Frontiers review
The multiple dimensions of dyspnea: Review and hypotheses

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Abstract

Although dyspnea is a common and troubling symptom, our understanding of the neurophysiology of dyspnea is woefully incomplete. Most measurements of dyspnea treat it as a single entity. Although the multidimensional dyspnea concept has been mentioned for many decades, only recently has the concept been the subject of experimental tests. Emerging evidence has begun to favor the hypothesis that dyspnea comprises multiple dimensions or components that can be measured as different entities. Most recently, studies have begun to show that there is a separable ‘affective dimension’ (i.e. unpleasantness and emotional impact). Understanding of the multidimensional measurement of pain is far in advance of dyspnea, and has enabled progress in the neurophysiology of pain, including identification of separate neural structures subserving various elements of pain perception. We propose here a multidimensional model of dyspnea based on a state-of-the-art pain model, and review existing evidence in the light of this model.

Introduction

Dyspnea is a clinical problem nearly as important as pain, affecting a quarter of the general population and half of seriously ill patients (the latter comparable to pain's impact) (Hammond, 1964, Kroenke et al., 1990, Desbiens et al., 1997). Yet, our understanding of the neurophysiology of dyspnea is far behind our understanding of pain. More sophisticated objective measurements of the subjective sensation of pain began to emerge over three decades ago, and have aided the study of pain neurophysiology, especially of cortical mechanisms.

Over the past three decades there has been an evolving recognition of the complexity and variety of sensations of breathing discomfort, yet dyspnea is still frequently treated in research papers and textbook chapters as a single perceptual dimension. The American Thoracic Society currently defines dyspnea as “a subjective experience of breathing discomfort that consists of qualitatively distinct sensations that vary in intensity” (ATS ad hoc Committee, 1999). It is now accepted by the majority of scientists studying dyspnea mechanisms that there are different dyspneas: they differ in the quality of dyspnea experience, the stimuli that evoke them, and the afferent pathways that subserve them (reviewed below). There is growing, but less developed, evidence that there is an affective and emotional dimension of dyspnea that does not entirely depend on the sensory strength of dyspnea (reviewed below). If, indeed, there are separable dimensions of dyspnea their measurement can provide a more complete understanding of dyspnea and its neural mechanisms. More complete measurement is necessary to provide quantitative answers to several important questions: (1) How does the dyspnea experienced by normal subjects in a laboratory differ from that of patients? (2) Why does the perception of dyspnea vary so much among patients with similar disease states? (3) What determines the impact of dyspnea on behavior and quality of life of patients? (4) Will a more complete evaluation of dyspnea lead to improved diagnosis and treatment?

Although various authors have posited the idea that dyspnea has several dimensions (and it is sometimes accepted as an article of faith), no hypothetical model has been proposed and rigorously tested. Our purpose here is to present a testable model for multidimensional dyspnea, and to examine the evidence for this model available to date.

Section snippets

Pain model

Half a century ago one of the leading figures in respiratory physiology suggested using concepts of pain perception to help understand dyspnea (Comroe, 1956). Perhaps because pain is much more common in even the healthy population, and because application of precise experimental pain stimuli does not require physiological training or a great deal of time, the science of pain is far advanced over the science of dyspnea. There are many similarities that make the pain-dyspnea analogy attractive:

A multidimensional model for dyspnea?

It is, of course, always possible to propose complex models that fit the data, and that make sense (at least to the modeler). We must ask, however, whether the more complex model of dyspnea is needed: Are there situations in which the simple model fails to fit the data? Does the added complexity pay for itself in better understanding? These questions are beginning to be answered, as discussed in this section.

Importance of the affective dimension

Most of the cortical regions activated by dyspnea are limbic or paralimbic; these areas known to be important in emotion and primal behavior. Primal emotions arising from the affective component of perceptions such as hunger, thirst, and dyspnea provide the drive for complex behaviors aimed at solving homeostatic problems. The cognitive capacity needed to formulate appropriate behavioral solutions over extended time and distance has led Denton to suggest that these primal sensations are the

Some applications of multidimensional scaling

The recognition and measurement of the multiple dimensions of dyspnea may help solve several persistent problems in dyspnea research: the translation between laboratory and clinical studies, the marked individual differences in patient's experience and response to dyspnea, and the mechanisms of therapies for symptomatic relief of dyspnea.

Summary

The multiple dimension model of pain is well developed and tested and has been in common use for decades; we are only beginning to test a similar model for dyspnea. It is likely that improved measurement that can result from a better model of dyspnea will improve our ability to compare laboratory studies with clinical situations and help understand the actions of therapeutic interventions designed to relieve the symptom of dyspnea when amelioration of the underlying cause is impossible. We hope

Acknowledgements

The authors are grateful to Mark Parshall, Paula Meek, and Richard Schwartzstein for useful discussions of the underlying concepts. We thank Dan Elkin for help in preparation of the manuscript and figures. This work supported by a grant NR10006 from the National Institute of Health (Banzett) and grant DAMD 17-00-2-0018 from the Department of the Army (Gracely).

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    Supported by NIH grants HL46690 & NR10006 to R. Banzett.

    1

    Current address: Department of Endodontics, UNC School of Dentistry, Center for Neurosensory Disorders, University of North Carolina, Chapel Hill, NC 27599, USA.

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