Sympathetic skin response in

obstructive sleep apnea syndrome

Beata ~akrzewska-Pniewska',Tadeusz PrzYbylowski2,

Krzysztof ~ y ~ k i n i e w i cAnna
z ~ , ~ostera-~ruszczyk',
Wadaw
~ r o s z c and
z ~ Barbara ~rneryk-~zajewska'
1
Department of Neurology and ' ~ e ~ a r t m e noft Pneumonology, Medical
Academy, l a Banach St., 02-097 Warsaw, Poland

Abstract. Examination of the sympathetic skin response (SSR), a

non-invasive method of studying conduction in the sympathetic nervous
system was performed in 15 male patients with obstructive sleep apnea
syndrome (OSAS) evaluated by polysomnography who were compared with
7 non-apneic snorers and 26 controls. The aim of the study was to assess
sympathetic nervous system function in OSAS, to compare the results with
those found in non-apneic heavy snorers, to define the pattern of
abnormalities and to study the correlations between SSR results and
polysomnographic parameters. In the OSAS group the mean hand latency was
significantly longer than in non-apneic snorers and healthy subjects. The most
characteristic pattern of abnormalities was an absence of a foot response
found in 12 of 15 OSAS patients. There were no correlations between SSR
abnormalities and polysomnographic parameters. The SSR method seems to
be useful in assessment of the sympathetic nervous system, especially of
those parts related to sudomotor function, in OSAS.

Key words: autonomic nervous system, obstructive sleep apnea, sympathetic

skin response
114 B. Zakrzewska-Pniewska et al.

INTRODUCTION The method is also time-consuming, which makes it im-

practical for wider clinical use.
Obstructive sleep apnea syndrome (OSAS) is charac- A slow reflex depolarization of the skin, the so-called
terized by an abnormal sleep-related breathing pattern galvanic skin response (GSR) or sympathetic skin re-
with apneic or hypopneic episodes, repetitive oxygen de- sponse (SSR), is known to occur following a deep breath,
saturation and short arousals. Recent investigations or an unexpected or arousing stimulus. It originates from
(Soliven et a1.1987, Gould et a1.1988, Martin 1989, synchronized activation of sweat glands as a response to
Stoohs et al. 1990, Young et al. 1993) have emphasized a volley discharge in efferent sympathetic nerve fibers.
an abnormal upper airway resistance accompanied by The experimental data show that the afferent pathway of
noisy breathing (snoring) in OSAS patients. the SSR consists of large myelinated fibers. This was
Autonomic nervous system activity changes are ob- demonstrated by inducing tourniquet ischemia in an arm
served in this syndrome. Parasympathetic tone is in- and recording the SSR from hand and foot: it was not rec-
creased during sleep (Bonsignore et a1.1994) but the ordable in both hand and foot after median nerve stimu-
sympathetic system may be activated during apnea lation, but was present in both following tibia1 nerve
(Cullen Hardy et al. 1994). Recent work points out the stimulation (Uncini et a1.1988). Ischemia induces con-
role of the activity of the autonomic system during apnea duction block in large-diameter fibers, but does not af-
and inter-apneic phase of sleep (Macefield et al. 1995, fect significantly unmyelinated ones. The central
1995a).Evaluation of sympathetic activity in humans by segment of the SSR is polysynaptic and influenced by a
electrophysiological means was, until the last decade, variety of facilitatory and inhibitory factors. The central
difficult to perform and was based mainly upon indirect control of sudomotor responses probably reaches corti-
testing, such as recording from effector organs (e.g., cal levels; an excitatory influence of the limbic cortex
blood pressure responses to postural changes, the cold has been shown in animals. Animal experiments have
pressor test, semiquantitative sweating examination, and shown the importance of the medullary reticular forma-
tests of pupillary response). tion as well as the powerful regulatory influences from
Recording of electrical potentials from the skin fol- the midbrain, hypothalamic or limbic structures (Isanat
lowing various stimuli have been used for a long time (to 1961, Willcott 1969).
our knowledge the first description was by Tarchanoff in Mental stress and emotional excitation have been
1890), but the physiological explanation of these respon- shown to increase the sympathetic activity ( Mc Leod et
ses remained unknown. Later, with the understanding a1.1987) and to have a facilitating effect on the SSR. The
that they depend upon activity of sweat glands, this tech- efferent side of the reflex is made up by sympathetic
nique has been extensively used in psychological and nerve fibers emerging from cells of the intermediolateral
psychophysiological research. The essential develop- nucleus which extends from T1 to L2. The axons of these
ment in our understanding of these skin potentials came white rami communicantes are myelinated and short;
from the introduction of microneurographic recording they end in the sympathetic paravertebral ganglia. Post-
techniques in sympathetic nerve fibers ,by Hagbarth -ganglionic fibers are unmyelinated (C) and innervate
(1972). Later workusing this technique helped to clarify sweat glands in the skin. Sympathetic fibers (sudomotor
the function of the afferent and efferent reflex pathways. as well as vasomotor) for the upper limb leave the spinal
It was shown that sympathetic outflow in human ex- cord at T2-T6 level; fibers that reach the lower limb
tremity nerves consists of two main types of activity: leave the cord at T12-L2 level and the sudomotor out
muscle sympathetic nerve activity (MSNA) and skin flow probably leaves the spinal cord earlier than the va-
sympathetic nerve activity (SSNA). MSNA mainly somotor one. The SSR is probably mediated mostly by
causes vasoconstrictor responses engaged in blood flow sweat gland activation. The most obvious demonstration
control, whereas SSNA contains vasoconstrictor and su- for that is that atropine, locally applied, inhibits the SSR
domotor impulses, engaged in thermoregulation. The (Knezevic and Bajada 1985). Since the eccrine glands are
technique of microneuronography is invasive. The intro- the only structures in the skin that are cholinergically in-
duction of the microelectrode into a nerve is painful, nervated, the influence of the SSR on sweat gland func-
clear records of sympathetic outflows are not obtained tion seems obvious. The response was shown to correlate
from every, even normal, subject. The investigated dis- well with the sweat response evoked by acetylocholine
charges are taken from a limited number of nerve fibers. iontophoresis, a direct measure of sudomotor activity.
 SSR in OSAS 115

The greatest density of eccrine sweat glands is in the pattern of SSR abnormalities and to study the correla-
palms and soles and emotional, in contrast to the ther- tions between SSR and polysomnographic parameters.
moregulator~,sweating is also most prominent at these
sites. This correlates with the ease of recording the SSR METHODS
from palms and soles compared to other skin areas.
Therefore we used this non-invasive technique for OSAS was diagnosed with the use of a computerized
studying the autonomic sympathetic sudomotor function polysomnograph SOMNOSTAR produced by Sensor
in obstructive sleep apnea patients and in non-apneic Medics (Sensor Medics Corporation, 22705 Savi Ranch
heavy snorers. Parkway, Yorba Linda, California).
The present work was carried out to evaluate the use- Sleep studies included routine parameters: EEG (C3-
fulness of the non-invasive test SSR in assessing the au- A2,Ol-A2), electrooculography (EOG) and EMG for
tonomic sympathetic sudomotor function in patients monitoring sleep stages, measurement of airway flow,
with OSAS. The aim of the study was also to compare movements of thorax and abdomen and pulsoximetry for
the results found in healthy controls, in non-apneic heavy diagnosis of disturbances of respiration during sleep
snorers and in OSAS patients. We wanted to define the (Martin 1989). Sleep stages were analyzed according to

P. H.
SSR: s t i m r. m e d .

1 I

0. O O m s STIMI: 7.0mA 6.00s

Fig. 1. Normal SSR response recorded in healthy control after right median nerve stimulation: rp, right palm; lp, left palm; rs,
right sole and Is, left sole responses. Voltage is given for each recording in pV per division (pV/D)
116 B. Zakrzewska-Pniewska et al.

criteria given by Rechtsaffen and Kales (1968). Sleep The latency and amplitude (from negative to positive
studies were conducted between 23.00 p.m. and 6.00 peak) of the largest response were measured. An
a.m. next morning. Apnea was defined as cessation of example of an SSRresponse in acontrol subject is shown
respiratory air flow for longer than 10 s. Hypopnea was in Fig. 1. The SSR was considered abnormal if the
diagnosed when a decrease of flow amplitude by more latency deviation was more than 2 SD compared with the
than 50% was observed for longer than 10 s with a par- control group. The degree of abnormality was quantified
allel desaturation and arousal. An apnea and hypopnea using our laboratory scores defined in Table I - grading
index (AHI) was calculated as the number of apneic and responses from 0 (normal) to 6 points (absent). The
hypopneic episodes per hour of sleep. SaOz min indi- correlations between SSR abnormalities (hand and foot
cates minimal oxygen saturation reading recorded dur- latency values as well as scores) and body mass index
ing sleep study. Sa02 mean indicates averaged oxygen (BMI), apnedhypopnea index (AHI), Sa02 mean and
saturation reading recorded during sleep study. SaOz min were studied using Pearson's correlation coef-
The sympathetic skin response was recorded in sub- ficients test. For group comparisons Wilcoxon rank- sum
jects lying supine in a semi-darkened room, with am- test was used. Statistical significance was defined as
bient temperature of 22-26 OC, after relaxing for 10 min. P<0.05. Values are presented as means SD. +
The SSR was recorded at the same time during the 24 h
cycle (between 10.00 a.m. and 11.00 a.m.). Mean p02 Subjects
found in the conditions of examination was: - 80.78 +
13.08 mm Hg in the non-apneic heavy snorers and 77.14 Obstructive sleep apnea syndrome was diagnozed in
f 8.00 mm Hg in the OSAS patients. Standard EMG disc 15 male patients with a mean age of 45.8 f7.2 years. All
electrodes were placed in the center of the right and left +
of them were obese with mean BMI of 36.9 6.2 kg/m2.
palms as well as in the center of the right and left soles There was no clinical evidence of peripheral neuropathy
with reference electrodes on the dorsal surface of hands on neurological examination. Most of the patients had
and feet. Five consecutive electrical stimuli with 10-12 severe sleep apnea syndrome: mean apned hypopnea
mA intensity and of 0.2 ms duration were applied to the index (AHI) was 51.4 f 18.3. Mean minimal SaOz ob-
right median nerve at the wrist. The stimuli were de- served during sleep was 63 f2096, mean value of averaged
livered at irregular intervals of more than 30 s to assure +
0 2 saturation was 85.4 8.5%. The results obtained in the
reproducibility. Recordings were made simultaneously OSAS group were compared with those from7 non- apneic
from four limbs with EVOMATIC Disa System using a +
heavy snorers whose mean age was 48.0 8.6 years, mean
band pass of 2-5,000 Hz for upper limbs and of 2- 2,000 BMI- 29.8 f 5.5 kg/m2, AH1 did not exceed 10 (mean AHI-
Hz for lower limbs. The input sensitivity was from 50 to 2.6 f 2.3). In non-apneic snorers the mean Sa02 value was
500 pV depending on the amplitude. 93.7 f 1.3% and mean minimal Sa02 value was 89.6 f 1.5.
The results of SSR studies in those two groups were com-
TABLE I pared with SSR findings in the control group of 26 healthy
subjects without breathing abnormalities during sleep
Sympathetic skin response scores with a mean age of 37.7 f 10.6 years.

0 normal RESULTS
1 increase in latency in one limb
2 absence of response from lower limbs +
In control subjects hand SSR had a latency of 1.32 0.10 s
3 increase in latency and decrease in amplitude from (right hand), 1.30 f 0.11 s (left hand). The mean latency
upper and lower limbs from lower limbs was 1.77 f 0.20 s (right and left foot).
4 increase in latency and decrease in amplitude from In the OSAS group the mean right hand latency was
upper limbs, absence of response from the lower
limbs
+
1.56 0.19 s, the mean left hand latency was 1.54 f 0.18 s
and it differed significantly from control group values
5 increase in latency and decrease in amplitude from
(P<0.05, Wilcoxon rank- sum test). The mean right and
one upper and absence of response from the other
left foot latency in OSAS patients was 2.08 k 0.42 s.
limbs
There was no significant difference between OSAS
6 absence of response
group and normal controls for mean foot latency because
 SSR in OSAS 117

TABLE I1

Mean SSR latencies in patients and controls. The foot response was absent in 12 of 15 OSAS patients and in two of 7 non-
-apneic snorers. Because of a small number of measurments the means of foot latency could not be statistically compared

Recording place OSAS group Non-apneic group Control group

(n = 15) (n = 7) (n = 26)

Right hand (x SD) + 1.56 + 0.19 s* +

1.50 0.14 s* 1.32k0.10 s
Left hand (x f SD) 1.54 + 0.18 s* +
1.48 0.13 s* 1.30k 0.10 s
+
Right foot (x SD) 2.08 + 0.42 s 2.00 f 0.14 s 1.77 f 0.20 s
+
Left foot (x SD) 2.08 + 0.42 s +
2.07 0.15 s 1.77 k 0.20 s

*P < 0.05.

J.W. 46y.
SSR: s t im r. med.

4 1s - l
- L

5uV/D

I
0. O O m s STIMI: 10.0mA 6.00s

Fig. 2. Abnormal SSR response recorded in patient with OSAS after right median nerve stimulation: the responses from upper
limbs are normal, absence of the response from lower limbs. Other explanation as in Fig. 1.
118 B. Zakrzewska-Pniewska et al.

TABLE I11 found and there was no SSR from others limbs. In one
patient there was no response from hands and feet. In two
SSR abnormalities in scores patients (13%) SSR was normal from all four limbs.
In non-apneic heavy snorers group the mean right
Score OSAS patients Non-apneic snorers hand latency was 1.50 f0.14 s and left hand latency was
(n = 15) (17 = 7 ) 1.48 f 0.13 s, these mean latencies from upper limbs dif-
fered significantly from these obtained in control group
0 (P<0.05). The mean right foot latency in non-apneic
1 snorers was - 2.00 f 0.14 s, on the left - 2.07 f 0.15 s.
2 There was no difference between these values and the re-
3 sults in the control group (Table 11) but the number of
4 SSR obtained was small (12 = 5).
5 In 5 cases (71%) all responses were present. In two of
6 them ( 28%) an abnormal SSR pattern was observed con-
Total
sisting of delay of hand latency and in 3 of 7 (43%) hand
(abnormal SSR)
and foot latencies were normal. In 2 of 7 patients there
was no response from lower limbs.
The quantitative SSR analysis in both non-normal
of the small number of responses obtained from lower groups and in controls was performed using the score
limbs (12 = 4) in OSAS patients (Table 11). system defined in our laboratory.
The main finding was an absence of foot response Table I11 and Fig. 3 show the scores found in the 3
found in 12 of 15 OSAS patients (80%) - see example in groups.
Fig. 2.). A delay in hand latency was observed in 5 (33%) The score analysis showed that in OSAS group SSR
of patients, whereas in 5 others the SSR recorded simul- changes were more pronounced than in non-apneic group.
taneously from upper limbs was normal. In 3 patients There was no correlation between SSR abnormalities
(20%) the SSR from upper and lower limbs was normal. (latencies and scores) and BMI, AHI, SaO2 min and Sa02
In one patient (6%) a response from one hand only was mean in OSAS and non-apneic group.

SSR ABNORMALITIES

SSR aLmormalities (scores)

Fig. 3. SSR abnormalities distribution (in scores) in OSAS and non-apneic group.
 SSR in OSAS 119

DISCUSSION tion. It is quite probable that during post-apnea the au-

tonomic nervous system is simultaneously affected by
The results of our study showed that sympathetic skin different factors such as hypoxia, arousal and lung infla-
response was very often absent or delayed in patients tion. The data obtained during obstructive sleep apnea
with obstructive sleep apnea syndrome (87%). In non- indicated that MSNA increased progressively during ap-
-apneic heavy snorers group such disturbances were less neas and fell abruptly at resumption of ventilation
frequent (present in 57961, whereas in healthy subjects (Macefield et al. 1995, 1995a).
the SSR was always present. Sympathetic skin nerve activity evaluated by micro-
The delay of latency or the absence of the SSR may neuronography reveals increase of SSNA in response to
reveal an autonomic sympathetic sudomotor activity de- mental stress, to sensory stimuli, to deep breathing and
fect (Tarchanoff 1890, Shahaniet al. 1984, Knezevic and apnea. Under resting conditions SSNA consists of ir-
Bajada 1985, Babaet al. 1988, Niakan et al. 1988, Uncini regular bursts of impulses varying in strenght and dura-
et al. 1988, Watahiki et al. 1989, Elie et al. 1995). tion in relation to the respiratory rhythm. Deep breathing
The delay in latency or the absence of the SSR may following sleep apnea induces a strong burst of SSNA.
depend on the functional lesion at different sympathetic The breathing disorder represented by sleep apnea
levels: at the afferent side of the SSR reflex arc repre- may be accompanied by sympathetic skin overactivity
sented by cutaneous nerves, at the central part, still in- revealed by microneuronography . Contrary to the micro-
completely known, or on the efferent side of the reflex neurographic data our results showed apermanent defect
pathways consisting of sudomotor sympathetic fibers. of sympathetic sudomotor system activity in OSAS pa-
Therefore the SSR delay or absence may not represent tients using the non-invasive technique of SSR. We pos-
only a peripheral effect due to altered responsiveness of tulate that overstimulation and hyperfunction of
sweat glands. sympathetic skin fibers accompaning apneic events
Hoeldtke et al. (1992) observed greatly diminished or proved by Macefield et al. (1995,1995a) may be fol-
absent autonomic surface potentials on the soles in pa- lowed by the failure of the sympathetic skin activity. A
tients with pure autonomic failure and in patients with similar mechanism for SSR abnormalities was proposed
multiple system atrophy. These authors proposed the by Dettmers et al. (1993) in patients with amyotrophic
SSR as a sensitive index of sympathetic dysfunction and lateral sclerosis. Sympathetic system hyperactivity may
not only peripheral gland dysfunction. The sympathetic be responsible for developement of arterial hypertension
skin response test is indicated for assessing the integrity in obese patients with sleep-disordered breathing as sug-
of peripheral sympathetic cholinergic function and in gested by Coy et al. (1996). Carlson et al. (1993) dem-
progressive autonomic failure syndromes (Ravits 1997). onstrated that resting muscle sympathetic outflow was
Electrodermal activity reflects sympathetic choliner- higher in sleep apnea patients than controls. As noted by
gic sudomotor function which induces changes in resist- Ferguson (1993), sympathetic outflow to muscle is regu-
ance of the skin to electric conduction (Knezevic and lated primarily by afferent information from cardiopul-
Bajada 1985, Uncini et al. 1988, Hoeldtke et al. 1992, monary and arterial chemoreceptors. Increased
Gutrecht 1994). The changes are regulated by activity in sympathetic activity might result from decreased inhibi-
the sweat glands but may be generated by presecretory tion, increased excitation, altered central neural process-
activity (Ravits 1997). ing of afferent information, or a combination of these
The sympathetic system was studied in apneic syn- mechanisms. Hedner et al. (1992) recently reported an
dromes by several authors (Hagbarth et al. 1972,Bonsignore abnormal pressor response to hypoxia in sleep apnea pa-
et al. 1994, Takeuchi et al. 1994, Macefield et al. 1995, tients, suggesting that chemoreflex function might be ab-
1995a) using microneuronography. It has been well es- normal in this disease. A link between intermittent
tablished (Bonsignore et al. 1994, Macefield et al. 1995) hypoxia and sustained sympathetic hyperactivity was re-
that the autonomic nervous system plays a crucial role cently suggested in humans by Morgan et al. (1995), who
A,,,.:,,~ +hPpoct-gpnei~ phase of apneic syndromes. Al- demonstrated that sympathetic activation could persist
tered autonomic responses are very common in OSAS even after removal of an hypoxic stimulus. A similar ac-
patients (Bonsignore et al. 1994) supporting the hypo- tivation of the sympathetic nervous system by episodic
thesis that OSAS may reset the threshold of autonomic hypoxia is suggested by the the work of Fletcher et al.
adaptation through chronic sympathetic overstimula- (1992) in rats. In these studies hypertension, which fol-
120 B. Zakrzewska-Pniewska et al.

lows exposure of rats to repetitive, non-apneic hypoxia, AH1 - apnea and hypopnea index
can be prevented by chemical sympathectomy. In all SaO2 min - minimal oxygen saturation during sleep
these situations the overactivity of sympathetic system SaO2 mean - averaged oxygen saturation during sleep
may be evaluated by microneuronography. But alterna- pO2 mean - partial oxygen pressure
tively, central neural processing of sympathetic activity BMI - body mass index
may be altered by chronic sleep disruption and sleep de- CPAP - continuous positive airways pressure
privation. Therefore in OSAS patients we postulate that
chronic sleep disruption due to the apneic episodes dur-
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