Assessing Respiratory

D i s t res s W h e n t h e
Patient Cannot Report
Dyspnea
a,b,
Margaret L. Campbell, PhD, RN *

KEYWORDS
 Dyspnea  Assessment  Cognitive impairment
 Dying  Distress

Ensuring patient comfort begins with a comprehensive assessment for symptom

distress. The dying patient poses unique challenges for assessment because of the
high prevalence of declining and impaired cognition that typifies this population.
The focus of this paper is on the practical clinical question: How can we recognize
respiratory distress when the patient cannot provide a report about dyspnea?

DEFINITIONS

Symptoms are subjective phenomena that can be perceived and verified only by the
person experiencing them. An expert panel representing the American Thoracic
Society defined dyspnea as: a subjective experience of breathing discomfort that
consists of qualitatively distinct sensations that vary in intensity.1 Symptom distress
has been conceptualized as the need to alter actions in response to a symptom;
and the physical or mental anguish and suffering that results from the symptom.2 A
sign is any abnormality indicating disease that is detectable by the individual or by
others. Respiratory distress has been conceptualized as an observable corollary to
dyspnea relying on signs that indicate the likely presence of dyspnea.3 Respiratory
distress, for the purpose of this paper, is the physical and/or emotional suffering
that results from the experience of dyspnea and is characterized by behaviors that
can be observed and measured.

PREVALENCE OF DYSPNEA AND COGNITIVE IMPAIRMENT AT THE END OF LIFE

A systematic review of symptom prevalence studies was done to determine the extent
to which patients with chronic progressive diseases have similar symptom profiles.4

a
Center for Health Research, College of Nursing, Wayne State University, 5557 Cass Avenue,
Detroit, MI 48202, USA
b
Nursing Research, Detroit Receiving Hospital, 4201 St Antoine, Detroit, MI 48201, USA
* Nursing Research, Detroit Receiving Hospital, 4201 St Antoine, Detroit, MI 48201.

Nurs Clin N Am 45 (2010) 363–373

doi:10.1016/j.cnur.2010.03.001 nursing.theclinics.com
0029-6465/10/$ – see front matter ª 2010 Elsevier Inc. All rights reserved.
364 Campbell

The prevalence of dyspnea and confusion across the 5 common conditions is illus-
trated in Table 1.
Heart disease is the leading cause of death in the United States, with chronic pulmonary
diseases ranked fourth. Pneumonia is the fifth leading cause for persons older than 65
years.5 The World Health Organization predicts that by 2020 chronic obstructive pulmo-
nary disease (COPD) will increase from the twelfth most prevalent disease worldwide to
the fifth and from the sixth most common cause of death to the third.6 As expected, the
prevalence of dyspnea is highest among people with COPD and heart disease.
Declining or impaired cognition is also highly prevalent among terminally ill patients,
particularly those who are elderly or referred from long-term care.7,8 Likewise, hypox-
emia temporarily impairs cognition, particularly if the PaO2 is less than 50 mm Hg;9
hypercarbia produces a narcotic effect at PaCO2 levels greater than 70 mm Hg.10,11
Patients with COPD who experience chronic blood gas alterations are likely to have
mild, chronic, cognitive impairment even when their oxygenation is stable with
declines from baseline occurring when they are hypoxemic.12–15
Patients with declining or impaired cognition are vulnerable to under recognition and
over or under treatment of their distress because clinicians may lack the ability to iden-
tify signs associated with the autonomic and emotional responses. A retrospective
audit of 185 charts from 5 long-term care facilities in Canada found that half of the resi-
dents who died were cognitively impaired; dyspnea was the most common symptom
(62%) but only 23% of residents with dyspnea had it treated.7 A corresponding result
was found in a large mortality follow-back survey of family members of patients who
died in an institutional setting. Families reported that 22% of patients with dyspnea did
not receive any or enough treatment.16 More than half the terminally ill hospitalized
patients (54%) in a prospective study were unable to provide even a simple yes or
no response to the query ‘‘Are you short of breath?’’ Inability to self-report was asso-
ciated with unconsciousness, impaired cognition, and nearness to death.17
Theoretically, the same physiologic changes that induce dyspnea in the patient with
intact cognition will produce respiratory distress when the patient is experiencing
declining cognition. The only difference in the 2 patient cohorts is in their ability to reli-
ably report their distress. The prevalence of respiratory distress at the end of life is not
known because patients unable to report have been largely excluded from prevalence
estimates.

COMMON SELF-REPORT TOOLS FOR ASSESSING DYSPNEA

The simplest form of assessment for dyspnea is to ask the patient: ‘‘are you short of
breath?’’ The yes or no response does not provide any qualitative information and

Table 1
Prevalence of dyspnea and confusion across conditions

Dyspnea Number of Confusion Number

Conditions Prevalence (%) Studies N Prevalence (%) of Studies N
Cancer 10–70 21 10,029 6–93 19 9154
AIDS 11–62 2 504 30–65 2
Heart disease 60–88 6 948 18–32 3 343
COPD 90–95 4 372 18–33 2 309

Data from Solano JP, Gomes B, Higginson IJ. A comparison of symptom prevalence in far advanced
cancer, AIDS, heart disease, chronic obstructive pulmonary disease and renal disease. J Pain
Symptom Manage 2006;31(1):58–69.
 Assessing Respiratory Distress 365

cannot be used to measure the intensity of the patient’s experience, but it does give
the examiner initial information. In the case of a cognitively impaired patient the simple
yes or no response may be all the patient can provide.
More informative but unidimensional tools include a numeric rating scale (NRS) and
a visual analog scale (VAS). The VAS is typically a 100-mm line anchored at either end
with descriptors such as ‘‘no breathlessness’’ to ‘‘greatest breathlessness.’’18 The
patient marks a point on the line to represent the intensity of breathlessness, which
is thus converted to a numerical value by measuring the millimeters in length
expressed. Horizontal and vertical versions of the VAS have high correlation (r 5
0.97) and have demonstrated construct and discriminate validity and responsiveness
in therapeutic trials.18 The NRS is a 0 to 10 integer scale that may be anchored with
descriptors such as 0 5 ‘‘no shortness of breath’’ and 10 5 ‘‘shortness of breath as
bad as can be.’’ The NRS has shown concurrent validity to VAS (r 5 0.56) and
construct validity for incident or short time frame dyspnea assessments.19
Patient report is considered the gold standard for measuring symptom distress.
Consciousness is necessary for cognition and cognitive functions are necessary to
generate and report a symptom or symptom distress. The patient must be able to
interpret sensory stimuli, pay attention to instructions and concentrate to form a report,
be able to communicate in some fashion, and be able to recall the previous report if
trending is requested. When cognition is impaired, reliance on proxy assessments
may occur. Concordance with the family’s perspective about the patient’s behavior
and level of comfort can be sought. However, proxy reports about respiratory distress
when the patient is unable to provide a self-report may be less reliable than reliance on
behavioral cues.20

BEHAVIORAL ASSESSMENT

As we evolved from water-dwelling to air-breathing organisms the dyspnea response

to asphyxiation began and has persisted over millions of years.21 This primal ancient
response produces compensatory behaviors and induces basic aversive emotions,
including fear.
The following theoretical model of respiratory distress (Fig. 1) was derived from
a synthesis of animal and human studies of biobehavioral responses to an asphyxial
threat. The model relies on subcortical neurologic systems in the emotional and auto-
nomic domains that are rapidly triggered in response to a threat of asphyxia.22 These
evolutionary ancient reactions produce compensatory responses oriented to
survival.21 Conditions that produce dyspnea (inspiratory effort, hypercarbia, and
hypoxemia) trigger a near immediate autonomic and primal fear reaction that
produces an array of observable behaviors.

ASPHYXIAL THREAT

An asphyxial threat is produced when pulmonary pathology produces 1 or more of

inspiratory effort, hypoxemia, or hypercarbia. A sense of inspiratory effort is produced
by conscious awareness of voluntary activation of skeletal muscles. Muscle receptors
provide feedback about muscle force and tension and information from these chest
wall receptors produce the conscious awareness of respiratory effort. The respiratory
muscles also activate autonomic central respiratory motor centers (pons and medulla)
that can contribute to the sense of effort; effort has been strongly correlated with
breathlessness.23
Hypercarbia and hypoxemia have long been known to produce an involuntary motor
response mediated in the brainstem to increase ventilation through increased rate and
366 Campbell

Asphyxial Threat Fear Report

Hypercarbia
Hypoxemia
Inspiratory Effort
Look of Fear

Autonomic
Nervous Grunting at
Amygdala
System End-Expiration

Pulmonary Stress Behaviors Restless/Frozen

Tachycardia
Tachypnea
Accessory Muscle Use
Nasal Flaring Tachycardia
Paradoxical Breathing Tachypnea

Fig. 1. A theoretical model of respiratory distress.

volume of breathing. Hypercarbia and hypoxemia also make independent contribu-

tions to the sensation of distress.24 Generally, hypercarbia will produce dyspnea
and its associated physiologic and emotional reactions when the partial pressure of
carbon dioxide (PCO2) increases by 5–10 mm Hg from the patient’s baseline level.25
Severe hypercarbia (PCO2 >80 mm Hg) produces a narcotic effect and at very high
levels suppresses the brainstem respiratory center causing death.10 Pathologic condi-
tions that produce respiratory distress do so by more than 1 mechanism. Sense of
effort, hypoxemia, and hypercarbia, however, are common to the pathologic condi-
tions that produce respiratory distress particularly during severe exacerbations and
respiratory failure.26

AUTONOMIC NERVOUS SYSTEM ACTIVATION

Respiratory sensors consist of central (medulla, pons, and cerebellum) and peripheral
chemoreceptors (aortic and carotid bodies) and peripheral sensory receptors found in
the chest wall, airways, and lungs. Stimulation of the respiratory center elicits an
increased respiratory and cardiac response through activation of the parabrachial
complex in the pons,27,28 sympathetic nervous system, and activation of the adrenal
medullary catecholamines (epinephrine and norepinephrine). Increased cardiac and
pulmonary performance from central respiratory control and the sympathetic nervous
system produce compensatory responses including accelerations in heart and respi-
ratory rates and increased lung volumes through recruitment of thoracic and abdom-
inal accessory muscles.29 These well-understood cardiorespiratory responses and
pulmonary stress behaviors are intended to restore respiratory homeostasis and
preserve life.

FEAR ACTIVATION

Emotions are short-lived psychophysiologic phenomena representing adaptation to

changing environmental demands. The emotion system is a set of interconnected
structures including the anterior thalamus, hypothalamus, septum, amygdala,
 Assessing Respiratory Distress 367

hippocampus, cingulate cortex, and the bed of the stria terminalis.30,31 These primitive
subcortical brain areas evolved after the brainstem but before the neocortex.32
An eliciting stimulus, such as an asphyxial threat, leads to a subcortical appraisal.
An important function of any emotion is the coordination of an optimal physiologic
environment to support the behavior that is called forth. Recruitment of responses
from the central and autonomic nervous systems provides for capacity to adapt and
survive. Some emotion systems, such as fear, are so primitive that conscious aware-
ness of their activation is not necessary for response recruitment given the predomi-
nance for survival over deliberation.33
Fear is the primal emotion most often associated with respiratory disability.34–36 The
amygdala is closely associated with the ability to identify threats, and in turn activates
a fear response array. The amygdala receives input via 2 pathways: cortical
(conscious) and subcortical (unconscious). Threat stimuli are communicated by
both pathways. The most rapid communication is from the sensory thalamus to the
amygdala with no conscious perception; this produces, in animals or humans, a rapid
response to the threat that precedes conscious awareness. A slower pathway
traverses the sensory thalamus to the sensory cortex to the amygdala providing
conscious appraisal of the threat stimulus.37 Thus, patients with brain lesions that
contribute to declining or impaired cognition may have a distorted or absent
conscious appraisal of threats but retain fear responses and behaviors because threat
stimuli are communicated via the rapid thalamic pathway.
The amygdala projects to multiple brain regions controlling endocrine, autonomic,
and motor activity.38 A threat elicits an amygdaloid response that controls brainstem
nuclei underlying facial expression, startle excitability, freezing behavior, and respira-
tory and cardiovascular changes.39–42 Fear is an aversive state triggered in people and
animals when survival is threatened. It is an evolutionarily old brain response that
controls behaviors necessary for survival of the individual and ultimately survival of
the species.

FEAR ACTIVATION BY AN ASPHYXIAL THREAT

The mechanisms that produce the sensation of uncomfortable breathing also produce
the strongly correlated negative emotional responses through activation of the amyg-
dala and other central nervous system processes. Investigators using brain imaging
techniques revealed elevated and robust activation of the amygdala and other subcor-
tical structures when air hunger was induced in healthy human subjects.43–49 Asphyxia
may induce a primal, innate, unconditioned, autonomic array of pulmonary stress and
fear behaviors because the threat to survival cannot be controlled.

BEHAVIORS ASSOCIATED WITH RESPIRATORY DISTRESS

This theoretical model is composed of behaviors activated simultaneously from the

autonomic nervous system and the amygdala. The autonomic pulmonary stress
behaviors include the recruitment of accessory muscles (sternocleidomastoid, inter-
costals, abdominal) that are displayed as elevation of the clavicles and/or paradoxic
breathing, which is an inward movement of the abdomen on inspiration50–52 tachy-
cardia and tachypnea,53 and an outward flaring of the distal external nares.54,55
Subcortical elicitation of fear produces an organized response array of facial,
vocal, motor, and physiologic responses that can be observed as measurable
behaviors. Fear in response to an asphyxial threat produces a characteristic look
of fear.56 The universal fearful facial expression is characterized by (1) the upper
iris is visible, (2) the teeth are visible, (3) the teeth are not parted, (4) there are lines
368 Campbell

in the forehead, (5) the eyebrows are flat, (6) the eyebrows are raised, and (7) there
are no wrinkles in the nose (Fig. 2).57 Fear in response to asphyxia is also postu-
lated to produce grunting at end expiration,58 restlessness,59–61 or freezing,62
and fear-specific physiologic support through heightened activation of the auto-
nomic nervous system, adrenal medulla, and ventromedial pons. These evolution-
arily ancient brain areas react to the threat of asphyxiation and produce
compensatory responses oriented to the survival of the individual and ultimately
of the species. Fear has been strongly correlated with dyspnea in studies of
patients with respiratory disease.51,63–66

FEAR AND PULMONARY STRESS BEHAVIORS TO AN ASPHYXIAL THREAT

ACROSS COGNITIVE STATES

An exploratory study was conducted to test the aforementioned biobehavioral theo-

retical model of responses to an asphyxial threat. Patients undergoing a ventilator
weaning trial (n 5 12) were assessed and observed at baseline and during weaning
with a capnograph/oximeter and video camera. Cognitive state (intact, mild, or
moderately or severely impaired) was categorized at baseline, and an emotion report
was elicited after the weaning trial. Pulmonary stress and fear behaviors were similar
across cognitive states and included in order of descending frequency: tachycardia/
tachypnea, accessory muscle use, fearful facial expression, paradoxic breathing,
and nasal flaring. Hypercarbia predicted activation of fear behaviors. Gender differ-
ences characterized emotion reporting; men did not report fear. An asphyxial threat
induced an innate array of behaviors that were not volitionally controlled and had the
same appearance across cognitive states (intact, mild, or moderately impaired).66

Fig. 2. Characteristic facial expression denoting fear. (Courtesy of Ursula Hess, Professor of
Psychology, University of Quebec at Montreal.)
 Assessing Respiratory Distress 369

DEVELOPMENT AND TESTING OF A RESPIRATORY DISTRESS OBSERVATION SCALE

A Respiratory Distress Observation Scale (RDOS) was developed from the aforemen-
tioned biobehavioral models (see Appendix) and was subsequently tested for reli-
ability and convergent and discriminant validity.67 Patient reports about dyspnea
were compared with displayed respiratory distress behaviors in 3 groups of 70
patients or volunteers (n 5 210). In the first group, pulmonary rehabilitation patients
were assessed with the RDOS after controlled exercise that induced hypoxemia as
measured by oximetry. The individuals were subsequently asked to report current
dyspnea on a dyspnea visual analog scale (DVAS). In the second group, patients
with postoperative orthopedic pain were evaluated with the RDOS and asked to report
current pain (pain numeric report) and dyspnea. In the third group, healthy volunteers
were assessed with the RDOS at rest and asked to report current dyspnea. The
internal consistency (alpha) of the RDOS was 0.78 (N 5 210). A positive correlation
between the RDOS and DVAS (P<.01) and an inverse correlation between RDOS
and peripheral oxygen saturation (SpO2; P<.01) were found, indicating convergent val-
idity. Significant mean differences were found when RDOS and DVAS scores from
dyspneic patients were compared with RDOS from patients with pain (P<.01) and
with healthy volunteers (P<.01) indicating discriminant validity. Of necessity, the
RDOS was tested with study participants who were cognitively intact and able to
provide a dyspnea self-report because there is no gold standard respiratory distress
observation tool with which to test convergent validity.67 The instrument has subse-
quently been revised and has undergone additional reliability and validity testing
with terminally ill patients dying from 1 or more of the following diagnoses: pneumonia,
heart failure, COPD, and lung cancer.67 Additional testing was needed with terminally
ill patients unable to self-report.
An observational design was used with 89 consecutive patients referred for inpa-
tient palliative care consultation and at risk for dyspnea who had 1 or more of lung
cancer, COPD, heart failure, or pneumonia. Patients were observed and the RDOS
scored once each day for up to 3 days after the initial consultation. Other measures
included dyspnea self-report, neurologic diagnoses, opioid or benzodiazepine use,
peripheral oxygen saturation, end-tidal carbon dioxide level, consciousness, cognitive
state, nearness to death, and patient demographics. Perfect interrater reliability
across data collectors was achieved. No differences in RDOS scoring were found
by patient demographics. RDOS was associated with the use of oxygen (P<.01),
oxygen saturation (P<.01), and nearness to death (P<.01). A significant decrease in
RDOS was found between the initial palliative care consultation and day 2 that corre-
sponded with treatment (P<.01) and with a significant increase in opioid administration
(P<.01). The reliability of this 8-item scale is sufficient (a 5 0.64).68
Declining consciousness and/or cognition are expected when patients are near
death. The RDOS performed well when tested with terminally ill patients who were
at risk for respiratory distress, most of whom could not self-report dyspnea. The
tool was sensitive to detect changes over time and measure response to treatment.
The RDOS is simple to use; scoring takes less than 5 minutes. The RDOS has clinical
and research usefulness to measure and trend respiratory distress and response to
treatment.

SUMMARY

Standard measures of dyspnea, such as a numeric report or VAS, rely on the patient’s
self-report. Declining consciousness and/or cognitive function and nearness to death
may interfere with dyspnea reporting making the patient vulnerable to under or over
370 Campbell

treatment. The ability to give even the simplest self-report (yes or no) about dyspnea is
lost in the near death phase of terminal illness, yet the ability to experience distress
may persist and may be overlooked and under or over treated. Other methods for
symptom assessment are needed in this context.

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APPENDIX: RESPIRATORY DISTRESS OBSERVATION SCALE (RDOS)

Variable 0 Points 1 Point 2 Points Total

Heart rate (beats per <90 90–109 R110
minute)
Respiratory rate %18 19–30 >30
(breaths per minute)
Restlessness: nonpurposeful None Occasional Frequent
movements slight movements
movements
Paradoxic breathing None Present
pattern: abdomen
moves in on inspiration
Accessory muscle use: None Slight rise Pronounced
rise in clavicle during rise
inspiration
Grunting at end None Present
expiration: guttural
sound
Nasal flaring: involuntary None Present
movement of nares
Look of fear Eyes wide open,
facial muscles
tense, brow
furrowed,
mouth open,
teeth together
Total

Instruction for use:

1. RDOS is not a substitute for patient self-report if able.
2. RDOS is an adult assessment tool.
3. RDOS cannot be used when the patient is paralyzed with a neuromuscular blocking agent.
4. Count respiratory and heart rates for 1 minute; auscultate if necessary.
5. Grunting may be audible with intubated patients on auscultation.
6. Fearful facial expressions.