Patients With Erythrophobia (Fear of Blushing

Patients With Erythrophobia (Fear of Blushing) Show Abnormal Autonomic
Regulation in Mental Stress Conditions
KURT LAEDERACH-HOFMANN, MD, FMH, APPM, LUTZ MUSSGAY, PHD, BRUNO BÜCHEL, MD,
PETER WIDLER, MD, FMH, AND HEINZ RÜDDEL, MD, PHD
Objective: The objective of this study was to analyze the autonomic functions of patients with erythrophobia.
Methods: Forty patients with a diagnosis of erythrophobia (female/male ratio 18/22) without any other organic
lesions and 20 healthy volunteers (female/male ratio 10/10) were assessed. Clinical evaluation was performed using
a modified version of semistructured interviews. Autonomic testing was performed by means of spectral analysis
of heart rate and continuous blood pressure by sparse discrete Fourier transformation at rest and under mental
stress. Results: There were no significant difference between the two samples in age, sex distribution, BMI, resting
systolic, or diastolic blood pressure, nor was there a difference in autonomic baseline functioning between the 40
patients with erythrophobia and the control subjects. On the other hand, patients with erythrophobia consistently
showed higher pulse rates (88 ⫾ 20 vs. 78 ⫾ 9 bpm, p ⬍ .05), higher total heart rate power values (8.40 ⫾ 0.63 vs.
8.07 ⫾ 1.02 p ⬍ .05), higher midfrequency spectral values (7.38 ⫾ 0.66 vs. 7.02 ⫾ 1.18, p ⬍ .01), higher
high-frequency spectral values (6.89 ⫾ 0.86 vs. 6.48 ⫾ 1.44, p ⬍ .05), and lower baroreceptor sensitivity (8.62 ⫾ 8.16
vs. 11.65 ⫾ 4.42, p ⬍ .005) than the healthy subjects. ANOVA showed a significant group interaction (p ⬍ .0001)
between the samples. Conclusions: This study provides evidence for abnormal autonomic functioning in patients
with erythrophobia when under mental stress. Key words: Autonomic testing, fear of blushing (erythrophobia),
baroreflex sensitivity, spectral analysis, blood pressure, semistructured interviews
BMI ⫽ body mass index; DSM-IV ⫽ Diagnostic and
Statistical Manual of Mental Diseases, fourth edition;
ICD-10⫽ International Classification of Diseases, tenth
edition; LF/HF ratio ⫽ low frequency/high frequency
ratio; R-R interval ⫽ beat-to-beat interval in the electrocardiogram.
Erythrophobia (or facial blushing) is an interesting
clinical and psychological phenomenon and is a psychosomatic disorder. It has been associated with embarrassment in both men and women when the symptom overrides normal ranges of socially accepted
emotional expression. Especially in adulthood, fear of
blushing seems to be quite common, whereas with
growing age symptoms often disappear or lessen (1).
Blushing can become a stubborn and incapacitating
symptom that often severely restricts the patient’s social life.
Introduced as a separate diagnostic entity at the turn
of the last century, today’s diagnostic manuals of psychiatric disorders only make a slight distinction between erythrophobia and phobia (2, 3). Depending on
From the Psychosomatics and Psychosocial Medicine (K.L-H.,
B.B., P.W.), Psychiatric Out-Patient Department, University of
Berne, Switzerland, and the Center for Psychobiological and Psychosomatic Research (L.M., H.R.), University of Trier, Psychosomatic Hospital St-Franziska-Stift, Bad Kreuznach, Germany.
Address reprint requests to: K. Laederach-Hofmann, University of
Berne, Psychiatric Out-Patient Department, CH-3010 Berne-Inselspital, Switzerland. Email: [email protected]
Received for publication December 8, 2000; revision received
April 30, 2001.
358
0033-3174/02/6402-0358
Copyright © 2002 by the American Psychosomatic Society
the particular case, possible DSM-IV categories for this
syndrome might include social phobia, anxiety disorder due to a general medical condition, anxiety disorder not otherwise specified, or possibly agoraphobia
without a history of panic disorder or specific phobia
(other type). Based on the number and type of social
situations feared, DSM-IV distinguishes between the
generalized and nongeneralized (specific or distinct)
subtype, which also overlap with the presence and
absence of the Axis II diagnosis of avoidant personality
disorder. Various research groups (4 –7) have investigated the distinguishing features of these subtypes.
Although some authors consider erythrophobia or fear
of blushing as a subtype of social phobia (8), Ogawa and
Bouderlique (9) offer a psychodynamic approach. They
subclassify an “anthropophobia” disorder, including autodysmorphophobia (fear of subjectively abnormal shape
of body parts, eg, overly large nose), scopophobia (fear of
showing parts of body, eg, arms or feet), erythrophobia
(fear of blushing when in contact with others), and olfactory reference syndrome (a syndrome including the
pathological fear of dispersing abnormal odors). Stein et
al. (10) suggested classifying the olfactory reference syndrome as an obsessive-compulsive disorder. It remains
unclear whether erythrophobia might also be a form of an
obsessive-compulsive disorder as Pohlen postulated
some yeas ago (11).
Many of the patients suffering from erythrophobia
report having undergone an odyssey of therapies, measures, and interventions, including behavioral and
medical treatment, in an effort to conquer the disease
which itself may end in social avoidance behavior and
isolation (12–14). Some of the patients suffer from
concurrent cardiovascular symptoms such as palpitations, sweating, or headache, all of which may lead to
Psychosomatic Medicine 64:358 –365 (2002)
ERYTHROPHOBIA AND STRESS REACTION
the suspicion of concomitant autonomic arousal. Some
findings suggest that chronic blushing can have major
psychiatric sequelae such as depression, social anxiety
disorder, or social phobia (15–19).
Despite a reasonable body of literature in classification issues, surprisingly, literature is scarce concerning relevant clinical and pathophysiological investigations. Similarly, epidemiological studies using newer
classification systems and respective prevalence data
are lacking today. So we have to rely on existing data
which, however, might not entirely suffice for precise
criteria used nowadays (1). Most of the research conducted to date is based on a psychoanalytical approach
(8, 9, 20 –22). In one study the Rorschach test was
administered to erythrophobic subjects (23). A thorough search of medical literature only revealed case
reports on erythrophobia (24 –26) or reports on the
following intervention strategies: behavioral therapy
(27–31), pharmacological intervention (32, 33), or different surgical approaches mainly consisting of endoscopic thoracic sympathectomy (34 –38).
In addition, blushing must be distinguished from
flushing (39, 40). Drummond and Lance (41) observed
that stimulating gustatory impulses has an effect on
the autonomic nervous system in patients with unilateral lesions of the sympathetic nerves (as a result of a
variety of disorders). Interestingly, the denervated side
showed flushing, inasmuch as the intact facial part
showed both sweating and flushing. Obviously, the
cervical sympathetic outflow is involved in thermoregulatory and emotionally elicited facial sweating, flushing, and blushing—which results in the pathophysiological explanation for the success of surgical
interventions. This hypothesis was developed based
on studies conducted by Mellander et al. (42) and Buck
and Park (43). The former research group stimulated
the respective regions by transmural nerve stimulation
and norepinephrine. They concluded that beta-adrenergic neuroeffector mechanisms of the facial veins
might be involved in emotional blushing. The latter
investigators found parallels to fight-flight reactions.
The investigations of local mechanisms enabled medicine to treat these patients with beta-blocking agents
(eg, (44) and Discussion section).
However, the question as to whether and to what
extent autonomic dysfunction of the cardiovascular
system might be involved in erythrophobia or social
phobia has not been clarified to date. Although autonomic dysfunction has been studied in a variety of
diseases (eg, coronary heart disease (45, 46), diabetes
mellitus (47), as well as in psychiatric disorders such
as panic disorder (12, 14, 48), somatization disorder
(49, 50), and anxiety or antisocial behavior (51)) it has
hitherto merely been the subject of speculation in
Psychosomatic Medicine 64:358 –365 (2002)
erythrophobia (52). Panic disorder has been revealed
as one of the psychiatric disorders with important
psychosomatic health risks (48, 53, 54) similar to depression (55) or somatic diseases as diabetes mellitus
(47). The pathophysiology of these disorders involved
in early death seems to involve autonomic nervous
system dysregulation (56). There is, however, a paucity of empirical data about patients with erythrophobia despite the fact that dysfunction of the autonomic
nervous system could have similar sequelae as in
panic or anxiety disorders. Hofmann et al. (5) showed
psychophysiological differences between social phobia subtypes during a social stress task. They compared three groups of patients: 23 patients with social
phobia; 9 patients who were not afflicted with
avoidant personality disorder, and 14 who were, and
compared them with 22 normal subjects who were
assigned the task of giving a talk in public. Differences
in heart rates were discernible between the three
groups. The patients with social phobia without
avoidant personality disorder had the highest rates.
Inasmuch as no significant differences were noted in
baseline values, there were significant differences between the groups’ heart rates when preparing and giving the talk (task by group). Our study seeks to clarify
whether patients suffering from erythrophobia display
abnormalities in autonomic functioning. In addition,
differences in reactivity in response to a mental stress
condition are included to complete the picture.
PATIENTS AND METHODS
Clinical Evaluation
All patients participated in the study because of intractable and
persistent symptoms of erythrophobia. Patients suffered from erythrophobia for a period of 4 to 22 years (mean, 11 years) and reported
having tried two to seven different therapeutic approaches without
any durable success. Because there is no sufficient description of
this disorder or a definition in either of the two psychiatric classification systems [DSM-IV (3) and ICD-10 (2)], we included patients
with the following symptoms:
• blushing of face or/and neck in any situation alone or in
company (with or without subjective perception of distress),
and
• distress when even thinking about the individual key situations, and
• consequently alteration in social contacts (number, time spent)
due to facial reddening or
• increasing avoidance of situations eliciting the respective reaction (so called “phobic development”) or
• problems in social, personal, or vocational performance due to
blushing or
• feelings of shame, guilt, or no such feelings associated with
blushing.
• These items were assessed using a semistructured interview
(57, 58). In addition, the above mentioned items correspond to
the most important psychometric instruments designed by
359
K. LAEDERACH-HOFMANN et al.
Leary and Meadows (59) for assessing patients with erythrophobia. All interviews were conducted by a physician who
was familiar neither with the testing procedures used nor with
the objectives of this study. The videotaped interviews were
used to evaluate the patients’ psychological status. Four patients had signs of a developing social phobia and eight reported social contacts as the main reason for blushing. In
addition, the following items were also assessed: symptoms or
signs of the disease, extent of symptom (face, head, and neck),
concomitant sweating etc., as well as previous treatment strategies used, former diseases or illnesses, medication, personal
medical history, use of alcohol, or smoking (Table 1).
• Forty patients with erythrophobia were selected out of a sample of 62 patients. Twenty-two were excluded because of age
(⬍18 years), presence of full-blown phobic symptoms, anxiety
or obsessive-compulsive traits, medication with beta-blocking
agents or tranquilizers, or major social or vocational problems
associated with blushing. Furthermore, most of the participants reported having tried out numerous medical treatments
including behavioral therapy. No patient had undergone surgery (thoracic sympathectomy) before testing. The 40 patients
were compared with 20 age- and sex-controlled healthy subjects. Control subjects were either staff members at the hospital
or members of the investigators’ families. They were healthy,
normotensive subjects who were not on any medication.
• Exclusion criteria for both groups included the presence of any
organic disease (besides erythrophobia for the patient group),
hypertension (following the new WHO criteria (60)), peripheral or autonomic neuropathy (diagnosed clinically and neurologically), coronary heart disease, and any other psychiatric
disorders. None of these control subjects suffered from erythrophobia or had a history of blushing. Nobody in either group
was a heavy smoker (more than one pack of cigarettes per day)
or alcohol drinker (more than 40 g of alcohol per day). If they
smoked or drank alcohol moderately, they had to have discontinued doing so at least 1 day before the onset of testing.
Autonomic Testing
Testing took place in the psychophysiological laboratory of the
Unit for Psychosomatic and Psychosocial Medicine, Department of
TABLE 1.
Basic Values of Patients with Erythrophobia and
Normal Control Subjectsa
Patients
N ⫽ 40
Control
Subjects p Values
N ⫽ 20
Age (years)
32 ⫾ 9
34 ⫾ 7
22.0 ⫾ 2.6 24.0 ⫾ 2.9
BMI (kg/m2)
Sex (female/male)
18/22
10/10
Duration of disease [years, (range)]
11 (4–22)
—
Smoking habits (persons with ⬍ 1
5/35
3/17
pack/d, y/n)
Treatment approaches (N: range)
2–7
—
Social phobia (ICD-10, F40.1) (y/n)
4/36
—
Dependence of symptoms on external
8/32
—
situations (y/n)
Extent of blushing (more than face)
3/37
—
(y/n)
Anxiety symptoms (PRIME-MD) (y/n)
4/36
—
a
NS
NS
NS
PRIME-MD denotes primary care evaluation of mental disorders.
360
Endocrinology and Diabetology, University of Berne, Switzerland.
All participants were informed about the nature of the recording, the
tasks, and the different test phases. Subjects remained comfortably
seated in a reclining chair throughout the whole session and were
instructed about the testing procedures. After application and adjustment of measuring devices there was a 20-minute equilibration
phase (61) and, thereafter, baseline values were recorded for a
5-minute period. The Stroop Color-Word Test was used as a mental
stress test (62) because it is an effective means of decreasing interbeat intervals and increasing systolic blood pressure, plasma norepinephrine, and epinephrine concentration (63). It is, therefore, a
valid mental stress test that can elicit the specific reaction pattern
suggested to be of importance in patients with erythrophobia (42).
Response time and error rate served as measures of performance
level. In addition, all patients and control subjects were pressured to
give faster and more accurate answers.
An electrocardiogram was recorded using self-adhesive electrodes attached to the right and left side of the chest just below the
collar bone and below the rib cage on the left side of the body. For
determination of R-peak time (2 ms accuracy), Einthoven lead II was
used. Tonometric blood pressure was assessed continuously by a
Colin device (Colin Inc., Takeda, Japan) with a reference pressure
cuff attached to the ipsilateral arm. The tonometric device was
placed on the radial artery of the left forearm that was placed on an
armrest. To measure breathing activity, a strain gauge (ZAK Inc,
Simbach/Inn, Germany) was positioned around the chest at the level
of the xyphoid process.
Spectral analysis of heart rate variability was performed with the
CARSPAN program (64). Data acquisition was done with a sampling
frequency of 512 Hz. The program uses a sparse discrete Fourier
transformation of the succession of cardiac events. To account for
the interdependency of power values with the respective heart rate,
ie, due to varying sex or age, raw values of power spectral density
were divided by the mean heart rate of the respective experimental
phase (64). Frequency bands were defined as follows: A low-frequency component encompassed the range of 0.02 to 0.06 Hz. The
midfrequency ranged from 0.07 to 0.14 Hz. In other studies, this
frequency band is often defined as low-frequency band (61, 65, 66).
The high-frequency band covered fast fluctuations in the range of
0.15 to 0.40 Hz. Total power represents fluctuations of the whole
spectrum from 0.02 to 0.40 Hz. For later analysis midfrequency and
high-frequency bands were considered relevant. The midfrequency
band reflects a mixture of sympathetic and parasympathetic tone,
whereas the high-frequency band is mainly influenced by parasympathetic activity (66, 67). Correspondingly, continuous blood pressure was subjected to spectral analysis. Also, to assess the ratio
between parasympathetic and sympathetic activity, the LF/HF ratio
was calculated. The ratio LF/HF gives an impression of the sympathovagal balance. This ratio has been derived from reflex maneuvers
of the baroreceptor function by phenylephrine or nitroglycerin test
or by application of negative or positive pressure around the neck or
at the lower limbs or by tilting (68). It has proved to be useful in
assessing regulatory reserve and balance (67). For the respective
frequency ranges, the modulus was determined on the basis of
coherence values between systolic finger blood pressure amplitude
and heart rate variation above 0.50. Mulder (64) was able to show
that the modulus within the midfrequency band expresses the momentary increase in baroreflex sensitivity (69, 70). Several groups
have confirmed the validity of noninvasively assessed baroreflex
sensitivity compared with more traditional tests (67, 71) such as the
phenylephrine method (69). In our sample, women were investigated for autonomic functions only in the second half of their menstrual cycle (61). Patients were informed about their test results and
Psychosomatic Medicine 64:358 –365 (2002)
ERYTHROPHOBIA AND STRESS REACTION
therapy options in a follow-up consultation after completion of test
evaluation.
Data Transformation and Statistical Analysis
Values were calculated for the resting and mental stress phase,
respectively. Statistical analyses were performed with a PC-based
SAS, and StatView package (SAS Company, Los Angeles, CA). Autonomic functions were used as raw-values of the frequency transformation (sparse discrete Fourier transformation) (CARSPAN, University of Groningen, NL) and transformed by the natural logarithm
(ln)—these were used in all additional analyses. Statistical significance was set at 0.05. Descriptive statistics as well as Student’s t
tests and ␹2 tests were performed. For group comparisons, ANOVA
was used.
RESULTS
Descriptive Statistics
There were no differences between patients and
control subjects in age [32 ⫾ 9 years (mean ⫾ SD) for
patients, and 34 ⫾ 7 for control subjects (p ⫽ NS)], sex
distribution [female/male quotient 18/22 for patients,
and 10/10 for healthy subjects (p ⫽ NS)], body mass
index (BMI) [22.0 ⫾ 2.6 kg/m2 for patients, and 24.0 ⫾
2.9 kg/m2 for control subjects (p ⫽ NS)], alcohol intake, and smoking.
Hemodynamic pattern. In resting conditions, systolic blood pressure did not significantly differ between groups. However, significantly shorter interbeat
intervals were found in patients than in controls (p ⬍
.05) denoting a higher heart rate. No other hemodynamic or spectral differences were found between patients with erythrophobia and normal control subjects
in resting conditions. However, in mental stress conditions patients with erythrophobia showed significantly shorter interbeat intervals (p ⬍ .005), and, consequently a higher heart rate (p ⬍ .05). Breathing
patterns and respiration rates were not significantly
different in either resting conditions or mental stress
tasks between patients and normal control subjects.
ANOVA revealed that the transformed spectral values of patients with erythrophobia and control subjects in resting conditions were not significantly different. For mental stress conditions patients and
normal control subjects showed different values in
total power heart rate spectra (p ⬍ .05), midfrequency
band (p ⬍ .005), and high-frequency band (p ⬍ .05).
Baroreflex sensitivity did not, however, reach the significance level (p ⫽ .19) neither in resting nor in mental stress conditions, although a tendency to lower
values was obvious in patients with erythrophobia.
The quotients of low frequency to high-frequency values, reflecting the sympathetic/parasympathetic balance were 1.15 for patients with erythrophobia, and
0.94 for normal subjects (p ⫽ NS) in resting conditions,
and 1.95 vs. 2.21 (p ⫽ NS) for patients and control
subjects, respectively, in mental stress conditions. In-
TABLE 2. Hemodynamic and Spectral Values (all Transformed By the Natural Logarithm {ln}) of Patients With Erythrophobia and
Normal Control Subjects in Resting and Mental Stress Conditions (p Values of ANOVA Testing for Repeated Measures)
Resting Condition
BP systolic (mm Hg)
BP diastolic (mm Hg)
Heart rate (bpm)
Interbeat intervals (ms)
Respiration frequency (Hz)
Total power heart rate (ln ms2)
Mid-frequency Power HR (ln ms2)
High-frequency Power HR (ln ms2)
LF/HF quotient (native spectra)
Baroreflex sensitivity (ms/mm Hg)
Mental Stress Testing
BP systolic
BP diastolic
Heart rate
Interbeat intervals (ms)
Respiration frequency (Hz)
Total power heart rate
Mid-frequency power HR
High-frequency power HR
LF/HF quotient (native spectra)
Baroreflex sensitivity (ms/mm Hg)
Psychosomatic Medicine 64:358 –365 (2002)
Patients
N ⫽ 40
Control Subjects
N ⫽ 20
p
Values
124 ⫾ 15
69 ⫾ 9
71 ⫾ 9
832 ⫾ 114
23 ⫾ 6
7.85 ⫾ 0.83
6.58 ⫾ 0.98
6.83 ⫾ 0.96
1.15 ⫾ 1.17
11.69 ⫾ 8.88
124 ⫾ 14
76 ⫾ 12
66 ⫾ 7
905 ⫾ 94
27 ⫾ 6
7.84 ⫾ 0.77
6.61 ⫾ 0.90
6.89 ⫾ 0.86
0.94 ⫾ 0.64
17.33 ⫾ 4.92
.702
.528
.072
.016
.073
.964
.908
.802
.460
.192
140 ⫾ 24
81 ⫾ 14
86 ⫾ 21
671 ⫾ 108
17 ⫾ 5
8.40 ⫾ 0.63
7.38 ⫾ 0.66
6.88 ⫾ 0.93
1.95 ⫾ 1.05
8.62 ⫾ 8.16
139 ⫾ 22
79 ⫾ 13
78 ⫾ 9
760 ⫾ 43
30 ⫾ 8
8.07 ⫾ 1.02
7.02 ⫾ 1.08
6.45 ⫾ 1.44
2.21 ⫾ 1.27
11.65 ⫾ 4.42
.907
.672
.046
.002
.072
.024
.019
.014
.421
.004
361
K. LAEDERACH-HOFMANN et al.
terbeat intervals as a measure of acceleration of heart
frequency revealed similar changes from resting to
mental stress testing in patients as in healthy subjects
(Table 2 and Figure 1).
The analysis of performance data revealed comparable complete response times of 1.21 ⫾ 0.07 sec for
patients and 1.19 ⫾ 0.05 sec for the control sample (p
⫽ .82). At the same time, no differences between
women and men were found and no significant difference in variance testing was discernible despite a visibly broader variance in men than in women, especially in the group of patients (Figure 2). In addition,
the number of correct answers (correct answers per
second) was similar in the patient (0.83 ⫾ 0.03) and
the healthy group of subjects (0.89 ⫾ 0.03), p ⫽ .43. For
all the above mentioned results, significant gender differences were not discernible.
Reactivity. By using ANOVA for repeated measures
with experimental groups as between conditions (resting, mental stress) and frequency bands as within factors, heart rate spectral values in mental stress conditions showed a significant interaction in total,
midfrequency, and high-frequency bands (all p ⬍ .001)
in that patients with erythrophobia revealed a less
marked reduction in heart rate variability than control
subjects (Figure 3).
In conclusion, patients with erythrophobia do not
seem to be able to reduce sympathetic and parasympathetic tone to comparable values as normal subjects
do or up-regulate it as an effect of a more pronounced
counterregulation in mental stress conditions. This
finding is in line with the hypotheses of Mellander et
al. (42).
DISCUSSION
Conducting autonomic tests with patients suffering
from long-standing erythrophobia [mean 11 years
(range 4 –22)] revealed interesting insights into autonomic regulation in these patients in comparison with
healthy subjects. The two samples did not show any
differences in age, sex, BMI, or systolic blood pressure.
In resting conditions, patients with erythrophobia
showed no significant differences in heart rate spectra
compared with the normal control subjects. During
mental stress testing patients with erythrophobia
showed significantly higher power values of total,
midfrequency, and high frequency spectra of heart rate
compared with control subjects indicating a significantly higher sympathetic and parasympathetic tone
in patients compared with normals. However, baroreflex sensitivity was not different to normal control
subjects. All the values of the patients were still within
normal ranges as described by the Task Force of the
362
Fig. 1.
Changes in interbeat intervals (ms) of patients with erythrophobia and normal control subjects from resting to mental
stress. Solid lines represent patients (N ⫽ 40), dotted lines
denote control subjects (N ⫽ 20).
Fig. 2.
Box plots of performance statistics of patients (N ⫽ 40) and
normal control subjects (N ⫽ 20) in mental stress testing
(Stroop-test) split by sex; f ⫽ females, m ⫽ males.
European Society of Cardiology and the North American Society of Pacing and Electrophysiology (67).
One important finding of our study with patients
suffering from erythrophobia is that these patients
seem to have alterations of the heart rate variability
profile compared with normal control subjects. All of
the patients had a significantly higher heart rate together with higher power spectral activity during mental stress than the healthy control subjects. This is
consistently true for total, midfrequency, and highfrequency spectra. Higher heart rate should be associated with lower heart rate variability, visible in lower
power spectral activity (66, 67, 72). This is, however,
exactly the opposite in patients with erythrophobia.
These patients have higher spectral activities during
mental stress than normal control subjects despite a
similar shortening of interbeat intervals. Patients with
erythrophobia might presumably have higher parasympathetic influences (represented in higher highfrequency values) to heart rate variation than do normal volunteers (73) together with higher sympathetic
activity. This is, however, only true of mental stress
conditions, whereas no difference is visible between
patients with erythrophobia and healthy control sub-
Psychosomatic Medicine 64:358 –365 (2002)
ERYTHROPHOBIA AND STRESS REACTION
described in a proportion of somatization or panic
disorder (13, 48, 50). The comparison of these findings
with patients suffering from blood phobia displayed
an opposite pattern. In a population of patients with
mitral valve prolapse, Kochiadakis et al. found a significant deviation in autonomic nervous system tone
with predominance of the sympathetic division. This
predominance was more marked in symptomatic patients. In a similar setting, Hofmann et al. (5) found
differences in heart rate analyses in various subgroups
of patients suffering from panic disease. Another
group (51) investigated spectral differences in male
adolescents with anxiety or antisocial behavior and
discerned a disruption of parasympathetic coherence
to heart rate changes in patients with antisocial and
sociophobic behavior. Parasympathetic and sympathetic activity (reflected by the midfrequency band) in
patients with erythrophobia is higher than in the control group under mental stress conditions. This suggests more active parasympathetic counterregulation
in patients with erythrophobia than in normal control
subjects—a fact which was speculated about by Mellander et al. (42) nearly 20 years ago. Thus, our findings discerned a marked difference in the reaction
pattern to mental stress; patients with erythrophobia
show altered autonomic regulation as opposed to normal control subjects.
Limitations
Fig. 3.
Group comparison of patients with erythrophobia and normal control subjects in resting and mental stress conditions.
Significant ANOVA effects for total power (p ⬍ .01), midfrequency (p ⬍ .05), and high-frequency (p ⬍ .001), top,
middle, and bottom, respectively. Units are arbitrary ln
power units (ln ms2), solid lines represent patients with
erythrophobia (N ⫽ 40), dotted lines denote control patients
(N ⫽ 20).
jects in resting conditions. Possible mechanisms for
this phenomenon may lie in altered sinus node susceptibility or a different breathing pattern of patients
compared with normal control subjects. The latter can
be excluded by the analysis of breathing frequency that
did not reveal any significant differences despite
slightly lower values in patients.
However, patients with erythrophobia are not characterized by altered baroreflex sensitivity as has been
Psychosomatic Medicine 64:358 –365 (2002)
Being the first study of autonomic functioning in
patients with erythrophobia compared with normal
control subjects, several limitations have to be discussed. First of all, the patients investigated may represent a sub-sample of patients with a severe form of
this disorder because they had a persistent history of
erythrophobia and had been referred to a specialized
medical unit at a University Hospital Center. In addition, the healthy volunteers recruited were either hospital staff members or related to the investigators. This
might have created a certain bias in that staff members
(who made up about one third of the healthy volunteers) might have been more familiar with the investigating procedure than the participating patients were.
However, the same argumentation need not apply to
the participating subjects who were related to the investigators because the latter were as unfamiliar with
testing procedures in a clinical setting as the patients.
We looked for possible differences in resting values
and mental stress values of autonomic function but
could not find any significant ones.
Different breathing patterns must be taken into account in possibly producing some of the differences
(presumably in high-frequency bands). In our study,
363
K. LAEDERACH-HOFMANN et al.
the values of breathing frequencies were, however, not
significantly different between patients with blushing
and normal control subjects.
Clinical Implications and Concluding Remarks
Erythrophobia is a frequent symptom in adolescents, which diminishes over time. Only few of the
patients suffering from this disorder may seek help
because they often consider it as a stigma and are often
told by their family physicians that there is no cure for
it. In addition, erythrophobia is generally treated as a
medical banality and no serious efforts are made to
treat it. Many of our patients, most of whom have
suffered for years, reported a history of multiple treatment failures. Based on this first study of the autonomic nervous system in patients suffering from erythrophobia, we demonstrated the presence of an
abnormal autonomic reaction to mental stress. Nevertheless, the question as to whether these findings are
an epiphenomenon or rather a cause of blushing has
yet to be answered. Therapy might, therefore, focus
either on improving coping strategies or reversing this
disease by means of medical or surgical measures.
REFERENCES
1. Abe K, Suzuki T. Prevalence of some symptoms in adolescence
and maturity: social phobias, anxiety symptoms, episodic illusions and idea of reference. Psychopathology 1986;19:200 –5.
2. World Health Organization. Pocket book to ICD-10 classification
of mental and behavioural disorders. New York: Churchill
Livingstone; 1994.
3. American Psychiatric Association. DSM-IV. Washington DC:
APA; 1994.
4. Heimberg R, Hope D, Dogde C, Becker R. DSM-III-R subtypes of
social phobia. Comparisons of generalized social phobics and
public speaking phobics. J Nerv Ment Dis 1990;178:172–9.
5. Hofmann S, Newman M, Ehlers A, Roth W. Psychophysiological
differences between subgroups of social phobia. J Abnorm Psychol 1995;104:224 –31.
6. Stein M. Neurobiological perspectives on social phobia: form
affiliation to zoology. Biol Psychiatry 1998;44:1277– 85.
7. Turner S, Beidel D, Townsley R. Social phobia: a comparison of
specific and generalized subtypes and avoidant personality disorder. J Abnorm Psychol 1992;101:326 –31.
8. Pollentier S. How erythrophobia became social phobia. An overview of the clinical-diagnostic topics. Nervenarzt 1992;63:
28 –33.
9. Ogawa T, Bouderlique J. Anthropophobia: psychopathological
approach to the interactions between body, inter-subjectivity
and language. Jpn J Psychiatry Neurol 1994;48:527–32.
10. Stein D, Le Roux L, Bouwer C, van Heerden B. Is olfactory
reference syndrome on the obsessive-compulsive spectrum?
Two cases and a discussion. J Neuropsychiatry Clin Neurosci
1998;10:96 –9.
11. Pohlen M. [A blushing psychoses. The structural relationship
between erythrophobia and observation-persecution delusions.]
Z Psychosom Med Psychoanal 1970;16:53–79.
364
12. Friedman BH, Thayer JF. Anxiety and autonomic flexibility: a
cardiovascular approach. Biol Psychol 1998;49:303–23.
13. Friedman BH, Thayer JF, Borkovec TD, Tyrrell RA, Johnson BH,
Columbo R. Autonomic characteristics of nonclinical panic and
blood phobia. Biol Psychiatry 1993;34:298 –310.
14. Buller R, Maier W, Heuser I, Frommberger U. Panic attacks and
avoidance behavior. Psychiatr Praxis 1990;17:41– 6.
15. Edelmann RJ. Correlates of chronic blushing. Br J Clin Psychol
1991;30:177– 8.
16. Ballenger JC. Recognizing, the patient with social anxiety disorder. Int Clin Psychopharmacol 2000;15 Suppl 1:S1–5.
17. Stein DJ, Bouwer C. Blushing and social phobia: a neuroethological speculation. Med Hypotheses 1997;49:101– 8.
18. Leary MR, Britt TW, Cutlip WDd, Templeton JL. Social blushing. Psychol Bull 1992;112:446 – 60.
19. Greist JH. The diagnosis of social phobia. J Clin Psychiatry
1995;56:5–12.
20. Dosuzkov T. Idosophobia: a form of pregenital conversion. Psychoanal Q 1975;44:253– 65.
21. Gerbaulet L. Psychodynamic factors in erythrophobia. Z Psychosom Med Psychoanal 1972;18:116 –30.
22. Karch FE. Blushing. Psychoanal Rev 1971;58:37–50.
23. Gonzalez de Chavez M, Orbe Garay I, Rodriguez Gorostiza I.
Results of the Rorschach test in erythrophobia. Actas Luso Esp
Neurol Psiquiatr 1968;27:525–32.
24. Gersholowitz P. A case of erythrophobia. S Afr Med J 1978;53:
880.
25. Dosuzkov T. 2 cases of erythrophobia (analysis of their differences). Evol Psychiatr (Paris) 1967;32:427– 48.
26. Polheim RW. The nature of erythrophobia. Psychother Psychosom 1966;14:32– 49.
27. Scholing A, Emmelkamp PM. Treatment of fear of blushing,
sweating, or trembling. Results at long-term follow-up. Behav
Modif 1996;20:338 –56.
28. Scholing A, Emmelkamp PM. Cognitive and behavioural treatments of fear of blushing, sweating or trembling. Behav Res Ther
1993;31:155–70.
29. Mersch PP, Hildebrand M, Lavy EH, Wessel I, van Hout WJ.
Somatic symptoms in social phobia: a treatment method based
on rational emotive therapy and paradoxical interventions. J
Behav Ther Exp Psychiatry 1992;23:199 –211.
30. Lamontagne Y. Treatment of erythrophobia by paradoxical intention. J Nerv Ment Dis 1978;166:304 – 6.
31. Welsh DK. Hypnotic control of blushing: a case study. Am J Clin
Hypn 1978;20:213– 6.
32. Jefferson JW. Social phobia: everyone’s disorder? J Clin Psychiatry 1996;57:28 –32.
33. van der Meer C. Pharmacotherapy of “idiopathic” excessive
blushing and hyperhidrosis. Acta Neurochir 1985;74:151–2.
34. Telaranta T. Treatment of social phobia by endoscopic thoracic
sympathicotomy. Eur J Surg Suppl 1998;580:27–32.
35. Claes G, Drott C, Dalman P, Rex L, Gothberg G, Fahlen T.
Treatment of facial blushing with endoscopic thoracal sympathicotomy. 85 per cent of patients are satisfied, but there are
adverse effects. Lakartidningen 1998;95:3660 –2.
36. Yilmaz EN, Dur AH, Cuesta MA, Rauwerda JA. Endoscopic
versus transaxillary thoracic sympathectomy for primary axillary and palmar hyperhidrosis and/or facial blushing: 5-yearexperience. Eur J Cardiothorac Surg 1996;10:168 –72.
37. Wittmoser R. Treatment of sweating and blushing by endoscopic
surgery. Acta Neurochir 1985;74:153– 4.
38. Julius AJ, van Mourik JC. Transaxillary thoracic sympathectomy
for the treatment of primary hyperhidrosis and rubeosis. Ned
Tijdschr Geneeskd 1985;129:1042–5.
Psychosomatic Medicine 64:358 –365 (2002)
ERYTHROPHOBIA AND STRESS REACTION
39. Ginsburg J, O’Reilly B. Are blushes the same as flushes? [abstract]. Clin Sci 1987;72:184.
40. Wilkin JK. Letter. Facial flushing is not blushing. N Engl J Med
1976;294:116 –7.
41. Drummond PD, Lance JW. Facial flushing and sweating mediated by the sympathetic nervous system. Brain 1987;110:
793– 803.
42. Mellander S, Andersson PO, Afzelius LE, Hellstrand P. Neural
beta-adrenergic dilatation of the facial vein in man. Possible
mechanism in emotional blushing. Acta Physiol Scand 1982;
114:393–9.
43. Buck RW, Parke RD. Behavioral and physiological response to
the presence of a friendly or neutral person in two types of
stressful situations. J Pers Soc Psychol 1972;24:143–53.
44. Drummond PD. The effect of adrenergic blockade on blushing
and facial flushing. Psychophysiology 1997;34:163– 8.
45. Kaufmann PG, McMahon RP, Becker LC, Bertolet B, Bonsall R,
Chaitman B, Cohen JD, Forman S, Goldberg AD, Freedland K,
Ketterer MW, Krantz DS, Pepine CJ, Raczynski J, Stone PH,
Taylor H, Knatterud GL, Sheps DS. The Psychophysiological
Investigations of Myocardial Ischemia (PIMI) study: objective,
methods, and variability of measures. Psychosom Med 1998;60:
56 – 63.
46. Zorin AV, Noeva EA, Khaspekova NB, Fedorova VI, Oknin V,
Shchennikov AV. Defects in autonomic regulation in myocardial ischemia. Ter Arkh 1999;71:57– 61.
47. O’Brien I, McFadden J, Corrall R. The influence of autonomic
neuropathy on mortality in insulin-dependent diabetes. Q J Med
1991;290:495–502.
48. Yeragani VK, Sobolewski E, Igel G, Johnson C, Jampala VC, Kay
J, Hillman N, Yeragani S, Vempati S. Decreased heart-period
variability in patients with panic disorder: a study of Holter ECG
records. Psychiatry Res 1998;78:89 –99.
49. Rief W, Shaw R, Fichter MM. Elevated levels of psychophysiological arousal and cortisol in patients with somatization syndrome. Psychosom Med 1998;60:198 –203.
50. Laederach-Hofmann K, Mussgay L, Wilde T, Rüddel H. Does
autonomic neuropathy contribute to the symptom pattern in
somatization disorder? Psychother Psychosom Med Psychol
2001;51:1–7.
51. Mezzacappa E, Tremblay RE, Kindlon D, Saul JP, Arseneault L,
Seguin J, Pihl RO, Earls F. Anxiety, antisocial behavior, and
heart rate regulation in adolescent males. J Child Psychol Psychiatry 1997;38:457– 69.
52. Cutlip I, Leary M. Anatomical and physiological bases of social
blushing: speculations from neurology and psychology. Behav
Neurol 1993;6:181–5.
53. Piccirillo G, Elvira S, Bucca C, Viola E, Cacciafesta M, Marigliano V. Abnormal passive head-up tilt test in subjects with symptoms of anxiety power spectral analysis study of heart rate and
blood pressure. Int J Cardiol 1997;60:121–31.
54. Graesbeck A, Rorsman B, Hagnell O, Isberg P. Mortality of anxiety syndromes in a normal population. The Lundby Study.
Neuropsychobiology 1996;33:118 –126.
55. Watkins LL, Grossman P. Association of depressive symptoms
with reduced baroreflex cardiac control in coronary artery disease. Am Heart J 1999;137:453–7.
56. Piccirillo G, Viola E, Bucca C, Santagada E, Raganato P, Tondo
Psychosomatic Medicine 64:358 –365 (2002)
57.
58.
59.
60.
61.
62.
63.
64.
65.
66.
67.
68.
69.
70.
71.
72.
73.
74.
A, Lucchetti D, Nocco M, Marigliano V. QT interval dispersion
and autonomic modulation in subjects with anxiety. J Lab Clin
Med 1999;133:461– 8.
Morgan C, Engel G. Interviewing the patient. Philadelphia:
Saunders; 1974.
Kernberg O. The semistructured psychoanalytical interview.
Psychiatr Clin North Am 1981;4:169 –95.
Leary M, Meadows S. Predictors, elicitors, and concomitants of
social blushing. J Pers Soc Psychol 1991;60:254 –262.
1999 World Health Organization—International Society of Hypertension Guidelines for the Management of Hypertension.
Guidelines Subcommittee. J Hypertens 1999;17:151– 83.
Sato N, Miyake S, Akatsu J, Kumashiro M. Power spectral analysis of heart rate variability in healthy young women during the
normal menstrual cycle. Psychosom Med 1995;57:331–5.
Tulen JH, Moleman P, van Steenis HG, Boomsma F. Characterization of stress reactions to the Stroop Color Word Test. Pharmacol Biochem Behav 1989;32:9 –15.
Hoshikawa Y, Yamamoto Y. Effects of Stroop color-word conflict test on the autonomic nervous system responses. Am J
Physiol 1997;272:H1113–21.
Mulder L. Assessment of cardiovascular reactivity by means
of spectral analysis. Rijksuniversiteit Groningen, Universiteitsdruckerij, 1988.
Ramaekers D, Ector H, Aubert A, Rubens A, Van de Werf F.
Heart rate variability and heart rate in healthy volunteers. Is the
female autonomic nervous system cardioprotective? Eur Heart J
1998;19:1334 – 41.
Berntson G, Bigger JJ, Eckberg D, Grossman P, Kaufmann P,
Malik M, Nagarja H, Porges S, Saul J, Stone P, von der Molen M.
Heart rate variability: origins, methods, and interpretative caveats. Psychophysiology 1997;34:623– 48.
Task Force of the European Society of Cardiology and the North
American Society of Pacing and Electrophysiology. Heart rate
variability. Standards of measurement, physiological interpretation, and clinical use. Eur Heart J 1996;17:354 – 81.
Presciuttini B, Duprez D, De Buyzere M, Clement DL. How to
study sympatho-vagal balance in arterial hypertension and the
effect of antihypertensive drugs? Acta Cardiol 1998;53:143–52.
Robbe HW, Mulder LJ, Rüddel H, Langewitz WA, Veldman JB,
Mulder G. Assessment of baroreceptor reflex sensitivity by
means of spectral analysis. Hypertension 1987;10:538 – 43.
Honzikova N, Fiser B, Honzik J. Noninvasive determination of
baroreflex sensitivity in man by means of spectral analysis.
Physiol Res 1992;41:31–7.
Ewing D. Cardiovascular reflexes and autonomic neuropathy.
Clin Sci 1978;55:321–7.
Goldberger JJ, Ahmed MW, Parker MA, Kadish AH. Dissociation
of heart rate variability from parasympathetic tone. Am J Physiol
1994;266:H2152–7.
Hayano J, Mukai S, Sakakibara M, Okada A, Takata K, Fujinami
T. Effects of respiratory interval on vagal modulation of heart
rate. Am J Physiol 1994;267:H33– 40.
Kochadiakis GE, Parthenakis FI, Zuridakis E, Rombola A, Chrysostomakis S, Vardas P. Is there increased sympathetic activity
in patients with mitral valve prolapse? Pacing Clin Electrophysiol 1996;19:1872– 6.
365