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Psychosomatic Medicine 62:401-412 (2000)
© 2000 American Psychosomatic Society


ORIGINAL ARTICLES

Emotions and Stress Increase Respiratory Resistance in Asthma

Thomas Ritz, PhD, Andrew Steptoe, PhD, Stephen DeWilde, MRCGP and Marco Costa, MSc

From the Departments of Psychology (T.R., A.S.) and General Practice (S.D.), St. George’s Hospital Medical School, University of London, London, United Kingdom; and the Department of Psychology (M.C.), University of Bologna, Bologna, Italy.

Address reprint requests to: Thomas Ritz, PhD, Department of Psychology, St. George’s Hospital Medical School, Tooting, Cranmer Terrace, London SW17 ORE, United Kingdom. Email: tritz{at}sghms.ac.uk


    ABSTRACT
 TOP
 ABSTRACT
 INTRODUCTION
 METHODS
 RESULTS
 DISCUSSION
 CONCLUSION
 ACKNOWLEDGMENTS
 REFERENCES
 
OBJECTIVES: Clinical reports suggest that various emotions and types of stress can precipitate asthmatic symptoms, but there is little experimental evidence to substantiate this claim. We studied the impact of different emotional states and stress on respiratory resistance in asthmatic and nonasthmatic individuals.

METHODS: Participants (24 asthmatic and 24 nonasthmatic patients) viewed short film sequences selected to induce anxiety, anger, depression, elation, happiness, contentment, or a neutral affective state and completed two stressful tasks, mental arithmetic to induce active coping efforts and viewing of medical slides to induce passive coping efforts. Oscillatory resistance, heart rate, blood pressure, baroreflex sensitivity, skin conductance level, respiration rate and volume, and self-reported affective state were measured throughout the session.

RESULTS: Uniform increases in oscillatory resistance were found in all emotional states compared with the neutral state and during mental arithmetic in both groups. Asthmatic patients showed stronger reactions to the medical slides than healthy control subjects, with significant increases in oscillatory resistance, blood pressure, skin conductance level, and minute volume, as well as higher levels of self-reported depression, arousal, and shortness of breath. Changes in oscillatory resistance were inconsistently correlated with other physiological indices.

CONCLUSIONS: Various emotional states and stress increase oscillatory resistance largely independently of concurrent increases in autonomic or ventilatory activity. The particular sensitivity of asthmatics to passive coping demand requires additional research.

Key Words: asthma • emotion • stress • respiratory resistance

Abbreviations: ANOVA = analysis of variance; BR = baroreflex; BRS =baroreflex sensitivity; BRSd = baroreflex sensitivitydown sequences; BRSu = baroreflex sensitivity upsequences; DBP = diastolic blood pressure; FRC = functionalresidual capacity; HR = heart rate; MANOVA = multivariateanalysis of variance; Ros = oscillatory resistance; RR = respiration rate; SBP = systolic blood pressure; SCL = skin conductance level; Vmin = minutevolume; VT = tidal volume.


    INTRODUCTION
 TOP
 ABSTRACT
 INTRODUCTION
 METHODS
 RESULTS
 DISCUSSION
 CONCLUSION
 ACKNOWLEDGMENTS
 REFERENCES
 
The study of psychological influences on pulmonary function has been a pervasive topic in asthma research throughout the years. Although a considerable body of experimental work has been published on the effects of bronchoconstrictive suggestions, comparably few experiments have been dedicated to the effects of emotions and stress on the airways (see Refs. 1 and 2 for reviews). Clinical reports have listed a variety of affective states as potential precursors of asthmatic symptoms (35). It has also been suggested that distinctive emotional states, such as sadness or depression, are particularly linked to an aggravation of symptoms in persons with asthma (6, 7). Similarly, experimental studies have shown that different emotional states, such as anxiety, anger, and joy, are equally capable of eliciting increases in airway resistance in asthmatics (810). However, no systematic comparison of a broader range of emotional states has yet been attempted, and comparisons between states of positive and negative valence are rare. Given the previous bias of experimental research in favor of negative emotions, the evidence for resistance increases is currently most robust for these affective states.

The fact that resistance increases are uniformly reported for negative and positive affective states has led to the alternative suggestion that valence-nonspecific emotional arousal might actually modulate airway response. A recent experiment of the first author involving induction of happy, depressed, and neutral states in nonasthmatic individuals yielded evidence of this type of response: Whereas resistance during neutral states remained largely unchanged, resistance increases were observed during both emotional states (11). In general, theoretical models organizing emotional experience along dimensional variables, such as valence or arousal, rather than categories of emotional states, such as anxiety, anger, and happiness, have been hypothesized to be superior in the study of respiration (12). It was therefore the aim of our study to investigate effects of different categories of emotional states on respiratory resistance in asthma and to explore whether airway response is determined by specific emotional states or by experienced arousal. Our physiological measurements included electrodermal activity, which has been established as a reliable marker of valence-nonspecific emotional arousal (13, 14).

Investigations into airway effects of stressful tasks remain inconclusive. Although a number of studies have reported increases in airway resistance during mental arithmetic (1517), loud noise stimulation (18), or aversive accident or operation films (16, 19, 20), other studies have reported no changes during mental arithmetic (21, 22) or even decreases during a reaction time task and mental arithmetic (23). Lehrer et al. (24) proposed that the active vs. passive coping demand of the task could be a useful distinction in explaining airway response to stress. Active tasks, such as mental arithmetic or a reaction time task, should lead to decreases in airway resistance, whereas passive tasks, such as viewing distressing films or noise stimulation, should lead to increases.

The rationale for this idea lies in the specifics of the autonomic regulation of the airways. The airway smooth muscles are mainly constricted by vagal excitation, whereas relaxation of the smooth muscles is triggered by sympathetic influences, in particular circulating epinephrine. Research into behaviorally evoked airway responses is therefore confronted with a paradox (2527): It could be expected that emotional arousal and psychosocial stress decrease airway resistance to the degree that they are accompanied by sympathetic activation and/or parasympathetic withdrawal. Experimental tasks that demand an active coping response typically elicit similar autonomic adjustments and are therefore expected to decrease airway resistance (24).

However, this is not in line with a remarkable number of clinical and experimental observations suggesting that increases in airway resistance are due to stress or states of emotional arousal. Studies using bronchoconstrictive suggestions, clearly arousing in their aversive character, have presented evidence of vagal mediation of increases in airway resistance (28, 29). These increases occur despite evidence of a concurrent sympathetic excitation (30), suggesting a nonreciprocal pattern of autonomic functioning under these experimental conditions. Vagally mediated bronchial constriction and extrabronchial sympathetic activity seem to be elevated in parallel in various stressful situations. It can be speculated that these are instances of emotional coactivation of the autonomic branches (31), which become particularly salient when airway response as a predominantly parasympathetic index is included in the study.

Increases in airway resistance can more readily be explained in stressful situations that are unavoidable or inescapable for the individual, demanding a passive coping response (24). Experimental situations demanding this type of behavioral adaptation typically lead to stronger vagal activation (32) and thus can be expected to trigger airway constrictions. A number of studies have confirmed this idea, with stressful films or noise stimulation leading to elevated airway resistance levels.

With respect to disease states such as asthma, additional assumptions are required to explain the hyperresponsiveness of the airways to psychosocial stimuli. A classic psychosomatic explanation draws on increased vagal discharge as a result of maladaptive conflict regulation and dysfunctional behavioral patterns (33). Specifically, habitual conservation-withdrawal reactions accompanied by the experience of depression and despair have been hypothesized to lead to strong, vagally mediated constrictions of the airways in asthmatic persons (6, 7, 33). Following this line of reasoning, one would also expect a stronger airway response of asthmatics to passive coping tasks. Studies comparing nonasthmatic and asthmatic groups in their response to aversive films are not fully consistent, with some showing a stronger response in asthmatics (16, 19) and others showing no differences (24).

Less attention has been directed to indices of sympathetic nervous system functioning. In earlier studies, there was speculation about diminished sympathetic responsiveness in asthmatic persons (34, 35). In a small sample of patients, Mathé and Knapp (16) reported evidence of a blunted response of the hypothalamic-medullary axis during stress in asthmatics. Alternatively, ß-receptor dysfunctioning has been postulated to account for asthmatic airway response; however, results remain largely inconclusive, and ß-receptor downregulation after ß-adrenergic bronchodilator use has to be taken into account as an alternative explanation (36).

Another explanation for a decreased sympathetic response and increased vagal discharge in asthmatics could lie in a stronger sensitivity of the BR. Carotid sinus and cardiac baroreceptors fire in response to arterial pressure increases, leading to vagally mediated HR slowing and a withdrawal of sympathetic efferent outflow. Hypersensitivity of this reflex action would lead to a stronger downregulation of the cardiovascular system in response to arterial pressure increases. BRS has been studied as an index of vagal system functioning in the cardiac system (37, 38). It is not known to what degree this reflex action generalizes to other autonomic systems. Animal experiments present evidence of a depression of ventilation during carotid baroreceptor stimulation (39). With respect to asthma, stronger BRS was observed in a subgroup of patients classified as intrinsic asthmatics (40); this sensitivity was thought to be related to a general cholinergic hyperresponsiveness in this patient group at different peripheral organ sites, including the bronchi. Although BRS is not a pure index of vagal control, because the reciprocal action of sympathetic efferent outflow is included in the reflex-induced HR adjustments, moderate positive correlations can be observed with other noninvasive indices of vagal functioning (4143). In addition, as studies with ß-adrenergic blockade have shown, sympathetic effects contribute to BRS to only a limited degree, particularly during the "up sequences" of the BR action, when cardiac slowing is triggered by blood pressure increases (43, 44).

Given these conflicting results and uncertainty about the mechanisms of airway responses to stress, additional investigation of active vs. passive coping tasks is indicated. In this study, we investigated sympathetic mechanisms and BR regulation as potential mediators of airway response to stress, particularly their contribution to a potentially stronger responsiveness of asthmatics to stressful tasks. Earlier research demonstrated a depression of BRS under behavioral stress (45), particularly during mental arithmetic (46). Stronger airway responses in asthmatics could be related to increases or a smaller depression in BRS under stressful conditions.


    METHODS
 TOP
 ABSTRACT
 INTRODUCTION
 METHODS
 RESULTS
 DISCUSSION
 CONCLUSION
 ACKNOWLEDGMENTS
 REFERENCES
 
Participants
Asthmatic patients and nonasthmatic participants (each N = 24) were recruited as volunteers from a local general practice. They responded to a letter of invitation to participate in a study on "everyday life experience and breathing." Five more participants (three asthmatics) were tested but excluded because of equipment failure. Groups were matched by age (mean, 30.0 years; range, 20–48 years) and gender (16 women). The complete protocol included keeping a peak-flow diary for 3 weeks after the laboratory session, which will be the subject of another report. All participants were nonsmokers and were free of psychiatric illnesses, cardiovascular diseases, family history of cardiovascular diseases, and respiratory diseases other than asthma (the nonasthmatic group had no respiratory diseases). Nonasthmatic patients were selected at random for the appropriate categories of age and gender from the register of the general practice. Their clinical notes indicated no serious illnesses. Degree of severity in asthmatic patients was mild to moderate (47). The mean duration of asthma was 16.9 years (range, 1–33 years), and the mean age of onset was 11.4 years (0–29 years); all but three reported onset before the age of 18 years. Allergic triggers were reported by 21 of the asthmatic patients (12 underwent skin tests [tests were not part of our procedures], the results of which were positive), and exercise triggers were reported by 20; psychological triggers were recalled as important in19 patients (in 6 of these patients only in combination with other exogenous trigger factors). Patients continued to take their prescribed asthma medication, which consisted mainly of ß-adrenergic bronchodilators or inhaled corticosteroids (no oral corticosteroids or long-acting bronchodilators were used). Asthmatic patients were tested during symptom-free periods and were instructed to take the last dose of their ß-adrenergic bronchodilators (if necessary) at least 8 hours before arriving at the laboratory.

Experimental Films and Tasks
Participants viewed seven film sequences that were preevaluated for eliciting certain emotional states, such as anxiety, anger, sadness, happiness, contentment, or neutral states (48). Most of the sequences were taken from commercially available movies. After a pilot test was conducted, two sketches of a British comedian were chosen for induction of happiness and elation to match cultural preferences. The duration of the film clips ranged from 90 to 290 seconds (mean = 224 seconds). The order of the films was randomized between participants; {chi}2 tests revealed no significant order effects for individual clips (p > .68–.99).

A mental arithmetic task was presented to elicit active coping behavior. A colored slide with seven lines of 14 one- and two-digit numbers was projected onto a screen. Participants were instructed to add up as many numbers as possible in 3 minutes. They were informed that the correctness of their results would be checked and were given fictional information about a difficult target most participants had previously achieved. Participants were instructed to calculate "in their mind" and not to move their lips, whisper, or "speak silently" during calculating. This task has been shown in a number of studies to elicit substantial cardiovascular and sympathetic nervous system responses (45, 49, 50). For passive coping behavior, nine medical slides from the International Affective Picture System (slides 3000, 3010, 3100, 3120, 3130, 3140, 3150, 3170, and 3250; Ref. 51) depicting injuries, mutilation, and corpses were presented in a continuous series for 3 minutes (20 seconds per slide). Participants were instructed to watch the screen and keep their eyes open during the whole presentation. The order of the active and passive tasks, as well as the films vs. tasks, was counterbalanced within each group.

Equipment and Measures
Physiological measures.

Total respiratory resistance was measured by forced oscillations using the Siemens Siregnost FD 5 with a fixed oscillation frequency of 10 Hz. The principles and technique of this method have been described extensively (52, 53). The participants breathe ambient air through a mouthpiece and tube (resistance, 0.015 kPa/liter per second) with the nose occluded. The obtained resistance measure (Ros, measured in kPa/liter per second) includes resistances of the total respiratory tract as well as tissue resistances; however, high correlations with the most sensitive measurement technique of airway resistance, the body plethysmography, have been reported (54). During the measurements, the cheeks were supported by an elastic band. Ros was recorded in a moving average of 7 seconds using a Grass 7D polygraph (Stag Instruments, Chalgrove, UK). Protocols were scored manually offline after artifacts in Ros due to swallowing were eliminated. Signals of 12 participants in each group were scored by a rater blinded to the experimental conditions, and initial analysis showed that the results were not affected by differences between raters.

VT was measured by means of a heated Hans Rudolph flow head (Type 3803) with a CS5 integrator (GM Instruments, Glasgow, UK) attached. The distal end of the oscilloresistometer tube was connected to the flow head. Zero drift of the equipment was automatically corrected after each breath. VT was estimated by expiratory flow under body temperature/pressure-saturated conditions. The output of the integrator was fed to the polygraph. Protocols were scored for VT and RR, and Vmin was calculated as VT x RR.

Skin resistance level was measured with Ag-AgCl electrodes (18 mm inner diameter) positioned on the thenar and hypothenar eminences of the left hand. Resistance was scored from the polygraph trace every 15 seconds, averaged across each trial, and converted to a log SCL value.

Beat-to-beat HR, SBP, and DBP were monitored continuously with a Finapres (model IV, TNO Biomedical Instrumentation, Amsterdam, Netherlands). The Finapres cuff was fitted to the middle phalanx of the middle finger of the left hand, which was positioned on an adjustable armrest at the level of the heart. Signals were sampled at 10 Hz and digitized using a Cambridge Electronic Design interface 1401 and were subsequently processed by microcomputer. BRS was analyzed offline using the spontaneous sequence technique (46). Sequences were detected in which SBP increased or decreased at least 1 mm Hg for three or more consecutive pulse intervals. Sequences of increasing SBP that were accompanied by a series of progressively lengthening pulse intervals (starting with lag 1, at least 4 ms per cycle) were identified as BRSu, and sequences of decreasing SBP accompanied by a series of shorting pulse intervals qualified as BRSd. For each individual sequence, a correlation coefficient and intercept were computed, and sensitivity was expressed as the change in pulse interval per change in SBP (ms/mm Hg). Only sequences with a correlation coefficient >0.80 were included. Average BRS was calculated separately for BRSu and BRSd.

BRS could not be analyzed in full for one participant because the number sequences was too low in some of the trials. Two asthmatic patients did not complete the passive coping task; condition means were thus calculated from remaining 50 or 130 seconds of measurements. Three participants removed the tube too early after the task and were consequently not included in the recovery analysis of Ros.

Psychological measures.
Self-reports of shortness of breath and emotion were given using visual analog scales (~8 cm) anchored with "not at all" and "quite strong." The list of emotions consisted of seven items: content, happy, anxious, depressed, angry, elated, and disgusted. In addition, for a dimensional description of the affective response, the nine-point Self Assessment Manikins of pleasure and arousal (55) were administered. For ease of interpretation in this report, 1 was assigned to the "displeasure" or "calm" poles of the scales, and 9 was assigned to the "pleasure" and "excited" poles. Six participants had missing values in one or the other rating scale. To compare both groups in terms of habitual affectivity and defensiveness, the Affect Intensity Measure (56), Toronto Alexithymia Scale (57), and Social Desirability Scale (58) were administered before the experiment.

Procedure
All laboratory sessions were scheduled individually in the afternoon or early evening. Participants first completed the questionnaires in a separate room. During the physiological measurements, participants were seated in a padded armchair in a light- and temperature-controlled laboratory. Data recording was directed from an adjacent control room. After the procedures had been explained, the transducers were attached. Participants were then trained in the use of the mouthpiece and nose clip for the respiration measurements. The experimental protocol started with a 5-minute rest period; during the last 3 minutes, measurements were recorded and served as baseline values. The lights were dimmed, and participants were instructed to keep their eyes open during all stages of the experiment and to avoid gross body movements. Ratings were then obtained on the mood and symptom scales and again after completion of each task or film clip. Participants were encouraged to complete the scales according to their personal feelings during the respective task or film rather than to follow any presumed expectations. After the last film or task, transducers were removed, and participants were given a short debriefing. Full information about the aims and background of the study were given after patients turned in the 3-week peak-flow diary, which followed the laboratory session.

Data Analysis
Physiological and psychological variables were analyzed by means of two-way, repeated-measures ANOVAs with group (asthmatic or nonasthmatic) as a between-participants variable and with film (seven levels: anxiety, anger, depression, neutral, elation, happiness, and contentment) or task (two levels: mental arithmetic and medical slides) as the within-participants variable. A Geisser-Greenhouse correction on degrees of freedom was performed when necessary. The success of emotion induction by films was tested by contrasting the ratings of the target emotion for the respective film with the ratings of the same emotion for 1) all other films and, as a more conservative criterion of success, 2) with the ratings of the same emotion for all other films of the same valence. In addition, the neutral film was expected to be lower in all target emotional states than the respective films. Ros was analyzed in two ANOVAs for measurements during film or task administration and for the first 20 seconds of measurements after films or tasks. This was done to study the short-term recovery of Ros. In line with earlier research, we tested two a priori hypotheses: 1) Increases in Ros would be found in asthmatics during negative emotional states compared with the neutral state, and 2) increases in Ros would be found in both groups during positive and negative emotional states as compared with the neutral state. The latter contrast was also tested for self-reported arousal and SCL as indicators of valence-nonspecific emotional arousal (13). Additional comparisons of means were calculated post hoc by means of the Newman-Keuls procedure (p < .05). Table 1 summarizes expected effects in autonomic indices for active and passive coping tasks and hypothetical differences between asthmatic and nonasthmatic patients derived from the literature.


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Table 1. Predicted and Observed Stress Effects in Asthmatic and Nonasthmatic Participantsa
 
Product-moment correlations (two-tailed significance test) were calculated for change scores of physiological parameters to elucidate covariation of Ros with other physiological indices between participants. Change scores were calculated by subtracting baseline from task measurements and neutral from emotional film measurements.


    RESULTS
 TOP
 ABSTRACT
 INTRODUCTION
 METHODS
 RESULTS
 DISCUSSION
 CONCLUSION
 ACKNOWLEDGMENTS
 REFERENCES
 
Baseline Differences
No group differences in baseline physiological measures or ratings were found (Table 2). Similarly, an overall MANOVA did not detect group differences in terms of habitual affectivity or defensiveness (F < 1).


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Table 2. Baseline Physiological Indices
 
Film Effects
Self-reported measures.

Each film reliably elicited the respective target emotion and revealed significantly higher ratings for this emotion than all other films (F(1,46) = 26.61 to 69.40, p values < .0001). Negative films were also effective when their respective target emotion ratings were compared with ratings of the same emotion in all other negative films (F(1,46) = 24.52 to 60.87, p values < .0001). However, comparison of target emotion ratings within positive films was not fully successful: The happiness film did not elicit higher happiness ratings when compared with the contentment film (F < 1), and the contentment film elicited only marginally higher contentment ratings when compared with the happiness and elation films (F(1,46) = 3.10, p < .084). The neutral film was significantly lower in all target emotions compared with the respective emotional films (F(1,46) = 21.77 to 51.93, p values < .001). Emotional films elicited more arousal than neutral films (F(1,45) = 9.05, p < .004), and post hoc tests revealed significantly higher arousal ratings for all but the contentment film (Figure 1, bottom). No differences between groups were found in self-reported responses to films.



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Fig. 1. Effects of emotional film sequences on Ros, SCL, and self-reported arousal in asthmatic and nonasthmatic patients.

 
Physiological measures.
For Ros, a significant effect of film presentation was found (F(6,276) = 7.42, p < .001). Ros was increased during all emotional films compared with the neutral film (Figure 1, top); the contrast was highly significant (F(1,46) = 39.66, p = .001), as was the contrast for increased Ros during negative emotional films for asthmatics (F(1,46) = 32.89, p < .001). Ros was still increased during the first 20 seconds after film presentations, (F(6,276) = 2.18, p = .046), with significant contrasts for emotional films compared with the neutral film (F(1,46) = 12.85, p < .001) and for asthmatics during negative films (F(1,46) = 12.93, p = .001).

Additional effects for film presentation were found in HR, RR, and SCL (F(6,276) = 3.78, 7.16, and 2.35, respectively; p values < .001, .001, and .049, respectively). Post hoc tests revealed higher RR during the anger and elation films as compared with the neutral film. SCL yielded a significant quadratic trend (F(1,46) = 6.14, p = .017), with higher values for emotional films compared with the neutral film (Figure 1, middle). Although means suggested a stronger response in some of the physiological measures, no significant main effects for group or interaction effects of group-by-film presentation were found. Only a few substantial correlations were found between increases in Ros (from neutral to emotional films) and changes in other physiological indices. In asthmatics, Ros during the anger film was positively correlated with RR (r = .41, p = .048); in nonasthmatic control subjects, Ros during the happiness film was positively correlated with RR and Vmin (r values = .52 and .42, respectively; p values = .009 and .041, respectively).

Task effects
Self-reported measures.
Task administration had a strong impact on emotion and shortness of breath ratings, as revealed by the task effect of the overall MANOVA (F(20,21) = 120.4, p < .001). Post hoc tests conducted after univariate ANOVAs showed that both tasks elicited significant increases in arousal and anxiety as well as decreases in pleasure, happiness, and contentment. The medical slides specifically increased depression, anger, and disgust.

Group-by-task interactions were found for shortness of breath (F(2,90) = 3.27, p = .043), depression (F(2,90) = 4.97, p = .016), and arousal (F(2,80) = 5.06, p = .009). This was due to group differences in medical slides, for which asthmatic patients reported significantly stronger increases in these ratings (Figure 2). Post hoc test also revealed higher task ratings in anxiety in the asthmatic group than in the nonasthmatic group.



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Fig. 2. Effects of active vs. passive coping tasks on selected physiological and self-reported measures in asthmatic and nonasthmatic patients.

 
Physiological measures.
Ros increases were observed during both tasks in both groups (F(2,92) = 12.45, p < .001). Post hoc tests comparing baseline with task means were significant for both tasks in asthmatic patients and for mental arithmetic in nonasthmatic subjects (Figure 2). During recovery, Ros remained elevated only in asthmatics, as revealed by a group-by-task interaction (F(2,86) = 4.71, p = .015) and significant results on post hoc tests. Substantial increases were found in HR, SBP, DBP, and SCL during tasks (F(2,92) = 31.91, 42.75, 35.32, and 20.49, respectively; p values < .001). Post hoc tests comparing baseline with task means were significant for all indices during mental arithmetic in both groups and for SBP, DBP, and SCL during medical slides in asthmatics. BRSu and BRSd were reduced during mental arithmetic in both groups (task: F(2,92) = 6.52 and 11.25, respectively; p values < .001 and .003, respectively); no main or interaction effects involving group were found. Table 1 summarizes expected and observed task effects for autonomic indices.

Group-by-task interactions revealed in asthmatic patients a smaller HR increase during mental arithmetic (F(2,92) = 3.51, p < .042) and a stronger increase in Vmin during viewing of medical slides (F(2,92) = 3.05, p < .052) (Figure 2).

For asthmatic patients, changes in Ros during mental arithmetic were negatively correlated with changes in BRSu and BRSd (r values = -.41 and -.49, respectively; p values = .047 and .016, respectively), indicating that stronger reductions in sensitivity were related to stronger increases in Ros. Changes in HR were also negatively related to changes in BRSu and BRSd in asthmatics (r values = -.51 and -.53, respectively; p values = .011 and .086, respectively) and nonasthmatics (r values = -.50 and -.67, respectively; p values = .011 and .001, respectively), suggesting that both increases in Ros and HR were linked to BRS decreases. In addition, changes in Ros were negatively related to changes in VT during both mental arithmetic and viewing of medical slides in the group with asthma (r values = -.38 and -.42, respectively; p values = .077 and .047, respectively).


    DISCUSSION
 TOP
 ABSTRACT
 INTRODUCTION
 METHODS
 RESULTS
 DISCUSSION
 CONCLUSION
 ACKNOWLEDGMENTS
 REFERENCES
 
Effects of Emotional Films on the Airways
Emotion induction by films revealed a striking and reliable pattern of changes in Ros. All emotional conditions showed increases in Ros compared with the neutral condition. This pattern was observed in measurements made during the films and to a slightly smaller degree in measurements made during the first 20 seconds after the films. Although the Ros increases are in line with those reported in clinical and experimental studies of airway response due to negative or positive emotional arousal (310), the Ros changes in our study were not specific to asthmatics. No interaction effects involving the group variable materialized, suggesting a general regulatory adjustment of airway resistance to this type of stimulation. A similar pattern of changes was also observed in nonasthmatic students in an earlier study of the first author, which involved viewing and imagery of happy, depressing, and neutral affective slides and self-referent statements (11). Research into behaviorally evoked airway responses indeed suggests qualitatively similar response patterns for nonasthmatic and asthmatic individuals, often with stronger responses in asthmatics (8, 16, 18, 19). The comparable intensity of response in both groups of our study may be due to effective medication management of the disease.

The only other measures that showed a comparable pattern of changes due to emotion induction were SCL and arousal ratings. It is tempting to interpret these findings as evidence of an arousal modulation of airway smooth muscle tone. Electrodermal activity is known to vary with the valence-nonspecific arousal of affective states (13, 14). However, the data did not completely fit this view: SCL was not increased during the depression film, and arousal ratings for contentment were not elevated above the neutral level. Future studies will need to determine whether these are sample-specific findings or whether behavioral determinants of airway resistance have to be conceptualized in different terms.

Physiological Mechanisms of Emotion-Induced Ros Increases
Our results revealed little about possible mechanisms of the observed Ros changes during emotion induction. SBP, DBP, and BRS measured as indices of sympathetic functioning and cardiovascular regulation showed few consistent changes, and correlational analyses remained uninformative. HR increased only under some conditions, and the direction of changes was opposite to expectations, which were based on a reciprocal mode of autonomic functioning. Ventilatory changes, which can influence airway tone and resistance measurements in a number of ways (5961), were significant only under some conditions, with happiness and elation showing the strongest increases in Vmin.

FRC is one of the most powerful ventilatory mediators of resistance changes but could not be included in this study. Inferring changes of FRC noninvasively from the end-expiratory volume level of the pneumotachograph trace (62) would have required the participants to breathe through the mouthpiece continuously throughout the experiment, a condition that is hardly tolerable and obviously counterproductive in emotion research. However, we do not believe that FRC changes facilitated the increases in Ros during viewing of emotional films. Behaviorally triggered increases in FRC, which would lead to relaxation of the airway smooth muscles, have typically been observed in situations requiring effort or coping with aversive events, such as the production of emotional facial expression (63) or sudden cooling of the skin (64). Therefore, FRC increases would be expected during emotional rather than neutral conditions, and these changes would have acted against the pattern of Ros increases we observed during emotional films.

Effects of Stress Tasks on the Airways
The results with our stress tasks did not confirm the main findings of Lehrer et al. (24), who observed decreases in Ros during active coping and no changes during passive coping. We found significant increases in Ros in both groups for the active coping task and in asthmatic patients for the passive coping task. Our results are therefore more in line with those of other studies of the effects of mental arithmetic (1517) and distressing films (16, 19, 20) on the airways. Lehrer et al. speculated that characteristics of the experimental situation in which the active coping task was administered, such as unavoidable criticism, might actually have elicited a passive coping response instead of the desired active response. However, the pressor response to mental arithmetic observed in cardiovascular variables and the BR suppression were typical responses to be expected under active coping demand (32, 46). In addition, the increases in depression, disgust, and anger that we found selectively for the passive task (medical slides) supported the idea of qualitative differences between the tasks in terms of active vs. passive coping.

It was interesting to note that the Ros increases in the initial period after completion of the stress tasks were more persistent in asthmatic than in nonasthmatic subjects. This can be explained only in part by a stronger airway response of asthmatics to the tasks, because group differences in response were seen only for the passive task. The finding is consistent with the results of Levenson (19), who reported sustained elevation of Ros in asthmatic patients after viewing of a particularly stressful film. A slower recovery from bronchoconstriction would obviously be an interesting feature with respect to disease states of the airways. Particular deficiencies of the organ system in recovery from behavioral stress have been studied as characteristics of other diseases, such as hypertension (65, 66), and our results at least suggest the recovery issue as an important direction for future studies of stress in asthma.

Sensitivity of Asthmatic Patients to the Passive Coping Task
More intriguing were the group differences we found with our experimental tasks. Asthmatic patients seemed to experience the passive coping task as more aversive than nonasthmatic participants. This was suggested by a higher level of self-reported shortness of breath and depression as well as a stronger response in a number of physiological indices, including Vmin, SCL, SBP, and DBP. For the latter three variables, the group-by-task interaction was not significant, but group differences in response were established by post hoc tests. The same was true for the response of Ros to the passive task, which was not significantly different from the baseline value in nonasthmatic participants. The more stressful character of the task for asthmatic individuals was also suggested by the fact that two of them declined to complete the task after viewing the first slides.

We can only speculate about the reasons for these group differences. The amount of Ros increases was not substantially different from that recorded during the active coping task or film viewing, and increases in the participants who interrupted the tasks were not clinically significant. Thus, the actual state of the airways was hardly a source of greater discomfort. Moreover, the observed response pattern in asthmatic patients was one of greater sympathetic activation during passive coping rather than of a stronger parasympathetic response. At first glance, this seems to contradict the hypothesis of a stronger vagal discharge during passive coping (32) and of a habitual response in asthmatics in particular (33). However, it is reminiscent of a number of speculative comparisons made between asthmatic and blood-phobic patients (7, 24, 33, 67). Typically, the response of a blood-phobic patient is of a biphasic nature, with increasing sympathetic arousal in the first phase, followed after some minutes by a second phase of a strong vagal discharge with cardiac inhibition (6769). The biphasic response is not restricted to phobic patients but can be observed in nonphobic patients to a smaller degree (69). It could be speculated that asthmatic patients are more sensitive to blood and injury-related stimuli because of their potential for triggering vagal discharge and leading to bronchial contractions. The greater sympathetic arousal observed in our group could then be interpreted as the first phase of a mild blood-phobic response.

Role of Sympathetic Mechanisms in the Airway Response to Stress Tasks
Concerning the mechanisms involved in the observed Ros increases during the tasks, we did not find compelling evidence of a sympathetic dysfunction in asthmatics. SBP and DBP both increased in response to mental arithmetic, and an even stronger response was seen in asthmatics during viewing of the medical slides. The lack of substantial covariation in Ros suggested an uncoupled relationship between these predominantly sympathetic indices and airway resistance. A further lack of relationship was observed between Ros and HR or SCL, both of which increased parallel to Ros, a pattern similar to that observed during film viewing. This observation is confirmed by results of other studies using stress or emotion induction in asthmatics (8, 15, 24), with some studies even reporting positive correlations between response in airway resistance and DBP (30) or SCL (70). Results such as these suggest an independence or even nonreciprocal coupling of the airway and cardiovascular or sudomotor systems during behavioral stimulation. However, it is worth noting that the HR response in asthmatics to mental arithmetic was actually weaker than in nonasthmatic control subjects. A similar finding was reported by Lehrer et al. (24). Before this is interpreted as a deficiency in sympathetic functioning, medication effects have to be considered as an alternative explanation. Commonly used ß-adrenergic bronchodilators have systemic side effects, and longer administration might lead to downregulation of the ß-receptors (36, 71). Unfortunately, the medication regimens in our patients were too homogenous to allow a comparison of HR response in medication subgroups.

Ventilatory and Upper Airway Effects
Finally, we found only limited evidence of indirect or artifactual mediation of Ros changes during the experimental tasks. Respiratory parameters other than Ros were not significantly affected by either stress task. VT changes seemed to have had a modulatory effect on Ros response during mental arithmetic in asthmatics. The negative correlations between Ros and VT changes correspond both to a reflex mechanism by which deep inspirations dilate the airways (59) and to the basic principle of resistance measurements, in that higher calibers of the airways exert less resistance against air flow (72). However, given no changes in mean values, VT was unlikely to be responsible for the net increase in Ros. Furthermore, movements of the glottis must be considered as an important source of artifactual influences on Ros measurements. This can be a concern particularly for the mental arithmetic task, in which covered speech or subvocalization could be expected, resulting in artifactual increase in Ros. Similarly, subvocalization has been claimed to accompany emotional information processing (73) and thus could be suspected to underlie the Ros increases we observed during viewing of emotional films. We do not think that this type of artifact exerted an important influence on our results, because most of the effects in Ros were still present after the film or task administration, while the participants stared at a blank screen. In addition, the correlational analysis suggested a covariation of Ros with other autonomic and ventilatory adjustments in at least some instances. The subvocalization hypothesis also cannot explain comparable Ros changes in an earlier study that included reading and imagery of neutral sentences yet yielded increases during emotional vs. neutral experimental conditions (11).


    CONCLUSION
 TOP
 ABSTRACT
 INTRODUCTION
 METHODS
 RESULTS
 DISCUSSION
 CONCLUSION
 ACKNOWLEDGMENTS
 REFERENCES
 
Our study suggests a rather uniform tendency of the airways to constrict under conditions of positive and negative emotional stimulation as well as active or passive coping with stress. Although these increases were not clinically significant in their magnitude, their character confirms clinical observations that a variety of emotional and stressful states are precursors of asthmatic symptoms. Although the airway response of nonasthmatic subjects and asthmatic patients taking medication was largely comparable in intensity, asthmatic patients showed evidence of slower recovery after stress. The response characteristics of the airways can be characterized as nonspecific emotional arousal reactions, which are independent of or nonreciprocally coupled with sympathetic activation. No single autonomic or ventilatory mechanism could explain the airway response under all conditions. Because the airways are targets of various dilating and constricting influences (59), we cannot rule out that different mechanisms were operating under different conditions to produce the uniform increases in Ros. More in-depth investigations of the mechanisms underlying single emotional states and coping situations are needed to clarify this. The stronger evidence of a distress response of asthmatic patients during the passive coping task suggests that this type of behavioral demand might have special significance for asthmatic patients. Additional research is needed to elucidate the psychological importance and autonomic dynamics associated with passive coping, particularly with blood and injury-related stimuli, in asthma.


    ACKNOWLEDGMENTS
 TOP
 ABSTRACT
 INTRODUCTION
 METHODS
 RESULTS
 DISCUSSION
 CONCLUSION
 ACKNOWLEDGMENTS
 REFERENCES
 
This study was supported by a postdoctoral research grant from the German Academic Exchange Service and the Department of Psychology at St. George’s Hospital. We are indebted to Bernhard Dahme for equipment support and advice.

Received for publication May 17, 1999.

Revision received October 26, 1999.


    REFERENCES
 TOP
 ABSTRACT
 INTRODUCTION
 METHODS
 RESULTS
 DISCUSSION
 CONCLUSION
 ACKNOWLEDGMENTS
 REFERENCES
 

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