene 1.8 4-a-Dimethylstyrene 4.5 Cyclofenchene 1.6 3,4-Dimethyl-2,4,6-octatriene 1.9 b-Citronellal 2.7 2-Phenethyl acetate 9.1 Citral 9.0 d-Cadinene 1.2 730 IGARASHI ET AL
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