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Cold face test in the assessment of trigeminal-brainstem- vagal function in humans.

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Cold Face Test in the Assessment
of Trigeminal-Brainstem-Vagal
Function in Humans
Ramesh K. Khurana, M D , Sadakiyo Watabiki, M D , J. R. Hebel, PhD,
Rodrigo Toro, M D , and Erland Nelson, M D , P h D
~
~~
Study of the reflex heart rate response in humans to apneic facial immersion (simulated diving) and its modifications
showed that bradycardia caused by simple application of cold compresses to the face (cold face test) correlated well
with that produced by the simulated diving reflex. Bilateral application of cold stimulus to the individual divisions
of the trigeminal nerve revealed the ophthalmic division to be the most sensitive pathway for this reflex. The cold
face test was standardized in 50 normal individuals and further validated in 10 patients by comparison with the
simulated diving reflex, the Valsalva maneuver, and administration of atropine. Patients with diabetes mellitus,
brainstem stroke, multiple sclerosis, or Shy-Drager syndrome developed less than normal bradycardia or minimal
tachycardia in response to the cold facial stimulus. The cold face test is a novel, simple, safe, and economical test of
the integrity of trigeminal-brainstem-vagal reflex pathways, can be utilized practically to assess vagal and brainstem dysfunctions, and has the special advantage of being applicable even in an uncooperative or comatose patient.
Khurana RK. Watabiki S, Hebel JR, et
al:
Cold face test in the assessmerit of trigeminal-brainstem-vagal
function in humans. Ann Neurol 7:144-149, 1980
T h e diving reflex is present in both animals and humans. Systematic studies of diving in vertebrates
were first reported by Paul Bert almost a century ago
[2]. Laurence Irving provided what is probably the
first electrocardiographic documentation of bradycardia in porpoises and humans during apneic underwater dives [9, 191. Autonomic effects evoked
by submersion in water include bradycardia, selective
vasoconstriction of the skin and viscera, diminished
cardiac output, and well-maintained blood pressure
[2]. In humans, immersion of the face alone produces
similar physiological changes [22], and this effect has
been called the simulated diving reflex (SDR). Wildenthal and his colleagues [28] have recently employed the S D R to correct paroxysmal atrial tachycardia by increasing vagal activity.
Because of our interest in autonomic function, we
explored the potential of the SDR in clinical assessment of trigeminal-brainstem-vagal function. However, it soon became apparent that most volunteers
had difficulty in holding their breath underwater for
more than 15 seconds. In o u r attempt to modify the
SDR and to devise a safe bedside test for patients
who might be uncooperative or unconscious, we
found that simple application of cold to the face (cold
face test, or CFT) reproduced the characteristic heart
rate and blood pressure changes of the SDR. T h e
CFT was validated against the SDR in normal volunteers and then utilized to assess trigeminalbrainstem-vagal function in patients with diabetic
autonomic dysfunction, brainstem stroke, multiple
sclerosis, o r Shy-Drager syndrome. T h e response of
the patients with diabetic autonomic neuropathy or
Shy-Drager syndrome to the CFT was compared with
other tests of parasympathetic function.
From the Departments of Neurology and of Social and Preventive
Medicine, University of Maryland School of Medicine, Baltimore,
Address reprint requests to Dr Khurana, Department of Neurology, University of Maryland, 22 S Green St, Baltimore, MD
MD.
21201.
Methods
Various modifications of the SDR were investigated with
the assistance of 33 volunteers in order to devise, evaluate,
and standardize a simple and reproducible bedside version
of the SDR, the CFT. Fourteen of the 33 volunteers were
also tested to compare the heart rate responses to application of cold to the face in the ophthalmic, maxillary, and
mandibular divisions of the trigeminal nerve. An additional
17 older volunteers were added to investigate the relationship of the CFT to age. The ages of these 50 volunteers
ranged from 19 to 85 with a mean of 33 years. Finally, 19
patients with clinically intact trigeminal nerve function but
with evidence of involvement of the brainstem or vagal
nerve (or both) were studied to assess the effects of suspected central or efferent lesions on the CFT. The CFT was
Accepted for publication June 24, 1079.
144
0364-5 134/8O/020144-06$01.25@ 1979 by Ramesh K. Khurana
validated against the SDR, the Valsalva maneuver, and an
atropine test in 10 of these patients.
Medical and ethical aspects of the study were approved
by the Human Volunteers Research Committee of the
University of Maryland School of Medicine. Procedures
were carried out with the informed consent of each participant. All control subjects were healthy, untrained volunteers. The subjects were familiarized with the equipment
and nature of the procedure. Heart rate and blood pressure
were monitored noninvasively by a heart rate monitor and
a sphygmomanometer. Cardiac rhythm was observed by
simultaneous electrocardiography. Reusable Therma-Kool
compresses (Nortech Laboratories, North Bellmore, NY
11710) provided the cold stimulus (1" to 2°C) over the
face. These compresses remain flexible even at freezing
temperatures and adapt easily to the facial contour,
thereby providing better contact with the skin. For the Valsalva maneuver, a mouthpiece attached by connective tubing to a mercury manometer quantitated expiratory pressure. A needle placed in the tubing permitted a small leak
during the expiratory strain and thereby prevented the
subject from maintaining intraoral pressure with the cheek
muscles [18].
W e decided to utilize change in heart rate as an index of
vagal function. Bradycardia is the best documented and
most easily quantitated of the normal circulatory adjustments following the diving reflex and its modifications
(SDR and CFT). Control values for cardiac rate and rhythm
were recorded with the subjects resting quietly prior to any
test maneuver. To adjust for basal differences, the results
were recorded as percentage of basal heart rate. An interval
of 5 minutes o r more was provided between tests to allow
blood pressure and pulse rate to return to baseline values.
At the onset of ventricular arrhythmias, stimulation was
immediately terminated. Heart rate and rhythm were recorded during the following stimuli:
1. Midinspiratory apnea only-the
2.
3.
4.
5.
subject, in supine position, executed a breath hold in midinspiration for as
long as possible up to 45 seconds o r more.
Cold compresses (CFT) only-Therma-Kool
compresses (1" to 2°C) were applied over the entire face of
the supine subject for a period of 1 minute. Ocular
pressure was avoided to prevent the oculocardiac reflex.
Combined CFT and midinspiratory apnea-cold compresses were placed o n the face, and the subject then
held breath in midinspiration for as long as possible up
to 45 seconds or more.
Combined SDR and midinspiratory apnea-on signal,
the prone subject, holding breath in midinspiration,
lowered his or her face u p to the ears in ice water (2" to
4"C), continuing for as long as tolerated up to 35 seconds. On signal to terminate submersion, the individual
lifted the face up while remaining in a prone position.
Additional procedures-in 14 volunteers the cold compresses (1" to 2°C) were selectively applied bilaterally
Table I . Clinical Details on I0 Patients Investigated
Patient No.,
Sex, and
Age (yr)
1. M, 34
2. M, 49
3 . M, 53
4 . M, 53
5. M, 54
6 . F, 43
7 . F, 56
8. M, 56
Diagnosis
Diabetes
mellitus
Diabetes
mellitus
Diabetes
mellitus
Diabetes
mellitus
Diabetes
mellitus
Diabetes
mellitus
Diabetes
mellitus
Sh y-Drager
syndrome
7. M, 68
Sh y-Drager
syndrome
10. M, 58
Shy-Drager
syndrome
Time
since
Diagnosis
Orthostatic
Retinop- Hypoathy
tension
Impotence
GI Dysfunction
Other
Major
Symptoms
+
None
-
None
+
None
1 5 yr
+
+
+
+
+
20 yr
-
15 yr
-
+
+
+
+
+
+
+
+
Peripheral
Neuropathy
14 yr
29 yr
8 Yr
10 yr
6 mo
Onset 7 yr,
diagnosis
1 Yr
Low-normal
conduction
velocities
+
-
Gustatory
sweating
None
Painful neuropathy
None
Parkinsonian
features, severe constipation
Parkinsonian
features,
xerostomia,
atonic bladder
Parkinsonian
features, constipation
Khurana et al: Cold Face Test in Humans
145
Results
Bradycardia occurred in all 33 normal subjects as a
response to the SDR and in 48 of 50 normal subjects
in response to the CFT; 2 individuals developed
paradoxical tachycardia. Cardiac arrhythmias occurred in 15% of individuals in response to the SDR
and the CFT; electrocardiographic patterns of junctional rhythm, nodal escape, and wandering atrial
pacemaker were recorded. Idioventricular rhythm
and failure to conduct the atrial stimulus in 1 individual developed only in response t o the SDR. The
immediate occurrence of premature ventricular contractions in response to the SDR in 1 subject necessitated stimulus withdrawal, with no ill effects; this
subject was excluded from the statistical analysis. In
all instances there was a prompt return to normal
rhythm upon stimulus withdrawal. The occurrence of
these rhythm disturbances underscores the need for
careful cardiac monitoring of patients during these
procedures.
Analysis of the heart rate responses to different
stimuli is presented in Table 2. The statistical
significance of the differences in response was assessed by the Wilcoxon matched-pairs signed-ranks
test [27]. The extent to which the response to the
CFT stimulus related to that obtained for the SDR
was measured by the product moment correlation
coefficient. Of the stimuli tested, the SDR produced
the highest average response, 36.9 k 15.2%. The
combination of CFT and apnea gave the next highest
average response, 24.7 & 16.2%; but the difference
from that obtained when only the CFT was utilized
was not statistically significant ( p > 0.10). The CFT
response also had the highest correlation (0.55) with
the SDR. N o t only did the CFT reproduce the characteristic heart rate changes of the SDR, but systemic
blood pressure increased also. The correlation
coefficient between age and the heart rate response
to CFT (-0.18) was not statistically different from
zero ( p > 0.05). The mean CFT response for the 50
over the face in the distribution of the ophthalmic,
maxillary, and mandibular divisions of the trigeminal
nerve for a period of 1 minute each. Preliminary studies
had shown that stimuli lasting 1 minute were sufficient
to evoke maximal response.
In the final stage of the project, 19 patients with neurological disorders were investigated. Patients treated with
drugs known to interfere with autonomic function or with
cardiopulmonary disease were excluded, as were those
with brainstem stroke who demonstrated absence of corneal
reflex or jaw jerk and who were taking anticoagulants.
Clinical information about the 7 diabetic patients as well as
the 3 patients with Shy-Drager syndrome is shown in Table
1; details on 2 patients with Shy-Drager syndrome (Nos. 8
and 9) have been reported separately [ 111. To assess the
integrity of the afferent limb, trigeminal nerve functions
were tested clinically and found to be intact in all patients
prior to their participation in the study. All these patients underwent the CFT. In addition to that test, the
patients included in Table 1 were evaluated using the SDR,
the Valsalva maneuver, and atropine tests.
For the Valsalva maneuver, the subject, in a semirecumbent position (15 degrees above the horizontal), started
forced expiration from the midinspiratory position and
maintained an expiratory pressure of 40 mm Hg for 10
seconds. Care was taken that pressure should rise sharply at
the onset and fall abruptly at the termination of expiratory
strain. The cardiac rate and rhythm were recorded from
before the start to at least 1 minute after completion of the
maneuver. As suggested by Levin [ 181, a “Valsalva ratio”
was calculated from the electrocardiographic recording by
the following equation:
Maximal tachycardia per minute
Maximal bradycardia per minute
A value of less than 1.38 was considered abnormal.
For the atropine test, a bolus of atropine sulfate (0.03
mg per kilogram of body weight) was administered intravenously. The heart rate was monitored for 15 minutes after
completion of the injection, and heart rate was expected to
increase by 38 ? 5.4 beats per minute [7].
Table 2. Bradycardia in Health,y Volunteers Tested with Various Stimuli
Type of Stimulus
Data
No. of subjects tested
Percent reduction in heart rate
Mean
SD
Correlation coefficient with
response to simulated diving
reflex
Simulated
Diving
Cold
Face
Avnea
Apnea
and
Cold
Face
33
50
29
33
14
14
14
36.9
15.2
...
21.4
16.6
0.55
4.4
12.5
0.15
24.7
16.2
0.35
28.0
21.1
0.46
11.2
9.0
0.07
11.9
10.1
0.15
146 Annals of Neurology Vol 7 No 2 February 1980
Division of Trigeminal Nerve
Used for Cold Stimulus
Ophthalmic
Maxillary
Mandibular
Tabable 3. Autonomic Functions in the 10 Patients Investigated"
~
Patient
No.
Valsalva Ratio
~~~~~
Cold Face Test
(% change
in heart rate)
Simulated Diving Reflex
(% change
in heart rate)
Atropine Test
(increase in heart
rate. beatdmin)
Tachycardia, 2.0%
No response
Tachycardia, 2.2%
No response
No response
Test not done
Test not done
Bradycardia, 2.1 %
No response
No increase
8
2
18
Bradycardia, 6.2%
~~~~~
1
2
1.o
1.23
3
0.97
4
5
9
1.14
1.07
1.12
1.06
1.06
1.03
Tachycardia, 2.0%
No response
Tachycardia, 2.7%
Tachycardia, 1.2%
Tachycardia, 4.4%
No response
No response
Bradycardia, 4.3%
No response
10
1.06
Bradycardia, 2.0%
6
7
8
4
20
8
12
No response to
1 mg dose
22
"See Table 1 for clinical detatls on these patients.
Table 4. Response t o the CFT in 9 Patients with Brainstem Lesions
Patient No.,
Sex, and
Age (yr)
Diagnosis
11. M, 75
Brainstem stroke
12. M, 60
Locked-in syndrome
13. F, 75
Brainstem stroke
14. M, 51
Brainstem stroke
15. M, 52
16. M, 71
17. F, 24
18. M, 36
19. M, 26
Locked-in syndrome
Brainstem stroke
Multiple sclerosis
Multiple sclerosis
Multiple sclerosis
*
volunteers was 21.4 16.6%. Cold compresses produced a significantly higher average response when
applied in the ophthalmic division of the trigeminal
nerve than in the other two divisions (p < 0.01 compared with maxillary division andp < 0.02 compared
with mandibular division). The cardiovascular response from bilateral stimulation of the ophthalmic
division correlated better with the SDR than did responses from bilateral stimulation of the mandibular
and maxillary divisions. It was evident from the analysis that in humans, the heart rate change in response
to the CFT correlated well with the SDR and that the
Time
since
Diagnosis
in heart rate)
2 da
7 da
14 da
60 da
1 da
2 da
7 da
90 da
4 da
7 da
10 da
4 wk
20 mo
4 wk
5 wk
9 Yr
11 yr
9 Yr
Tachycardia, 7.4%
No response
Bradycardia, 13.4%
Bradycardia 4.0%
No response
Bradycardia, 4.8%
Bradycardia, 2.4%
No response
Tachycardia, 2.2%
Tachycardia, 7.9%
Tachycardia, 7.5%
Bradycardia, 4.5%
Same
No response
Bradycardia, 2.1%
Tachycardia, 40.6%
No response
Tachycardia, 3.3%
Cold Face Test
(% change
afferent endings responsive to the CFT are mostly
located in the ophthalmic division of the trigeminal
nerve.
Seven diabetic patients with autonomic dysfunction and 3 patients with Shy-Drager syndrome were
studied to compare the CFT with other tests of vagal
function, i.e., the SDR [4],atropine test [7], and Valsalva maneuver [ 171. The data are presented in Table
3. In each of the 10 dysautonomic patients studied,
neither the CFT nor the SDR produced a normal degree of bradycardia; some patients even showed
minimal tachycardia. Blood pressure rose in 8 pa-
Khurana et al: Cold Face Test in Humans 147
tients, was minimally increased in Patient 9, and was
unchanged in Patient 8. The SDR was performed
validly in only 8 patients because 2 were unable to
hold their breath under water. The Valsalva ratio was
abnormal in all 10 patients, ranging from 1.0 to 1.23.
Intravenous administration of atropine also failed to
produce the normal degree of tachycardia in any of
these patients. Thus the abnormal responses to the
CFT correlated well with those to the SDR, the Valsalva maneuver, and the atropine test in all patients.
Of the 10 patients, 1 (Patient 8) subsequently died
of complications of the Shy-Drager syndrome. Histological study of the vagus nerve revealed severe
demyelination with relative sparing of the nucleus
ambiguus and dorsal motor vagal nucleus.
Nine patients with recent or longstanding brainstem lesions were studied to determine the effect on
the CFT response. The results in these patients are
summarized in Table 4. Three patients (Nos. 11, 12,
and 13) with acute vascular insult to the brainstem
initially displayed either no response or tachycardia,
and sequential testing in 2 of them suggested some
correlation of bradycardia with clinical improvement.
The third patient, however, showed accentuation of
the abnormal response as her neurological status improved. Six patients (Nos. 14 through 19) with
long-term involvement of the brainstem also showed
minimal bradycardia, no response, or tachycardia. A
follow-up evaluation of Patient 14, 20 months later,
demonstrated clinical recovery without further improvement in response to the CFT. All patients manifested a blood pressure rise in response to CFT.
Discussion
Cardiovascular reflexes involving trigeminovagal
pathways have been elicited in humans by application
of a sinusoidal electric current to the various peripheral branches of the trigeminal nerve [2 11 and in rabbits by electrical stimulation of the trigeminal tract
and its nucleus in the brainstem [16]. In both experimental situations, stimuli have caused bradycardia and hypotension. A reflex produced by irritation
of the trigeminal nasopharyngeal nerve endings is
also known to cause bradycardia [26]. The diving
reflex and its modifications (SDR, CFT) constitute
another variety of trigeminovagal reflex which is a
reproducible [22] response to a physiological stimulus with a transient increase in blood pressure [ 2 8 ] .
This study validated the CFT in comparison with the
SDR in 33 normal volunteers and standardized it in
50 healthy individuals. In response to the CFT, all
subjects showed a blood pressure rise and all but
2 manifested bradycardia. T h e development of a
paradoxical response-i.e., tachycardia-in these 2 individualsmay have resulted from the elevated intrathorack pressure during this test, which can initiate the
pulmonary vagal reflex [2, 5 , 231 causing tachycardia.
148
Annals of Neurology
Vol 7 No 2
February 1980
The neuroanatomical pathways of the diving reflex
consist of facial receptors, trigeminal afferent nerve
pathways, central brainstem connections, sympathetic and parasympathetic efferent pathways, and effector organs. In humans, the afferent nerve endings
have been considered sensitive to cold, wet, or noxious stimuli during the response to face immersion
[20, 22, 2 4 , 251. Afferent impulses travel via the
trigeminal nerves to the brainstem. Andersen [ 11 has
demonstrated in ducks that the bradycardia accompanying the diving reflex depends on integrity of the
trigeminal nerve, particularly its ophthalmic division.
Our investigations indicate that the ophthalmic division is the most sensitive trigeminal pathway in humans. The centers for this reflex are located in the
medullary region and can function independently of
higher centers. However, higher centers can have
either an inhibitory or a facilitatory effect on the
medullary region [29]. The sympathetic efferent
pathways mediate peripheral vasoconstriction [8].
The parasympathetic efferent pathway is the vagus
nerve, the cardioinhibitory response being abolished
by vagotomy or atropinization in animals [2, 221. Increased vagal activity is primarily responsible for the
decrease in heart rate. It is evident that diving, simulated diving, or the cold face test can each demonstrate integrity of the trigeminal-brainstem-vagal
pathways, and interference anywhere in the reflex arc
can alter or abolish the characteristic cardiovascular
response.
Bennett and his colleagues [4] investigated the
cardiovascular reflex responses to apnea accompanied by immersion of the face in water (SDR) in 2 1
unselected diabetic patients. Eleven subjects demonstrated tachycardia, little change in mean arterial
pressure, and forearm vasoconstriction or vasodilatation. They reasoned that mixed responses argue
against these abnormalities being due to an afferent
lesion. W e studied the cardiovascular responses to
the CFT in patients with clinically intact afferent
pathway functions and suspected lesions at the central or efferent levels (or both) of the neural axis, to
collect information which could further the use of the
CFT in localization. Patients with an established
diagnosis of diabetic neuropathy were utilized since
pathological involvement of the peripheral vagus
nerve in this disorder is well known [15]. The patients with brainstem stroke and multiple sclerosis
were selected as examples of intraparenchymal involvement, and those of Shy-Drager syndrome were
presumed to have lesions affecting either or both
areas of the neural axis [3]. It was apparent that acute
as well as chronic brainstem lesions and peripheral
vagus nerve lesions altered the heart rate responses
to the CFT, whereas a rise in blood pressure occurred
in both instances. The findings indicate that measurement of these two cardiovascular variables-
blood pressure and heart rate-would
not differentiate between a central and an efferent lesion.
Clinical assessment of the trigeminal nerve and brainstem functions is essential for accurate localization of
the lesion.
The present study was carried out to investigate
the role of the CFT as a possible simple bedside
“tool” in the diagnosis of vagal and brainstem dysfunction. As anticipated, the patients with vagal
hypoactivity (see Tables 1 and 3) did not develop as
marked bradycardia as did the normal subjects from
vagotonic stimulation using the CFT, the SDR, and
the Valsalva maneuver. In addition, these patients
manifested less than normal tachycardia in response
to pharmacological doses of atropine. The clinical
evidence of vagal dysfunction was corroborated
pathologically by severe vagal demyelination in the
single patient who was subsequently examined postmortem. The impaired heart rate response to the
CFT in patients with brainstem dysfunction (see
Table 4 ) suggested that the CFT could be of additional value in localizing suspected pontomedullary
lesions. Clinical applications of the CFT might also
include: (1) study of cardiovascular autonomic disturbances, independent of baroreceptor stimulation;
(2) longitudinal studies of the progress of autonomic
dysfunction; and (3) demonstration of persistence of
sympathetic functions in the absence of the counteracting effects of vagal functions. The last point
suggests the possible pathophysiological mechanism
involved in the occurrence of pressor responses [ 101,
acute gastric lesions [ 131, cardiac disturbances, and
higher mortality in stroke patients [6, 141.
7.
8.
9.
10.
11.
12.
13.
14.
15.
16.
17.
18.
19.
20.
21.
Supported by the Pangborn Fund, a grant-in-aid award from the
American Heart Association, and NINCDS Grant 5 P50 NSO
6779-1 0.
22.
Presented in part at the 102nd Annual Meecing of the American
Neurological Association, June, 1977 [12].
23.
24.
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Khurana et al: Cold Face Test in Humans
149
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