Rollercoaster asthma: When positive emotional stress interferes with dyspnea perception☆
Introduction
Asthma is the most common of chronic diseases and is characterized by recurrent attacks of airway obstruction, which can be measured via lung-function testing. A reduction in lung function is associated with dyspnea (the generic term for breathlessness, shortness of breath, tightness of the chest, difficult breathing), concern, worry, and negative emotional stress (Lehrer, Feldman, Giardino, Song, & Schmaling, 2002). Although reduction in lung function and dyspnea are generally coinciding, physicians and researchers are now familiar with a phenomenon that caused lots of surprise in the 70s of the last century, when it was found that lung function and dyspnea often poorly relate. That is, individuals with asthma may complain of dyspnea when testing does not reveal any deviation in lung function, or, contrarily, individuals with asthma do not report dyspnea in the midst of an asthma attack (Lehrer et al., 2002).
Many studies have shown that this relationship between lung function and dyspnea is influenced by emotional situations, particularly because anxious patients tend to overperceive dyspnea (Boulet, Cournoyer, Deschesnes, Leblanc, & Nouwen, 1994; Janson, Bjornsson, Hetta, & Boman, 1994; Rietveld, Everaerd, & Van Beest, 1999; Rietveld, Van Beest, & Everaerd, 1999; Spinhoven, Van Peski-Oosterbaan, Van der Does, Willems, & Sterk, 1997; Tiller, Pain, & Biddle, 1987). Likewise, the counter-intuitive observation that individuals with asthma were less accurate than controls in the perception of externally applied interruptions in airflow while breathing through a tube-like apparatus has also been attributed to emotional influences (Rietveld, Kolk, Prins, & Van Beest, 1997). Furthermore, recent research has shown that long-term negative emotional stress in individuals with asthma is associated with a shift in immune response, favoring airway sensitivity. For example, one study showed that a reduction in lung function in students with asthma was more likely during a high-stress examination period, as compared to a low-stress post-examination period (Liu et al., 2002).
However, the effects of acute positive emotional stress on parameters of asthma seem to have been neglected. Positive stress would be defined as a state of heightened physiological arousal in conjunction with subjective reports of positive mood or emotion, e.g. joy or happiness. From a psycho-physiological perspective, there seems to be little difference in the physiological response during emotional stress that subjects perceive negatively versus positively (Anderson, 1990; Blascovich, 1990). For example, in vivo assessment with ambulatory equipment revealed similar effects of positive and negative emotions on heart rate and blood pressure (Jacob et al., 1999). A difference would be that negative emotions may have longer lasting effects on heart beat than positive emotions, e.g. until 5 min after the emotional event (Brosschot & Thayer, 2003). Physiological differences within minutes following a negative or positive stressor would probably be negligible.
On the subjective level, the difference between positive and negative emotional stress could be crucial for dyspnea perception. Literature has suggested that individuals with asthma have learned to associate negative situations, emotional stress, being upset or distressed, with difficult breathing, and are thus likely to overperceive dyspnea in such situations (Bass & Gardner, 1995; Boulet et al., 1994; Houtveen, Rietveld, & De Geus, 2003; Meyer, Kroner-Herwig, & Sporkel, 1990; Rietveld, Everaerd, & Creer, 2001; Ritz, Steptoe, DeWilde, & Costa, 2002; Schmaling, McKnight, & Afari, 2002). The possibility of an opposite effect, a learned association between happy, joyful situations, and breathing without dyspnea, resulting in underperception of airways obstruction, has been suggested in literature, but not experimentally tested (Kang & Fox, 2000; Miller & Wood, 1997; Rietveld & Everaerd, 2000). The few studies to the positive emotion–asthma relationship (e.g. Miller & Wood, 1997) focused on diary self-reports of individuals with asthma, or while they were watching emotional films, whereas severe dyspnea may generally relate to acute high-arousal situations (Janson et al., 1994). Indeed, substantial errors in dyspnea perception are to be expected when individuals are emotionally stressed and highly aroused (Rietveld & Houtveen, 2004). Hence, when studying the influence of positive emotions on dyspnea perception, high levels of subjective stress in conjunction with physiological arousal, e.g. enhanced heart rate and blood pressure seems warranted.
The current study tested the effect of acute positive emotional stress on dyspnea perception. Volunteer women with asthma and matched controls underwent rollercoaster rides to evoke positive emotional stress (cf. Meston & Frohlich, 2003). Dyspnea, lung function, and control variables were repeatedly measured over a 2-day period. The hypothesis was tested that positive emotional stress after riding a rollercoaster interferes with dyspnea perception, resulting in low-dyspnea scores among women with asthma. It was expected that the rollercoaster would evoke anticipatory negative emotions in conjunction with enhanced heart rate and blood pressure shortly before the task, and positive emotions in conjunction with enhanced heart rate and blood pressure immediately after the task.
The rollercoaster rides were selected for this study because they would not meet the ethical and practical problems of induction of emotional states. The participants were tested whether their anticipatory feelings met the criterion of a positive emotional stress task. In this respect, all participants had prior experience with a rollercoaster ride and claimed that they would enjoy the task. Pilot testing showed that the heart rate acceleration mentioned from novice riders in literature (Kuschyk, 2005; Pringle, Macfarlane, & Cobbe, 1989) were not reached. Because of this rather mild heart rate acceleration after a single ride, it was decided to have all participants do the ride twice, one immediately following the other.
Only women were selected for this study because of huge gender differences in both stress response and symptom perception. With respect to stress response, Taylor et al. (2000) emphasized the gender difference in their ‘Tend–Befriend’ versus ‘Fight–Flight’ stress response. They argued that these basic differences have physiological and endocrinological correlates with consequences for all aspects of the stress response (cf. Matthews, Davis, Stoney, Owens, & Caggiula, 1991; Matthews and Stoney, 1988). With respect to gender differences in symptom perception, both clinical and experimental studies have shown that women report more somatic symptoms, including dyspnea, and cough more often, than men (Gijsbers-van Wijk, Huisman, & Kolk, 1996; Rietveld & Rijssenbeek-Nouwens, 1998). Although these differences may reflect gender differences in mood states, rather than differences in perceptual capacity (Gijsbers-van Wijk & Kolk, 1997), the current study was based on a homogenous group with only young women with and without asthma taking part.
Heart rate and blood pressure were repeatedly measured as markers of physiological arousal, in order to confirm the effect of the rollercoaster, and to gain insight in the physiological response underlying dyspnea perception. Positive and negative mood states were measured as a rough indicator of feeling states throughout the study. Somatic symptoms relating to the rollercoaster were also repeatedly measured. Trait anxiety was measured as a marker of neuroticism, to be able to exclude highly anxious individuals, and to gain insight in the influence of neuroticism on dyspnea perception. Individuals with high scores on neuroticism would (a) eagerly scan their body for signs and symptoms of disease; (b) be vulnerable to falsely perceive general sensations in terms of asthma and dyspnea; and (c) react emotionally and excessively to dyspnea (Rietveld & Houtveen, 2004).
Section snippets
Participants
The participants were 25 female university students with a medical diagnosis of severe asthma who were matched on age, gender, and education with 15 healthy controls. Control women were, according to self-report intake forms, free of chronic disease and were symptom-free at intake.
All women with asthma used inhalation corticosteroids in excess of 800 mg daily. They continued using this kind of medication during the test period, which serves to control airway inflammation and decreases the
Results
All analyses were conducted using a 2 (group: asthma, control)×4 (measurement: intake, just before rollercoaster rides, immediately after rollercoaster rides, 24 h after rollercoaster rides) analysis of variance with measurement as within variable. In addition, Tukey's HSD comparisons were performed to determine the nature of the effects. The means and standard deviations of all dependent measures are presented in Table 1.
Discussion
The results showed that women with asthma experienced more dyspnea during negative emotional stress in conjunction with a normal lung function, than during positive emotional stress and a reduction in lung function, even though 39% of these women had a reduction in lung function of >10%. For women without asthma, dyspnea followed the same pattern as dizziness, nausea, and heart pounding: that is, peaking after and not before the rollercoaster rides. The overall results (a) supported the
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This research was supported by a grand from the Netherlands Asthma Foundation awarded to Simon Rietveld, and by a Veni grant from the Netherlands Organization for Scientific Research (NWO: 451-04-069) to Ilja van Beest.