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ORIGINAL ARTICLES |
From the Division of Public Health Services and Research, University of Florida College of Dentistry, Gainesville, FL.
Address correspondence and reprint requests to Dr. Roger Fillingim, 1600 SW Archer Road, Box 100404, Gainesville, FL 32610. E-mail: rfillingim{at}dental.ufl.edu
| ABSTRACT |
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METHODS: A sex-balanced (13 men and 13 women) randomized crossover design was used to obtain pre- and posttreatment change scores for quantitative sensory ratings of contact heat, pressure, and ischemic pain across separate inhalation treatment conditions using essential oil of lavender, essential oil of rosemary, and distilled water (control). Subjective reports of treatment-related changes in pain intensity and pain unpleasantness were obtained for each condition using a visual analog scale. We interpret our findings with respect to the separate dimensions of sensory and affective processing of pain.
RESULTS: Analyses revealed the absence of changes in quantitative pain sensitivity ratings between conditions. However, retrospectively, subjects global impression of treatment outcome indicated that both pain intensity and pain unpleasantness were reduced after treatment with lavender and marginally reduced after treatment with rosemary, compared with the control condition.
CONCLUSION: These findings suggest that aromatherapy may not elicit a direct analgesic effect but instead may alter affective appraisal of the experience and consequent retrospective evaluation of treatment-related pain.
Key Words: aromatherapy, sensory testing, pain intensity, pain unpleasantness.
Abbreviations: PANAS = Positive Affect and Negative Affect Scale;; RIA = radioimmunoassay;; STAI = State Trait Anxiety Index;; VAS = visual analog scales.
| INTRODUCTION |
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Three well-designed clinical studies have been published supporting the benefits of aromatherapy for general medical management. Sparks and colleagues demonstrated that peppermint oil significantly reduced colon spasm when added to barium enema suspension, compared with an equal number of patients (n = 70) receiving barium suspension without peppermint oil (10). Woolfson and Hewitt randomized 36 intensive care unit patients to one of three groups: massage with lavender, massage without lavender, or rest only (21). Treatment consisted of 20 minutes of foot massage twice a week for 5 weeks. A significantly greater number of patients in the lavender massage group demonstrated decreased heart rate, compared with the other two groups. These results suggest that oil of lavender reduces physiological arousal above that provided by massage alone or rest only. Similar conclusions were obtained by Buckle, who recorded emotional and behavioral stress levels during a randomized double-blind trial using two different species of lavender massaged for 20 minutes on 2 consecutive days into the extremities and forehead of two groups of postcardiac bypass patients (N = 28) (22). A significant difference in self-reported stress between the two groups was attributed to the differential therapeutic effect between the two species of lavender oil, and not to the effect of massage because this was common to all treatment conditions.
The relaxant effect of oil of lavender has also been demonstrated in experimental studies with humans. Diego and colleagues used standardized measures of electroencephalogram (EEG) activity, alertness, and mood for 40 adults after inhalation of either oil of lavender or oil of rosemary (considered a stimulating odor) (9). Subjects were given simple math computations before and after the therapy. Subjects who received the lavender aroma reported a significantly improved mood, displayed a significant improvement on math computation accuracy, and exhibited a significant increase in EEG frontal alpha power, suggesting increased drowsiness. In contrast, the rosemary aroma group showed a decrease in EEG frontal alpha power and beta power, suggesting increased alertness. Moss and colleagues also used essential oils of lavender and rosemary in a study of cognitive performance and mood in which 144 volunteers were randomly assigned to one of three groups: lavender, rosemary, or control (23). Subjects were deceived as to the genuine aim of the study and were asked to complete a computerized cognitive assessment battery. Visual analog mood questionnaires were completed before exposure to each condition and after completion of the cognitive assessment battery. They found that lavender produced a decrease in performance of attention and working memory capacity and reaction times compared with controls. Rosemary enhanced memory performance but reduced memory reaction times compared with controls. In terms of posttest mood ratings, the control group was significantly less content than both the rosemary and lavender groups. Other studies have similarly reported improved memory performance (2,3) and alertness (7) after olfactory exposure to different odors.
Very few studies have investigated the effects of aromatherapy in the treatment and management of pain (5,6,8,24). Gobel and colleagues used a crossover design to compare treatment effect between inhaled peppermint, acetaminophen, peppermint plus acetaminophen, and placebo for headache pain in 41 adult males (11). Peppermint and acetaminophen were equally effective in reducing headache pain and both were significantly better than placebo. Gobel et al. topically administered preparations of peppermint oil, eucalyptus, and ethanol to the forehead and temples of 32 healthy males, using a double-blind, randomized, crossover design (12). Pre- and postmanipulation measures included temporal electromyogram (EMG) activity, mood state, and sensitivity to experimental pain. Significant results included decreased emotional irritation, decreased resting EMG, and diminished ischemic pain only for those preparations containing peppermint oil. Marchand and Arsenault investigated the effects of pleasant, unpleasant, and neutral odors on mood and pain ratings (6). Twenty men and 20 women individually rank ordered a series of common odors (eg, orange water, vinegar, baby oil) as pleasant, unpleasant, or neutral. They then completed a series of 3-minute hand immersions in a hot circulating bath (4648°C) while continually smelling one of the three previously selected odors (most pleasant, most unpleasant, and closest to neutral). Pain intensity and pain unpleasantness ratings were reported every 15 seconds during each trial. Women perceived significantly less pain intensity and pain unpleasantness during inhalation of the pleasant odor relative to the unpleasant or neutral odors. Pain intensity and unpleasantness did not differ across odor conditions for men. These findings suggest a sex-dependent effect of pleasant odor on perceived pain intensity and unpleasantness. It remains to be seen whether therapeutic essential oils produce similar effects.
The purpose of this investigation was to examine the effects of olfactory absorption of two commonly used therapeutic essential oils on sensory and affective responses to experimentally induced pain. We hypothesized that inhalation of essential oil of lavender and rosemary, both essential oils with purported analgesic properties (1,8) but opposite effects on affective arousal, would decrease pain in response to noxious heat, pressure, and ischemic stimuli. Second, we hypothesized subjective reports of pain intensity and pain unpleasantness to be less after separate inhalation treatment sessions with both essential oil of lavender and rosemary.
| METHODS |
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A male and female experimenter were present during each session (6,2629). To control for hormonal fluctuation believed to influence pain sensitivity (30), all sessions were conducted during the follicular phase (between days 4 and 10 after menses) (31). To minimize measurement error, the same experimenter obtained measures during each of the three sessions, with male and female experimenters randomized between subjects.
Subjects
Twenty-six healthy, nonsmoking and unmedicated adult subjects (13 men and 13 premenopausal women) were recruited from a pool of subjects who completed a similar experimental pain protocol within the past 18 months. These subjects were thus familiar with the quantitative sensory testing apparatus and methodology, which reduced novelty effects. Subjects were blinded to the studys hypotheses and treatment conditions. The study protocol conformed to the Institutional Review Board of the University of Florida. Subjects were paid $75 for completion of the study. All subjects completed the study.
Session Baseline
On arrival, subjects provided informed consent and were comfortably seated in a reclining chair in a sound-attenuated room. Subjects then completed psychological measures assessing affectivity (Positive Affect and Negative Affect Scale; PANAS (32), measures of trait and situational anxiety (State Trait Anxiety Index; STAI) (33), and present mood, using the Profile of Mood States (34). Demographics and health history information and a questionnaire assessing the subjects familiarity with and attitudes about complementary and alternative therapy modalities were completed during the first session.
Experimental Pain Tasks
Thermal Pain Threshold, Tolerance, and Temporal Summation Procedures
Thermal pain stimuli were delivered using a computer-controlled Medoc Thermal Sensory Analyzer (TSA-2001, Ramat Yishai, Israel), which is a peltier-element-based stimulator using a 3 x 3-cm thermode. The thermode was placed on the right dorsal forearm. Its position was altered slightly between trials in order to avoid either sensitization or habituation of cutaneous receptors. The maximum permitted temperature was 52°C. Subjects could terminate the heat stimulus at any point by pressing a control device button or by verbal command.
Heat pain threshold and tolerance were obtained three times each. On initiation of each trial, the thermal contact increased in temperature at a rate of 0.5°C/second from a baseline temperature of 32°C. For pain threshold, subjects were instructed to press a control button "when the heat first becomes painful, when you first feel pain." For pain tolerance, subjects were instructed to press the button "when you no longer feel able to tolerate the pain."
Temporal summation of thermal pain was assessed using a series of 10 consecutive 0.5-second-long heat pulses, with an interpulse interval of 2.5 seconds. Separate series of 10 trials with target temperatures of 49°C and 52°C were delivered to the right ventral forearm. At each pulse peak, subjects rated the intensity of the stimulus using a verbal rating scale, with anchors of 0 (no pain) and 100 (most intense pain imaginable). A rating of 20 was defined as "barely painful."
Pressure Pain Procedure
Pressure pain threshold was measured using a digital, handheld, clinical grade pressure algometer (Jtech, Heber City, UT). Pressure was applied at the rate of 0.5 kg/second to the right upper trapezius and the right masseter, using a 0.5-cm2 probe. Subjects were instructed to respond verbally when "the pressure first becomes painful, when you first feel pain." Three trials were completed for each site.
Ischemic Pain Procedure
Ischemic pain was assessed using the submaximal effort tourniquet procedure (35). The ischemic pain task consisted of elevating the right arm above heart level for 30 seconds. Circulation was then occluded using a standard blood pressure cuff inflated to 240 mm Hg. The arm was then lowered and the subject completed 20 hand-grip exercises of 2-second duration at 4-second intervals at 50% of their maximum grip strength. Subjects were instructed to report when they first felt pain (pain threshold) and when the pain became intolerable (pain tolerance), and the time required to reach these two endpoints was recorded. Every 30 seconds after the first report of ischemic pain, subjects rated in alternate order their ischemic pain intensity and unpleasantness using a 0 to 20 combined verbalnumerical box scales (36). The procedure was terminated when one of the following occurred: a rating of 20 was obtained, on request by the subject, or after 15 minutes.
Treatment Condition
Treatment consisted of the randomized application of 5 drops of essential oil of lavender, rosemary, or distilled water to a 2 x 2-inch cotton gauze. The gauze was attached to the front of the subjects garment, approximately 12 inches below their nose. Subjects were directed to breathe normally while they sat quietly in a recliner for 10 minutes. The gauze remained in place while subjects then began the posttreatment experimental pain procedures. This procedure reflects a modification of that used by others (8) by increasing the application dose and duration of exposure (24).
Salivary Cortisol
Saliva samples for determination of cortisol were obtained to coincide with the end of the resting period, the end of treatment, and the midpoints of the pre- and posttreatment pain tasks. Samples were collected 25 minutes after each of these time points, thus coinciding with the peak cortisol concentration present in the saliva (37). Samples were collected using an absorbent cotton pellet (Salivette, Sarstedt Inc., Newton, NC) and frozen at 20°C. Before assay, saliva was extracted from the Salivettes by thawing and then centrifugation (Beckman refrigerated centrifuge, Model J-6B) at 3000 RPM at 4°C for 20 minutes. Salivary cortisol levels were determined using the DSL-2000 cortisol radioimmunoassay (RIA) kit (Diagnostic Systems Laboratories, Inc., Webster, TX) with modifications. The modifications increased the sensitivity of the cortisol assay and provided a reliable assay system to detect salivary cortisol in all samples provided. Modifications of the standard cortisol RIA procedures were as follows: a) All standards and controls provided were diluted 1:10 with the cortisol assay dilution buffer. This provided a working standard curve range of (0.056.00 µg/dl); b) All standards, controls and unknowns were assayed in duplicate at 100 µl; c) Cortisol (I125) reagent and cortisol antiserum complex were added in 100-µl volumes to all appropriate tubes; and d) All samples were incubated overnight at room temperature. All other RIA procedures followed the protocol provided in the DSL-2000 cortisol RIA kit. With the above modifications, this provided an assay system that had a sensitivity of 0.05 µg/dl (at 90% binding) and an intra-assay CV and interassay CV of 3.95% and 4.94%, respectively.
Postsession Questionnaire
After completing each sessions posttreatment experimental pain procedures, subjects completed a postsession evaluation questionnaire. Using 100-mm visual analog scales (VAS), subjects were asked to rate whether the sessions odor was relaxing (0-mm anchor) or stimulating (100-mm anchor). Ratings of 50 mm indicated a neutral rating for each VAS. Also, subjects rated whether the sessions aroma increased pain intensity and pain unpleasantness (0-mm anchor) or decreased pain intensity and pain unpleasantness (100-mm anchor). Finally, subjects rated the intensity of the odor using a 100-mm VAS with anchors of "not noticeable" (0 mm) and "intense" (100 mm).
Analysis
Between-session differences for baseline anxiety, affectivity, and posttreatment evaluation questionnaire data were tested using a series of one-way analysis of variance (ANOVA) and Wilcoxon Z for related, nonparametric samples. A series of 2 Time (pretreatment, posttreatment) x 3 Condition (control, lavender, rosemary) repeated-measures ANOVA were used to test for time-by-condition interaction effects on sensory test scores, cardiovascular measures (systolic blood pressure, diastolic blood pressure, heart rate) and salivary cortisol. Main effects for sex were tested by entering sex as a between-subjects factor for each ANOVA. Bonferroni adjustments were used to correct for post hoc pairwise comparisons. Two measures were derived from the temporal summation procedure. First, the average of all 10 pain ratings were computed. Then, the maximum increase was calculated as the difference between the ratings of first heat pulse and the maximum rating from the remaining pulses. Average ratings of ischemic pain intensity and unpleasantness were computed by calculating the mean of all ratings for each subject. For subjects who terminated the task before the time limit, their last rating was carried forward for all future time points.
| RESULTS |
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Physiological Responses
Tables 1 and 2
show that the Time x Condition interaction was not significant for cortisol or for any of the cardiovascular measures (p values
.32), suggesting the absence of neuroendocrine or autonomic responses to treatment. With the exception of systolic blood pressure, the main effect for sex was likewise not significant, demonstrating that men and women responded similarly and consistently within and between sessions (systolic blood pressure: p = .02, all others: p > .31).
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.02). Consistently, women reported lower heat and pressure tolerance and greater windup (heat pulse) pain relative to men. Main effects of time emerged for several pain measures (Heat Tolerance, Trapezius Pressure, Ischemic Threshold and 49°C and 52°C Maximum Heat Ratings), with all effects except Ischemic Threshold in the direction of greater pain sensitivity during the postassessment.
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| DISCUSSION |
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Effect of Aromatherapy on Physiological Response
The absence of pre- posttreatment differences indicates that our treatment conditions did not elicit a detectable neuroendocrine or autonomic response. The absence of a cortisol sex main effect indicates that both mens and womens neuroendocrine responses were equal at the end of the 10-minute quiet resting baseline and treatment periods. Though not significantly different (with the exception of systolic blood pressure), cardiovascular sex effects were in the expected direction.
Effect of Aromatherapy on Quantitative Sensory Testing
The results of quantitative sensory testing revealed a significant prepost treatment difference across experimental conditions only for the 49°C Heat Pulse task, when ratings were calculated as the difference between the first and last of the 10 pulses. It is noteworthy that this apparent treatment effect was obtained between the Lavender and Rosemary treatment conditions, and not between the Control and either essential oil treatment condition. Thus, the absence of control matched changes in pain response after inhalation of essential oils indicates that the treatment condition we employed produced no analgesic effects. As reported by others (6), main sex effects were observed for several of the pain measures (Heat Tolerance, 49°C and 52°C Heat Pulse and Masseter and Trapezius Pressure). All women in this study were scheduled during the follicular phase of their menstrual cycle (49 days after the onset of menses). It is possible that controlling for cycle phase eliminated potential sex differences for the other pain measures (4). Also, all subjects in this study had participated in a previous experimental pain investigation; therefore, reduced novelty effects may have diminished any sex differences. Moreover, a selection bias may have attenuated sex differences, because those subjects who found the pain stimuli most distressing would have been less likely to volunteer for another laboratory pain experiment.
To our knowledge, this is the first time that quantitative sensory testing with healthy subjects has been used to test for possible analgesic effects of inhaled essential oils. In the only other published experimental pain report, Gobel et al. topically administered four different test preparations to the forehead and temples of 32 healthy males, using a double-blind, randomized, crossover design (12). Test preparations included combinations of peppermint oil, eucalyptus, and ethanol. Pre- and postmanipulation measures included temporal EMG activity, mood state, and sensitivity to experimental pain. Pain stimuli were selected to simulate tension-type headache symptoms. Stimuli included ischemic pain (pressure cuff placed around the cranium), mechanical pressure pain (pressure algometer applied to the scalp and middle phalanx of the middle finger), and thermal pain (contact thermistor applied to the forehead). After treatment with peppermint oil, subjects reported decreased emotional irritation and demonstrated decreased resting EMG. Ischemic pain, but not thermal or mechanical pain ratings were significantly reduced. It is possible that the topical application, versus the inhalation used in our study, was responsible for the pain-reducing effects of their intervention. It remains to be seen how the topical application of essential oils may affect quantitative sensory testing.
Retrospective Reports of Treatment Effects
Retrospective evaluation of the effects of aromatherapy suggest that when asked to self-report any perceived change in pain sensitivity after treatment, subjects reported that they experienced less pain intensity and pain unpleasantness after the Lavender treatment and a trend toward less pain intensity after the Rosemary treatment, relative to the Control condition. There was no clear sex-related trend in this self-report, although men reported diminished pain intensity and women reported diminished pain unpleasantness in the Lavender condition. Although the inhalation of the essential oils did not elicit a detectable analgesic response, the use of these oils may have provided an additional pleasant sensory and affective stimulus, which could alter overall evaluation of the pain experience, thus influencing retrospective evaluation of the treatment effects. This interpretation is consistent with those of others who have demonstrated aroma-mediated changes in affect in both the clinical and laboratory setting (46,9,18,22,24,3840). The role of affectivity as an integral component of the pain experience has been well documented (4147). From the results of the present study, it appears that the use of aromatherapy for the management of acute pain may produce beneficial effects not through direct physiological mechanisms, but by providing a competing pleasant sensory and affective experience that can alter retrospective pain evaluation.
Limitations
Several limitations of this study deserve mention. First, subjects in this study were familiar with sensory testing methods through previous participation in another sensory study, which is both a strength and a limitation. The benefit is that the variability associated with novelty effects was reduced; however, recruiting experienced subjects may have introduced a selection bias, and a different pattern of results may have emerged with naïve participants. Another limitation is the relatively small sample size; however, given the minimal effect sizes, the sample size required to detect significant aromatherapy effects on psychophysical responses would be prohibitive. In addition, the aromatherapy intervention may not have been potent enough to alter pain responses, and a more intense and/or more prolonged aromatherapy treatment may have been more effective. Lastly, it is possible that providing odor property ratings (ie, analog rating from stimulating to relaxing) immediately before the posttreatment pain ratings may have biased a response toward diminished pain ratings. However, this seems unlikely as the subjects affective response to the odor was established before the posttreatment pain stimuli and postsession questionnaire.
| CONCLUSION |
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Received for publication October 23, 2003.
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