current perspectives on symptom perception in asthma: a biomedical and psychological review

INTERNATIONAL JOURNAL OF BEHAVIORAL MEDICINE, 6(2), 120-134 Copyright �9 1999, Lawrence Erlbaum Associates, Inc.

Current Perspectives on Symptom Perception in Asthma: A Biomedical

and Psychological Review

Simon Rietveld and Jos F. Brosschot

Symptom perception in patients with asthma is often inadequate. Patients may fail to perceive serious airway obstruction or suffer from breathlessness without objective cause. These extremes are associated with fatal asthma and excessive use of medicines, respectively. This article covers symptom perception in a multidisciplinary perspec- tive. A presentation of current definitions and methods for studying symptom perception in asthma is followed by a summary of theories on the origin of breathlessness. Next, biomedical and psychological factors influencing symptom perception are ex- amined. Preliminary biomedical research emphasizes neural pathway impairment, but causal factors remain inconclusive, particularly regarding the overperception of symptoms. Psychological studies suggest that the accuracy of symptom perception is influenced by (a) competition between asthmatic and nonasthmatic sensory information, (b) negative emotions, and (c) acquired response tendencies (e.g. habituation to symptoms, repression of symptoms, selective perception, and false interpretation of symptoms). These factors may favor either blunted perception or overperception. Empirical data in support of psychological factors are still insufficient. Methodological problems and procedures to improve symptom perception are discussed.

Key words: airway obstruction; asthma; breathlessness; symptom perception

Simon Rietveld, Department of Clinical Psychology, University of Amsterdam, The Netherlands; Jos F. Brosschot, Department of Psychology, Leiden University, The Netherlands.

Preparation of this article was supported by a post-doctoral fellowship to Dr. Jos F. Brosschot from the Royal Netberlands Academy of Art and Sciences.

The authors thank James Boutos, David Vaghi, and Cedric Sands for commenting on the original manuscript.

Correspondence concerning this article should be addressed to Simon Rietveld, Department of Psy- chology, Leiden University, Roetersstraat 15, 1018 WB Amsterdam, The Netherlands. E-mail: kp_rietveld @ macmail.psy.uva.nl

RIETVELD AND BROSSCHOT 121

A life-threatening attack of airway obstruction in asthma can develop within 1 hr, and awareness of symptoms and consequent rapid administration of medicines is essential. However, clinical observations indicate that patients with asthma may either consider themselves symptom-free in the midst of an asthma attack or con- versely suffer from breathlessness without airway obstruction (Boulet, Deschesnes, Turcotte, & Gignac, 1991; Rubinfeld & Pain, 1976, 1977). The general risks of inaccurate symptom perception include fatal asthma, inadequate use of (often potentially dangerous) medication, and poor asthma management (Creer, 1987; Creer & Gustafson, 1989). Some extreme examples may illustrate this. An adolescent boy with mild asthma, who previously participated in our research, left his house without using medication. Some minutes later he collapsed in the subway and died of suffocation on transport to the hospital. An adolescent girl experienced choking sensations after she had been painfully embarrassed at a party, but no evidence of airway obstruction could be found when her pulmonary function was tested in the emergency clinic.

Nevertheless, some patients with asthma may easily perceive an approaching attack and may accurately evaluate the state of their airways. There is no theory sufficiently explaining inaccurate symptom perception (Barnes, 1994; Jones, 1992; Pratter & Barter, 1991).

This article attempts to explain inaccurate symptom perception by examining the relevant literature. The first section comprises definitions and methods for studying symptom perception. The major theories on the origin of breathlessness are summarized. Next, biomedical and psychological factors influencing symptom perception are reviewed. The methodological influences in research are summarized, followed by an evaluation of the possibility to improve the accuracy of symptom perception in patients with asthma.

DEFINITIONS AND METHODS TO STUDY SYMPTOM PERCEPTION IN ASTHMA

Symptom perception refers to the conscious awareness of a symptom, which is based on unconscious information processing (the symptom perception process). Although physicians search for physical signs, patients have symptoms based on afferent neural information. Whereas biomedical research addresses the stimulus level, associated with pathophysiology, psychologists focus at the response level, associated with patients' complaints.

A first method to investigate the accuracy of symptom perception in patients with asthma is to study how breathlessness and lung function are related (Rietveld, 1998). A second method involves signal detection experimentation. The individuals breathe through a face mask and respond to externally applied airflow interruptions by pressing a button. The ratio between presented stimuli and correct detections de-

122 SYMPTOM PERCEPTION IN ASTHMA

notes perceptual accuracy (Dahme, Richter, & Mass, 1996). A third method of studying symptom perception in asthma comprises the relation between actual lung function and lung function as estimated by patients themselves (Reader, Dolce, Duke, Kazynski, & Bailey, 1990).

CLINICAL CRITERIA FOR AIRWAY OBSTRUCTION AND BREATHLESSNESS

The gold standard for airway obstruction is a reduction in lung function (forced expiratory volume in 1 sec) of> 20%. This reduction is considered clinically relevant, warranting bronchodilator medication.

Breathlessness (dyspnea) is usually described as difficult, labored breathing, shortness of breath, or tightness of the chest (Killian, 1988; Skevington, Pilaar, Routh, & MacLeod, 1997). Breathlessness is not specific to asthma and is common in healthy individuals after physical exercise and during attacks of hyperventilation, agoraphobia, or panic (Carr, Lehrer, & Hochron, 1992; Saisch, Wessely, & Gardner, 1996).

The experience of breathlessness seems to incorporate several different sensations. Participants in a study by Banzett and colleagues (1990) reported a coinci- dence of breathlessness and anxiety, discomfort, warm sensations, heart pounding, irritability, and headache. A factor analysis on symptom scores showed that breathlessness during airway obstruction comprises up to five concomitant symptom factors: panic-fear, awareness of airway obstruction, hyperventilation, fa- tigue, and irritability (Brooks et al., 1989; Simon et al., 1990). These secondary symptoms of asthma, including chest pain and cough, may often dominate the patients' complaints. In some patients persistent cough has been documented as the only symptom during airway obstruction (Rietveld & Rijssenbeek-Nouwens, 1998).

THE ORIGIN OF THE BREATHLESSNESS RESPONSE

The etiology of breathlessness has been associated with increased effort of respiratory muscles and changes in arterial gas levels. In a series of classic psychophysical experiments, Campbell and colleagues tested the hypothesis that breathlessness originates from afferent information from the respiratory muscles during excessive tension or labor (Campbell, Robson, & Norman, 1967). They blocked the afferent pathway with curare and observed that this significantly increased the time that the participants could hold their breath without breathlessness.

Contrary to this model, Banzett and colleagues demonstrated that afferent information from the respiratory muscles is not essential for breathlessness. They


successfully induced breathlessness by increasing the level of carbon dioxide in the gas mixture administered to paralyzed quadriplegics who fully depend on arti- ficial ventilation (Banzett, Lansing, Reid, Adams, & Brown, 1989).

Although hypoxia may also induce breathlessness, variations in oxygen levels do not play a major role in normal life (MacBugler, Roberts, & Spirer, 1993). The topic is therefore not further discussed. Nonetheless, the involvement of different mechanisms in inaccurate symptom perception remains a topic for debate (Adams, Lane, Shea, Cockcroft, & Guz, 1985; Barnes, 1992; Muers, 1993). The specificity and clarity of afferent neural information underlying breathlessness seems often lacking. Another model is required to explain breathlessness in relation to airway obstruction.

FACTORS INFLUENCING SYMPTOM PERCEPTION

As noted before, the outcome of the symptom perception process can be inaccurate in opposite directions: (a) blunted perception of airway obstruction, and (b) overperception of information, resulting in breathlessness without airway obstruction. Biomedically and psychologically orientated researchers have attempted to explain inaccurate symptom perception in asthma.

Biomedical Factors

Many investigators have attempted to explain why patients with asthma in the early classic study by Rubinfeld and Pain (1976) reported themselves symptom-free during an airway provocation test that reduced their lung function to 50%.

One explanation for this perceptual impairment can possibly be found in airway pathophysiology, associated with interference of afferent neural transfer (Burdon, Juniper, Killian, Hargreave, & Campbell, 1982). Accurate symptom perception is also thought to be influenced by chronic inflammatory processes in the asthmatic airways, associated with changes in receptor sensitivity (Wolkove et al., 1992). Such an effect is observed in patients with cystic fibrosis where excessive mucosal secretion in the airways causes a heightened threshold for cough when exposed to cough-provoking agents (Chang, Phelan, Sawyer, E1 Brocco, & Robertson, 1997).

There is no direct test of this hypothesis in patients with asthma, but the impact of pathophysiology in the perception of airway obstruction has indirectly been tested by comparing the perceptual capacity of different participant groups. The results showed that the perception of patients with asthma is indeed somewhat less accurate than that of normal controls and somewhat more accurate than that of patients with a more severe chronic obstructive pulmonary disease (Burki, Mitchel, Chaudhary, Zechman, & Campbell, 1978; Del Volgo-Mathiot & Bonnel, 1991; Ergood, Epstein, Ackerman, & Fireman, 1985; Gottfried, Altose, Kelsen, &


Cherniack, 1981; Noseda, Schmerber, Prigogine, & Yernault, 1992; Sly, Landau, & Weymouth, 1985).

Long-term asthma and environmental factors such as smoking would generally enhance airway pathophysiology (Kauffmann, Annesi, & Chwalow, 1997). Con- sequently, the expectation would be that within the asthma population the lowest perceptual accuracy exists in patients with the most severe chronic asthma. Empir- ical data confirm that perceptual accuracy in elderly asthmatics is generally dimin- ished (Marks et al., 1996; Tack, Altose, & Cherniack, 1982). However, recent experimental results suggested that young children with relatively mild asthma are as inaccurate as adults with severe asthma (Fritz, Klein, & Overholser, 1990; Montserrat et al., 1988; Rietvetd, Prins, & Kolk, 1996). In addition, several studies indicated that the accuracy of symptom perception is independent of asthma severity, lung function, airway hyperresponsiveness, and prescribed medication (Janson-Bjerklie, Ruma, Stulbarg, & Carrieri-Kohlman, 1987; Rietveld & Colland, 1999; Rietveld, Kolk, Prins, & Van Beest, 1997). The differences in perceptual accuracy over time in patients with a stable lung function further dismiss the notion that lung pathology accounts for inaccurate symptom perception in patients with asthma (Hudgel, Cooperson, & Kinsman, 1982; Wilson & Jones, 1990).

Other possible physiological explanations of inaccurate symptom perception are the locus of airway obstruction and the speed of development of asthmatic reactions (Bierman, Spiro, & Petheram, 1984). Gradually developing asthmatic reactions, like the reactions to allergens, are perceived less well than are acute reactions (Turcotte, Corbeil, & Boulet, 1990).

The perception of airway obstruction can also be influenced by symptoms often occurring concurrently with asthma, such as nasal congestion, having a cold, cough, or excessive sputum, or saliva production. The occurrence of these symptoms may often enhance the subjective experience of breathlessness, irrespective of degree of airway obstruction (Dirks & Schraa, 1983; Nishino, Tagaito, & Sakurai, 1997).

Finally, several biomedically orientated studies showed that different manip- ulations and substances causing airway obstruction do not substantially influence breathlessness (Cristiano & Schwarzstein, 1997; Marks et at., 1996; Teramoto et al., 1996). Turcotte and colleagues (1990) found no difference in breathlessness after induction of airway obstruction through physical exercise, allergens, or histamine inhalation. Preliminary results suggest that corticosteroids may have a positive effect on symptom perception, whereas sodium chromoglycate does not, although both drugs act against airway inflamma- tion (Higgs & Laszlo, 1996).

Although biomedical explanations are often plausible, there is insufficient empirical support to assume their overall explanatory potential, particularly regarding overperception of symptoms.


Psychological Factors

Three psychological factors, operating on different levels of information processing, may explain inaccurate symptom perception: (a) competition between asthmatic and nonasthmatic cues; (b) negative emotions; and (c) acquired response tendencies, including unconscious repression (denial) of symptoms, habituation (or adaptation) to symptoms, conscious neglect of symptoms, selective perception of symptoms, and false interpretation of symptoms.

Competition of Cues and the Meaning of Information

The "competition of cues" model refers to temporal limitations in sensory information processing. It is argued that the human capacity to process sensory information is limited and that the probability of noticing afferent neural information can be expressed as a function of the ratio of available internal and external information (Blitz & Dinnerstein, 1977; Pennebaker & Lightner, 1980). For instance, with an abundance of external stimulation, hardly any capacity for processing internal information remains. Cioffi (1991 ) illustrated the opposite effect by pointing to a sud- den increase in an ache or pain in the dead of night, as the house grows silent and the previously ignored internal state can easily become the focus of attention.

In chronic disease, however, learning over time may have the effect that the meaning of sensory information may determine the direction of information processing, reducing the role of a competition of cues (Fillingim & Fine, 1986). Rietveld, Kolk, Prins, et al. (1997) showed that external stimulation with short dis- tracting films enhanced the accuracy of detection of airflow interruptions. Only "false positive responses" (responses when there was no airflow interruption) were reduced. Hence, the perception of meaningful information (actual airflow interruption) remained unaffected by the competition of cues by means of films.

Consequently, the influence of the model may be important in novice patients with asthma, but once the meaning of particular information has been established in memory, the impact of the competition of cues may diminish. Selective perception and other acquired response tendencies may become more important than a competition between cues.

Negative Emotions

Although a linear relation between breathlessness and negative emotions is rarely found, breathlessness and emotional distress broadly overlap (Wilson & Jones, 1991). Clinical observations often show that negative emotions dominate the experience of asthma attacks (Isenberg, Lehrer, & Hochron, 1992; Spinhoven, Van Peski-Oosterbaan, VanderDoes, Willems, & Sterk, 1997). Approximately two thirds of asthmatic children undergo panic when they notice the onset of airway ob-


struction (Janson, Bjornsson, Hetta, & Boman, 1994). Extreme emotional arousal may often interfere with accurate symptom perception. In general, negative emotions seem to favor biased symptom perception (Hollandsworth, Kirkland, Jones, Van Norman, & Glazesky, 1979). One explanation would be that patients with asthma in a negative emotional state are inclined to evaluate ambiguous symptoms negatively, enhancing breathlessness (Costa & McCrae, 1987; Watson & Pennebaker, 1989). Dirks and Schraa (1983) suggested that negative emotions can also be interpreted by a patient as symptoms of asthma, enhancing breathlessness.

The relation between emotions and asthma can be very subtle. In a study with asthmatic adolescents, negative emotions that were induced prior to a physical exercise task had the effect that exercise-induced sensations were interpreted as though they were asthma symptoms, enhancing breathlessness (Rietveld & Prins, 1998b). Another study with asthmatic adolescents showed how complex the relation between negative emotions and asthma can be. Three adolescent girls cried from frustration and breathlessness after a mental stress task. They experienced a full-blown asthma attack. However, both the girls and the researchers were sur- prised to learn that lung function and blood gas values had not changed at all (Rietveld, Van Beest & Everaerd, 1999).

Considering that negative emotions are generally coinciding with asthma experiences, blunting of asthma symptoms could occur when negative emotions are occasionally absent during exacerbation (Rietveld & Prins, 1998b). Perceived control over symptoms and trust in medicines or medical staff are generally associated with low anxiety and low breathlessness (Pennebaker, 1982). These psychological factors would mediate in the relation between emotions and symptoms and could explain blunted perception. Indirect support for this assumption came from a study where emotions were experimentally held at baseline level by means of ran- dom presentation of intervals with different externally applied airflow interruptions. The result showed that breathlessness remained fairly constant during baseline level to severe (66%) airflow interruption (Rietveld, 1999). In other words, absence of negative emotions is associated with mild breathlessness and may thereby explain blunted perception of airway obstruction. Another assumption has been that patients with asthma inhibit emotional expressions to prevent the occurrence of emotion-induced asthma attacks (Hollaender & Florin, 1983). The secondary effect would be that asthma symptoms, coinciding with emotions, are also inhibited.

Despite the unmistaken interaction between emotions and symptom perception, careful research is required to establish the complex patterns of influence.

Acquired Response Tendencies

Patients' experience with symptoms and knowledge of asthma is structured in :ognitive schemata in memory that, beyond conscious awareness, influence subse-

RIETVELD AND BROSSCHOT 1 2 7

quent symptom perception (Lacroix, Martin, Avendano, & Goldstein, 1991). One might assume that the accuracy of symptom perception increases with the acquisi- tion of knowledge and familiarity with the symptoms of disease. However, there is no empirical support for this lay assumption. Instead, symptom perception appears to become less accurate after repeated experience with symptoms (Bishop, 1987; Pennebaker, 1982; Pennebaker & Skelton, 1981; Yellowlees & Ruffin, 1989). Re- sponse tendencies that patients acquired in the course of their living with asthma may unconsciously determine the processing of sensory information. Response tendencies may explain blunted as well as overperception of symptoms.

Repression and neglect of symptoms. Several clinical reports exist about patients who appear to have either unconsciously repressed (denied) or con- sciously neglected asthma symptoms (Steiner, Higgs, Fritz, Laszlo, & Harvey, 1987). However, despite persistent anecdotal evidence, empirical support for unconscious repression of symptoms is meager. Moreover, the attempt to differenti- ate between repression and mere inaccurate symptom perception by other causes may pose a substantial methodological problem.

It has been reported that some patients seem to be aware of airway obstruction but are simply not bothered by it (Rubinfeld & Pain, 1976, 1977; Yellowlees & Ruffin, 1989). Factors that have been mentioned as accounting for such conscious neglect of symptoms are previous experiences related to perceived control (or absence of control) over symptoms and absence of negative emotions (Avia & Kanfer, 1980; Wilson & Jones, 1990).

Habituation and adaptation to symptoms. Habituation to chronic symptoms or prolonged airway obstruction may also explain blunted symptom perception. This implies that breathlessness gradually fades away despite marked ongoing airway obstruction. Rietveld (1997) measured breathlessness in normal adolescents during short versus prolonged severe external airflow interruption. Some adolescents reported less breathlessness after prolonged interruption, which was suggestive of habituation. Other support for habituation comes from studies with substance-induced airway obstruction. Patients who already had airway obstruction before additional experimental induction of airway obstruction seemed less aware of symptoms (Burdon et al., 1982).

As an alternative explanation, patients with asthma may also have learned to re- strict physical activity during airway obstruction and thereby decrease the meta- bolic demands for oxygen, resulting in modest breathlessness in the face of potentially serious airway obstruction.

Selective perception. Other acquired response tendencies may favor overperception of symptoms. Human beings are not generally passive receivers of afferent neural information but are equipped to explain somatic events and monitor


actively and selectively for relevant information (Pennebaker, 1982; Robbins & Kirmayer, 1991). Selective perception of meaningful information is an unconscious process, although conscious attention to particular information can be very important. Selective perception has been conceptualized as an active and unconscious tendency to process specific, internal or external information with priority. There is a natural drive to associate sensory stimuli with the existing representa- tions in memory (Lacroix et al., 1991). The implication may be that ambiguous afferent information is interpreted in conformity with the expectations generated by illness schemata, resulting in false interpretation of information (Pennebaker & Skelton, 198 I). In other words, information that is merely associated with asthma, but not causally related to airway obstruction, can be interpreted as though it were airway obstruction, enhancing breathlessness. Rietveld and colleagues showed that children with asthma in a physical exercise setting reported excessive breathlessness after receiving false feedback of asthmatic wheezing sounds and negative lung-function information, suggestive of airway obstruction (Rietveld, Kolk, Colland, & Prins, 1997; Rietveld, Kolk, & Prins, 1996). In another study, induced itching did not contribute to breathlessness, but when combined with general sensations after physical exercise, itching significantly enhanced breathlessness (Rietveld, Everaerd, & Van Beest, 1999). Selective perception on the basis of learned associations between symptoms and situations may generally enhance the likelihood that pathophysiology is perceived and enhances symptom magnitude. These effects may occasionally reach the level of overperception. False interpretation of symptoms can be adaptive, in the sense that pathophysiology is early perceived, but may often favor overperception.

False interpretation of information may also favor blunted perception of airway obstruction. A 10-year-old boy with mild asthma came to the laboratory for a physical exercise task. He complained of having the flu, which was confirmed by his father, himself an asthma patient. However, testing revealed that the boy's lung function was reduced by 70% ! False interpretation of airway obstruction in terms of general symptoms or asthma-irrelevant diseases could often explain blunting, but empirical data are rare (Dirks & Schraa, 1983; Rietveld & Prins, 1998a).

CONCLUSIONS AND DISCUSSION

The perception of airway obstruction is a subjective experience. The magnitude of this experience cannot be sufficiently explained only by stimulus properties. Three main conclusions can be drawn from the preceding sections. First, afferent neural information from airway obstruction is diverse and often vague and ambiguous. These signals may be contaminated by secondary signals, and they become even more unclear in the course of disease. Second, all information regarding asthma symptoms (being highly important to survival) is extensively elaborated emotion-


ally and cognitively. Third, in many patients, these elaborations develop into fairly stable response tendencies to cope with the often ambiguous symptoms of asthma.

Although acquired response tendencies are adaptive in the sense that they facil- itate the early perception of airway obstruction, they often result in a biased perception, manifest in inaccurate blunted perception or overperception of symptoms.

There is little support for a perceptual bias caused by a competition of internal versus external cues. Negative emotions and acquired response tendencies may ac- count for overperception of symptoms. Empirical support for the influence of psychological factors in blunted symptom perception is modest.

In summary, biomedical factors are more plausible in blunted perception, and psychological factors in overperception.

Methodological Problems

The study of symptom perception is plagued by methodological difficulties. All the methods used have serious disadvantages. First, the parallel assessment of breathlessness and lung function during induced airway obstruction in the laboratory pre- cludes the possibility that participants are naive. Unfortunately, they are aware of the procedures and their effects and may act accordingly. Hence, breathlessness assessment may often be confounded by anticipation and reasoning. Moreover, the assessment of lung function involves forced breathing and is thereby confounded by motivational and emotional factors (Moran, 1991). An alternative method of studying symptom perception uses an external apparatus to interrupt airflow. This method allows the assessment of a series of stimulus-response relations, which is essential for a reliable conclusion about a participant's perceptual capacity. The major disadvantage is that forced breathing through a mouthpiece or face mask is different from an actual internal airway obstruction. The difference is likely to be reflected in respiratory and emotional variables. The third method of studying symptom perception comprises the comparison of estimated and objective mea- surement of peak expiratory flow rates. However, estimating physical performance is different from reporting breathlessness, as has been shown by Silverman and colleagues (1987).

Recent progress with in vivo assessment of spontaneous asthma symptoms is promising and may improve the external validity of symptom-perception research (Myrtek & Brugner, 1996; Rietveld & Rijssenbeek-Nouwens, 1998). Despite technical problems, these studies have the advantage that patients are measured when they are relatively naive under natural circumstances.

Improving Symptom Perception

The influence of psychological factors in inaccurate symptom perception may suggest that patients can learn to improve their perception of airway obstruction. Re-


markably, there only have been a few attempts to improve actual symptom perception in asthma. Silverman et al. (1987) successfully trained asthmatic patients to estimate their lung function better, but they were not able to get them to report breathlessness accurately during fluctuations in lung function (cf. Kendrick, Higgs, Whitfield ,& Laszlo, 1993; Reader et al., 1990). Stout, Kotses, and Creer (1993) improved symptom perception in healthy adults by means of exposure to externally applied airflow interruptions. The clinical relevance of these studies is consider- able, and further attempts with patients are warranted. There are many studies showing that symptom perception can be improved by the use of peak flow meters (Creer, 1987). Daily use of this device in the home situation would lead asthmatic patients to a proper evaluation of airway obstruction and use of medication. Unfor- tunately, most users seem to grow careless over time in the correct handling of the meter, or omit using it after some time without symptoms. Hence, prescribing a peak flow meter in the self-management of asthma requires follow-up training in the proper handling of this useful device (Higgs, Richardson, Lea, Lewis, & Laszlo, 1986).

Future Research

The clinical problems and risks associated with inaccurate symptom perception in patients with asthma warrant new research, concentrating on a multifactorial de- sign, including biomedical and psychological factors. The many factors addressed in this review should be considered in the light of their unique contribution in symptom perception. Particular attention should be given to stable response patterns that can systematically affect patients' ability to cope with asthma.

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current perspectives on symptom perception in asthma: a biomedical and psychological review

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