Olfactory influences on mood and autonomic, endocrine, and immune function

Summary

Despite aromatherapy's popularity, efficacy data are scant, and potential mechanisms are controversial. This randomized controlled trial examined the psychological, autonomic, endocrine, and immune consequences of one purported relaxant odor (lavender), one stimulant odor (lemon), and a no-odor control (water), before and after a stressor (cold pressor); 56 healthy men and women were exposed to each of the odors during three separate visits. To assess the effects of expectancies, participants randomized to the “blind” condition were given no information about the odors they would smell; “primed” individuals were told what odors they would smell during the session, and what changes to expect. Experimenters were blind.

Self-report and unobtrusive mood measures provided robust evidence that lemon oil reliably enhances positive mood compared to water and lavender regardless of expectancies or previous use of aromatherapy. Moreover, norepinephrine levels following the cold pressor remained elevated when subjects smelled lemon, compared to water or lavender. DTH responses to Candida were larger following inhalation of water than lemon or lavender. Odors did not reliably alter IL-6 and IL-10 production, salivary cortisol, heart rate or blood pressure, skin barrier repair following tape stripping, or pain ratings following the cold pressor.

Introduction

Widely utilized, aromatherapy is employed for relief of pain, relaxation and anxiety reduction, and enhanced energy; essential oils have been used to help women cope with labor pain, to relieve chemotherapy side effects, to enhance the rehabilitation of cardiac patients, to promote restful sleep, and to reduce post-surgical discomfort (Price and Price, 1999). However, efficacy data are scant, and potential mechanisms of action are controversial.

The “lock and key” or systemic effect theory posits that essential oils act like a drug or enzyme, such that particular odors should have very specific effects (Hirsch, 2001), a popular view among aromatherapy practitioners who prescribe certain odors for distinct health problems (Hirsch, 2001). For example, short-term inhalation of lavender oil (typically over the space of a few hours) is described as therapeutic for insomnia, influenza, headaches, migraines, anxiety, nervousness, and melancholy (Price and Price, 1999). Others have argued that lavender enhances immune function, as well as treating lung and sinus infections, laryngitis, and asthma (Keville and Green, 1995). These and other authors have emphasized lavender's relaxant properties (Grace, 1999; Tisserand and Balacs, 1995).

Following a long history in folklore, lavender has been used as a sleep aid, and one small study suggested that the ambient odor of lavender can significantly enhance the amount of time asleep after withdrawal of medication for insomnia (Hardy et al., 1995). In another sleep study, lavender oil presented the first 2 min of every 10 min period for 40 min increased deep or slow-wave sleep compared to a control (distilled water) stimulus (Goel et al., 2005). Contingent negative variation (CNV), an EEG shift that occurs when individuals are expecting an event (e.g., a light that will signal a tone), is diminished by sedatives and enhanced by stimulants; lavender decreased CNV, but it did not affect reaction time or heart rate as sedatives do (Torii et al., 1988). Further, a comparison of rosemary and lavender oils using EEG and math computations showed that lavender increased patterns consistent with drowsiness, and subjects reported greater relaxation, while rosemary produced EEG patterns interpreted as increased alertness, consistent with faster and more accurate math test results (Diego et al., 1998).

In contrast to lavender's sedative characterization, lemon oil is described as activating, immunomodulatory, and mood enhancing (Buchbauer et al., 1993; Keville and Green, 1995; Lis-Balchin and Hart, 2002; Price and Price, 1999); it has also been touted as an inhalation remedy for respiratory tract infections (Grace, 1999). Lemon oil has been associated with increased heart rate and enhanced mental and physical task performance in human studies (Jellinek, 1997). In addition, in one study participants exposed to lemon oil reported fewer physical symptoms than individuals exposed to the unpleasant smell of dimethyl sulfide (Knasko, 1992).

Although some essential oils like lavender and lemon have been classified as either sedative or stimulating and these categories are broadly related to their putative CNS actions, there does not seem to be general agreement on mechanisms of action, and the health benefits are unclear; autonomic and self-report data have typically been used as a surrogate for health outcomes. In fact, despite the clear presumption that aromatherapy has immune consequences, we found only one human study that included immunological measures (Komori et al., 1995). Indeed, more broadly, most studies lack physiological or objectively assessed health endpoints.

Placebo and expectancy effects are central problems in human olfactory research, and interpretation of a number of studies is difficult for this reason; few studies are double or even single blind, and many assessed only a single odor without any control conditions (Martin, 2006). The paucity of these key controls is important because of what Jellinek terms the “placebo mechanism” (Jellinek, 1997); unlike the systemic effects theory described above, this theory holds that the characteristics of the odorant are irrelevant, and individuals’ expectancies determine the pattern of responses. In support of this perspective, participants to whom it was suggested that an odor would affect performance showed an improvement in math calculations, even when they were in fact exposed to no odor (Knasko et al., 1990). The general affective theory or reflectorial effect theory (Hirsch, 2001) provides yet another conceptual framework; it suggests that odors perceived as positive may induce positive moods, and these mood changes may enhance both physical and psychological well being.

To compare and contrast the diverse perspectives about whether and how odors affect health, we examined the autonomic, endocrine, and immune consequences of one purported sedating or relaxant odor, lavender, one activating or stimulant odor, lemon, and distilled water as a no-odor control during both resting and “challenge” or stress conditions in a mixed or between-within repeated measures design; each subject served as his or her own control during three separate 6 h visits. Depending on their random assignment, participants were either given no information about what odors they would be smelling or what to expect (the “blind” group), or they were told what odors they would smell and what changes to expect from the relaxant, stimulant, or no odor exposures (the “primed” group).

Our protocol for each session included a cold pressor, a laboratory stressor that elevates stress-related hormones, heart rate, and blood pressure (Blandini et al., 1995; Hirsch and Liebert, 1998). Both before and after the cold pressor we performed tape stripping, a common dermatological paradigm for studying restoration of the skin barrier, a process mediated by both endocrine and immune systems (Choi et al., 2005). Our design thus provided a way to examine the ability of lemon and lavender odors to modulate stress and pain responses to the cold pressor, as well as wound healing via the speed of skin barrier repair.

Specific predictions can be derived from the various theories posited to explain the effects of essential oils. For example, if the systemic effect theory is correct, even relatively short-term exposure to lavender would be expected to produce larger declines in the production of cortisol and catecholamines, faster skin barrier repair, lower pain ratings in response to the cold pressor, and smaller stress-related immunological changes compared to lemon and the no-odor control; short-term exposure to lemon oil should produce greater transient increases in positive affect, heart rate, blood pressure, and catecholamines than either lavender oil or the no-odor control. If expectancies determine the pattern of responses (Jellinek, 1997), then the primed group's mood and physiological responses to lemon and lavender odors would be greater than the blind group; similarly, those with positive expectancies about aromatherapy in advance of participation would be expected to show greater changes. By assessing olfactory influences on mood and autonomic, endocrine, and immune function, our design allowed us to contrast these diverse conceptual perspectives, clarify mechanisms, and assess possible clinical efficacy.