Respiratory Medicine (2014) 108, 1049e1055
Available online at www.sciencedirect.com
ScienceDirect
journal homepage: www.elsevier.com/locate/rmed
Nocturnal snoring decreases daytime
baroreceptor sensitivity
Christoph Schöbel a,b, Ingo Fietze a, Martin Glos a,
Inett Schary a, Alexander Blau a, Gert Baumann b,
Thomas Penzel a,*
a
b
Sleep Medicine Center, Charité Universitätsmedizin Berlin, Berlin, Germany
Center for Cardiology and Angiology, Charité Universitätsmedizin Berlin, Berlin, Germany
Received 29 December 2013; accepted 24 March 2014
Available online 2 April 2014
KEYWORDS
Snoring;
Sleep disordered
breathing;
Baroreceptor
sensitivity;
Heart rate variability;
Cardiovascular risk
Summary
Background: In patients with obstructive sleep apnea heart rate variability and baroreceptor
sensitivity during night and daytime are impaired. Snoring without obstructive sleep apnea
may already influence heart rate variability and baroreceptor sensitivity during daytime.
Methods: Cardiovascular daytime testing was performed in 11 snorers and age, BMI, and
gender matched controls. Sleep apnea and snoring were quantified by sleep recordings. Paced
breathing was performed during daytime with ECG, non-invasive blood pressure, and respiration recorded. Heart rate variability and blood pressure variability were analyzed in the time
and frequency domain. Baroreceptor sensitivity (alpha gain) was calculated.
Results: In snorers a significant increase in high frequency systolic blood pressure variability
(SBPVeHF) compared to control group (0.37 mm Hg2 vs. 0.11 mm Hg2 for 12 breaths and
0.35 mm Hg2 vs. 0.10 mm Hg2 for 15 breaths) was demonstrated. Furthermore a lower baroreceptor sensitivity was found in snorers compared to controls (9.2 ms/mm Hg vs. 16.2 ms/
mm Hg for 12 breaths and 8.5 ms/mm Hg vs. 17.4 ms/mm Hg for 15 breaths per minute) using
the paced breathing protocol. Mean heart rate was elevated in snorers as well.
Conclusions: Snorers may have a reduced parasympathetic tone during daytime rather than an
increased sympathetic tone.
ª 2014 Elsevier Ltd. All rights reserved.
* Corresponding author. Charité Universitätsmedizin Berlin, Sleep Medicine Center, Charitéplatz 1, D-10117 Berlin, Germany. Tel.: þ49 30
450513 013; fax: þ49 30 450513906.
E-mail address: thomas.penzel@charite.de (T. Penzel).
http://dx.doi.org/10.1016/j.rmed.2014.03.012
0954-6111/ª 2014 Elsevier Ltd. All rights reserved.
1050
C. Schöbel et al.
Introduction
Methods
Sleep related breathing disorders have a high prevalence
and are associated with an elevated cardiovascular risk.
Sleep apnea patients have an increased cardiovascular
morbidity and mortality [1]. Patients have a lower life expectancy and a higher risk for cardiovascular consequences
such as stroke, myocardial infarction, and cardiac arrhythmias. The risk to develop arterial hypertension and
heart failure is increased [2,3]. The most important pathophysiological mechanisms in sleep disordered breathing
are upper airway obstruction, repetitive intermittent hypoxemia, and intrathoracic pressure changes. Many cardiovascular consequences can be related to concomitant
changes in autonomic tone.
Each apnea event is a cessation of oronasal airflow for at
least 10 s duration. Each hypopnea event is a reduction of
airflow by at least 50% in amplitude for at least 10 s
accompanied by an oxygen desaturation by at least 3% [4].
Sleep apnea severity is specified by the apnea hypopnea
index (AHI) which corresponds to the number of apnea and
hypopnea events per hour of sleep. Patients with an AHI
between 5 and 15 events/hour suffer from mild sleep
apnea, between 15 and 30 events/hour from moderate
sleep apnea and above 30 events per hour from severe
sleep apnea. Large studies proved that patients with
moderate and severe sleep apnea have an increased cardiovascular risk [5].
Snoring is regarded as a precursor for sleep disordered
breathing. Whether snoring itself with few apnea and
hypopnea events (AHI < 5 events/hour) causes an increased
cardiovascular risk is not clarified. A large epidemiological
study by Marin et al. did not detect an increase in cardiovascular events in snorers compared to controls after 12
years [1]. However studies in animals showed that snoring
associated micro vibrations caused micro lesions on the
extracranial vessels which increased the risk for local
arteriosclerosis [4,6e8]. Mateika et al. showed a reduction
in baroreceptor sensitivity (BRS) in snorers with a low AHI
and interpreted this as an indication for increased cardiovascular risk [9].
Assessment of autonomous tone can be done directly
and indirectly. Direct recordings require microneurographic
recording of sympathetic nerve activity on the perineous
nerve [10]. This method is painful and not practical in
clinical studies. Indirect assessment of autonomic tone is
performed using heart rate variability (HRV), blood pressure variability (BPV), and baroreceptor sensitivity (BRS)
[10]. Based on HRV a summarizing value, called sympathovagal balance, can be calculated. Sympathetic tone is
increased in patients with sleep disordered breathing not
only at nighttime but also during daytime [3]. This is reflected by both an impaired HRV and BRS. This can be an
indicator for elevated cardiovascular risk [11].
CPAP treatment in patients with obstructive sleep apnea
improves sympathovagal balance after three months usage
[12].
That sympathovagal balance is affected in snorers had
been shown previously [9]. Whether sympathovagal balance
is impaired in snorers not only at nighttime [13e15] but also
during daytime, similar to obstructive sleep apnea [16] is
the focus of this study.
Subjects
For the study 14 patients with snoring and without sleep
apnea were recruited between February 2004 and July 2005
at the sleep center. Selection criteria were strict and focuses on snoring without sleep apnea. For each snorer a
carefully selected healthy control subject was matched for
age, BMI and gender. All subjects were investigated for
daytime autonomous function using the same experimental
protocol. For daytime testing of autonomous functions
a customized experimental protocol was used. Because the
autonomous nervous system is modulated by many mental
and physical factors, a strict and standardized study protocol was conducted in order to standardize these influences. The study was approved by the institutional ethics
committee.
One patient could not be evaluated due to technical
problems with the daytime recording and two other patients resigned from the study without giving reasons.
Finally data from 11 patients and 11 matched controls could
be used for consequent analysis. The characteristics of the
two matched groups of snorers and controls are presented
in Table 1.
All subjects were recorded with a six-channel portable
sleep apnea monitoring device (Embletta, Embla Systems
Inc., Broomfield, CO, USA) to evaluate the presence of
sleep apnea and to detect sleep related movement disorders (e.g. periodic leg movements during sleep) before
daytime testing. The portable sleep monitoring device did
record oral airflow, respiratory effort with belt sensors,
snoring by an analysis of pressure fluctuations, body position, oxygen saturation and pulse rate. The number of
apnea and hypopnea events per hour of estimated sleep
(AHI) were evaluated. We used the integrated Embla
derived snoring signal by vibration in the nasal cannula as
provided by the Somnologica-Software to quantify the time
with snoring noise against the total recording time [17].
Subjects completed a clinical investigation, a questionnaire
to assess daytime sleepiness (Epworth Sleepiness Scale,
ESS), a lung function test to exclude restrictive and
obstructive pulmonary disorders, and clinical chemistry of
blood to exclude other disorders and drug use. Inclusion
criteria were age above 20 years, a BMI lower than 40 kg/
m2, an AHI lower than 5 events per hour, a history of reported snoring and acceptance to participate in the study.
Exclusion criteria were misuse of sedating drugs, abuse of
Table 1 Characteristics of the controls and the snorers
are presented. There are no significant differences between
groups.
Female
Male
Age [years]
BMI [kg/m2]
AHI [events/hour]
Controls
Snorers
1
10
41.1 8.5
26.3 3.6
3.18
1
10
43.1 8.7
27.3 3.8
3.45
Nocturnal snoring decreases daytime baroreceptor sensitivity
alcohol, use of anti-arrhythmic drugs, chronic cardiovascular disorders, pain disorders, acute or chronic inflammatory disorders, thyroid disorders, mental or neurological
disorders, disorders which would affect the respiratory
system, and other sleep disorders.
Eleven healthy control subjects were selected to match in
terms of age, gender, and BMI. These subjects were selected
from a group of volunteers with undisturbed sleep being
recruited for another cohort of healthy sleepers [18]. For the
control group all the disorders mentioned above were
excluded as well by checking for pathological thresholds.
The control group underwent a cardiorespiratory polysomnography in a sleep center in order to exclude all sleep
disorders, sleep disordered breathing in particular and
presence of snoring as well.
Study protocol
Daytime testing of cardiovascular functions in terms of HRV,
blood pressure variability (BPV), and BRS took place between 9 and 12 in the morning after the portable sleep
testing at home (Embletta, Embla Systems Inc., Broomfield,
CO, USA). Subjects were instructed not to use caffeine and
vasoactive agents on the morning before the assessment.
Testing followed a standardized protocol which proved
to be effective in previous investigations [18e20]. Recorded signals were ECG (lead II), nasal airflow with pressure
sensors using nasal prongs, ribcage and abdominal respiratory movements with piezo sensors, and non-invasive
continuous blood pressure (Portapres). Signals were recorded using a polysomnography recorder (Embla A10, Embla
Systems Inc., Broomfield, CO, USA). Subjects were seated
with the upper body in 45 resting position. After a test run
the protocol was performed in always the same order: six
minutes quiet breathing followed by three times 6 min
paced breathing at three different paces, 6 then 12 then 15
breaths per minute. At the end of the protocol another
6 min breathing at rest followed. Pacing was performed
with a metronome and there were short breaks of two minutes duration between the test sessions. Paced breathing
episodes with 6 breaths were not further analyzed because
subjects could not maintain this frequency well enough in
terms of regularity.
Signal analysis
ECG and the blood pressure signal were analyzed using the
MATLAB software (The Math-Works Inc., Natick, MA, USA)
with previously described algorithms [19e21]. ReR intervals and systolic blood pressure were calculated. Artifacts were removed and episodes with 180 consecutive
heart beats were selected. Time series were interpolated
using cubic splines, and were re-sampled at 4 Hz. Fast
Fourier transform (FFT) was applied to calculate power
spectra of HRV and systolic blood pressure variability (SBPV)
Low frequency (LF Z 0.04e0.15 Hz) and high frequency
(HF Z 0.15e0.4 Hz) spectral bands were integrated for HRV
(HRV-LF, HRV-HF) and SBPV (SBPV-LF, SBPV-HF) analysis.
In HRV, vagal activity is the main contributor to the HF
component for subjects in supine position under controlled
respiration
without
pharmacological
or
physical
1051
interventions. The LF component reflects both sympathetic
and vagal autonomic activity [22]. Another important measure of HRV is the root mean square of successive heartbeat
interval differences (RMSSD). RMSSD reflects the short-term
variation of heart rate and is claimed to be a good surrogate for LF/HF-ratio as marker for sympatho-vagal balance
[23]. The spontaneous baroreceptor sensitivity (BRS) is based
on the permanent activity of the baroreflex feedback loop
integrating spontaneous fluctuations. The BRS was calculated using the squared root of the ratio of HRV and SBPV (so
called a-gain). This was performed separately for the LF and
HF spectral bands resulting in a-LF and a-HF. Finally, the a
index was calculated as the mean of a-LF and a-HF [24]. All
BRS values were expressed in ms/mm Hg. The a-LF displayed
the gain of the arterial pressureeRR interval relationship in
the spectral region not linked to the breathing frequency
whilst the a-HF component mirrors the gain in the spectral
region of the breathing frequency [25]. The a index presented the average of a-LF and a-HF and provided an evaluation of the overall baroreceptor gain [26].
For statistical analyses SPSS for Windows (version 12.0,
SPSS, Chicago, IL) was applied. Result parameters were
presented with median, lower and upper quartile to be independent of distribution assumptions. For testing differences between groups (Table 2) ManneWhitney-U-Test was
applied for non-parametric variables. Differences were
considered significant at a two-tailed p-value of 0.05. Tables
1 and 2 expresses the results as means standard deviation.
Results
Both groups were carefully matched and did not differ in
terms of age, BMI, and gender. Both groups had no sleep
apnea with a confirmed AHI < 5 events/hour of sleep, see
Table 1. None of the snorers nor the healthy subjects had
arterial hypertension. The mean blood pressure in the
snorers was 140/85 mm Hg.
Assessing the cardiac autonomic nervous system by
quantifying HRV and BPV considered the paced breathing
episodes with a pace of 12 and 15 breaths per minute. The
results of the comparison are presented in Table 2.
With paced breathing at both breathing rates snorers did
show an increased heart rate compared to controls
(p < 0.05). Heart rate variability measures did not differ
between the groups. With respect to blood pressure variability significant differences were observed for the high
frequency component of systolic blood pressure variability
(SBPVeHF) The other blood pressure variability parameters
did not show significant differences between controls and
snorers. For baroreceptor sensitivity expressed as alpha
gain significant differences were found and shown for a
Index (Fig. 1).
Discussion
Results showed a significant increase in high frequency
blood pressure variability and a significant decrease in
baroreceptor sensitivity between healthy volunteers and
snorers at the paced breathing tests during daytime.
Snorers did show in addition an increased heart rate at
paced breathing. Together this may indicate a reduction in
1052
C. Schöbel et al.
Table 2 Results for heart rate variability, blood pressure variability and baroreceptor sensitivity for the daytime testing during
paced breathing. Significant differences were seen for both 12 and 15 breaths per minute for mean RR intervals, SBPV-HF, for aHF, and for a index.
Parameter
Controls
Snorers
12/min
Mean RR intervals (ms)
RMSSD (ms)
HRV-LF (ms2)
HRV-HF (ms2)
Mean SBP (mmHg)
SBPV-LF (mm Hg2)
SBPV-HF (mm Hg2)
Mean DBP (mm Hg)
a-LF (ms/mm Hg)
a-HF (ms/mm Hg)
a index (ms/mm Hg)
948
35.5
23.0
40.2
141.1
0.26
0.11
69.9
10.31
22.16
16.24
15/min
115
14.2
13.0
33.4
17.1
0.13
0.08
8.7
3.7
12.8
7.0
956
39.1
18.2
26.2
136.0
0.31
0.10
69.4
10.13
28.20
17.41
137
21.0
11.1
21.8
19.1
0.21
0.10
9.4
5.1
15.4
8.4
parasympathetic tone in snorers during daytime rather than
an increased sympathetic tone.
Blood pressure variability reflects periodic variations of
blood pressure due to vasomotion and respiration. Paced
breathing was used to control the influence of respiration
on blood pressure. The low frequency component of BPV
mirrors sympathetic activity and the high frequency
component mirrors the mechanical influence of respiration
on systolic blood pressure [27,28]. Our study showed an
increase of BPV-HF and a minor non-significant increase of
BPV-LF. This was interpreted as a sign for increased blood
pressure variability in snorers. This effect was not been
shown before. Lombardi et al. (2000) [29] demonstrated a
higher BPV in sleep apnea patients compared to controls.
Our data confirmed this effect for people snoring only.
30,0
p < 0.05
p < 0.05
12/min
15/min
p-Value
12/min
Controls
Snorers
25,0
20,0
15,0
10,0
5,0
0,0
α index [ms/mmHg]
Figure 1 The alpha index which provides an evaluation of
the overall baroreceptor gain is shown for paced breathing at
12 and 15 breaths per minute. Box plots show the significant
differences between controls (left side) and snorers (right side)
for both breathing rates.
836
36.4
21.2
46.9
124.3
0.39
0.37
72.3
8.56
9.74
9.15
15/min
81
24.2
13.1
54.4
21.1
0.42
0.24
11.5
3.3
3.6
2.5
848
36.3
20.6
46.2
126.4
0.49
0.35
72.5
7.03
9.94
8.48
94
36.9
15.3
81.6
22.5
0.42
0.28
13.1
2.3
5.9
2.7
12/min
15/min
0.029
n. s.
n. s.
n. s.
n. s.
n. s.
0.004
n. s.
n. s.
0.015
0.015
0.042
n. s.
n. s.
n. s.
n. s.
n. s.
0.05
n. s.
n. s.
0.014
0.05
Baroreceptor sensitivity reflects the sensitivity of the
baroreceptor on changes in arterial blood pressure. During
resting conditions the baroreceptor sensitivity characterizes the state of the autonomous tone [30]. The result of
normal baroreflex function is an attenuation of short term
blood pressure variations. Several studies proved that
baroreceptor sensitivity is lower in patients with hypertension, diabetes mellitus, smokers, and obstructive sleep
apnea [11,31,32]. Gates et al. [15] found a lower BRS in
snorers compared to control subjects only in sleep, but not
in wakefulness. Treatment with CPAP had a beneficial effect and led to an increase of BRS in snorers. BRS was
calculated using the spontaneous baroreflex-sequencing
technique which is well proven but also critiqued [33].
BRS was investigated during spontaneous respiration during
NREM sleep and wake state prior to the onset of sleep. Thus
it was not possible to eliminate the modulating effect of
respiration on gain of baroreceptor reflex [34,35]. Therefore we used a standardized protocol with paced breathing
in wakefulness. So we tried to get nearly constant inspiratory time (Ti) at the defined breathing rate as changes of Ti
could lead to changes in BRS. Nevertheless we did neither
measure exact inspiratory time nor tidal volume. Though
we can imagine that paced breathing forced by a metronome can lead to increase in breathing effort by mental
focusing on respiration. This can result in higher changes in
intrathoracic pressure with possible concomitant activation
of the Bainbridge reflex [36,37]. The subsequent increases
in sympathetic activity would be reflected in reduced BRS.
However this would have also be shown in healthy control
group. In general, in our study BRS was calculated using
squared root of ratio of HRV and SBPV in LF and HF spectral
bands to finally obtain a-index. Therefore findings about
BRS changes of our study cannot simply be compared with
findings of Gates et al. Thus in our study the a-LF index did
not differ between snorers and controls in our study. The
reduced a-HF index observed in our study can be interpreted as a sign of reduced parasympathetic reflex activity
in snorers. One possible interpretation is a reduced stimulation of lung stretch receptors [29] leading to reduced
activity of vagal afferents. Furthermore De Boer [38]
mentioned that BRS above a respiratory rate of 0.2 Hz,
Nocturnal snoring decreases daytime baroreceptor sensitivity
corresponding to 12 breaths per minute is dominated by
parasympathetic drive. However other measures of parasympathetic tone such as RMSSD and HRV-HF did not support this assumption. Hilton et al. [16] investigated
obstructive sleep apnea patients and found a decrease of
the power in the high frequency band during daytime.
Young [39] showed small blood pressure differences
when comparing primary snorers and healthy subjects. Our
study confirmed the results presented by Leroy [40], who
did not demonstrate differences in blood pressure when
comparing snorers (AHI < 15 events/hour) with sleep apnea
patients (AHI 15 events/hour).
Heart rate variability which predominantly reflects
parasympathetic tone showed no differences between
snorers and controls in our study despite mean heart rate
was different. Gates et al. [14] investigated HRV during
nighttime in snorers and healthy controls and also found no
differences. Only with eliminating snoring by CPAP therapy
they could show an increase in sympathetic activity (SNSA)
and a reduction in parasympathetic activity (PNSA). Discussing their findings they postulated the influence of
activated vagal afferents during snoring which may be
weaker in non-snoring episodes (e.g. under CPAP treatment) and therefore leading to a reduction in PNSA and an
increase in SNSA in non-snoring episodes. However they
analyzed HRV only in several 15-min snoring- and nonsnoring segments of NREM sleep (stage 2 or slow-wave
sleep according to stage 3) and excluded REM-stage
explicitly. We did HRV-analysis selecting 180 consecutive
heart beats during testing period in wakefulness. Despite
following the standardized protocol to exclude possible
modulating factors, autonomous tone in wakefulness is
completely different to NREM sleep in which mentioned
vagal afferents could have more impact on overall sympathovagal balance than in REM sleep or wake state.
Furthermore Gates et al. critically discussed HRV differences as short term effect of CPAP treatment as it was
performed in snorers and healthy controls only for 7 days
before HRV analysis.
Ferini-Strambi [41] reported a reduced HRV only when
the AHI was above 10 per hour and Hilton [16] reported a
reduced HRV, especially the high frequency components,
during daytime in sleep apnea patients, independent of
sympathetic tone.
A limitation of the present study is a small number of
patients and controls. Snorers were subject to portable
monitoring with a six-channel sleep apnea monitoring device to exclude the presence of sleep apnea. We are
conscious that the calculated AHI only refers to recording
time and not to total sleep time as calculated by the gold
standard of polysomnography. However, especially in Germany, portable monitoring with a six-channel monitoring
device is a well established diagnostic tool used in clinical
practice to exclude sleep apnea in patients with snoring.
We assessed snoring using the integrated Embla derived
snoring signal by vibration in nasal cannula. It could be
shown that cannula can only measure a range from 0 to
100 Hz although fundamental frequency of snore events
measured by sound analysis is set from 50 to 250 Hz.
Therefore cannula vibration assessment of snoring can miss
a portion of snore events leading to underestimation of real
snoring occurrence [17].
1053
Nevertheless the results contribute to the current discussion because the influences of respiration on parameters
of autonomous tone were carefully excluded by our study
protocol. Studies on parameters derived from the autonomous nervous system regulation during nighttime and
spontaneous breathing, have the advantage to avoid psychological influences and to avoid interaction with test instructions. Our protocol with daytime testing may suffer
from these effects but still we eliminated the effects of
breathing on baroreceptor sensitivity. The only remaining
limitation was that during paced breathing there was no
quantitative control for breath volume. Nevertheless we
are convinced that a standardized approach was useful
when comparing these sensitive parameters.
For non-invasive recording of blood pressure finger
photoplethysmography (Portapres) was used. This method
is generally accepted to analyze blood pressure variability
but not valid for absolute blood pressure values [42]. When
processing the recorded data, single ectopic beats were
eliminated by interpolation. Patients with clinically relevant arrhythmias were excluded from the study.
Bixler described an association of snoring and arterial
hypertension [6]. Mechanisms for the development of hypertension can be the mechanical influence on the carotid
arteries and the carotid blood pressure receptors. This may
cause carotid atherosclerosis [7,43] and sleep fragmentation as a direct effect of snoring noise [43]. Dunai et al. [44]
demonstrated an increased cardiovascular risk in a crosssectional study on heavy snorers compared to quiet
snorers. In that study snoring was a reported feature. Heavy
snorers reported breathing pauses in addition and therefore
obstructive sleep apnea may be responsible for the
increased cardiovascular risk in heavy snorers.
The Sleep Heart Health Study found no correlation between reported snoring and arterial hypertension [45]. For
subjects with an AHI < 10 events/hour morbidity for cardiovascular diseases was not increased. Unfortunately the
Wisconsin Sleep Cohort did not assess snoring quantitatively. Checking for the incidence of hypertension in subjects with an AHI < 5 events/hour in this cohort then 40%
developed hypertension during an observational period of
four years [39]. Rich et al. [8] reported in their communitybased study an elevated overall mortality in subjects with
heavy snoring and a BMI < 30 kg/m2 even without
obstructive sleep apnea. The study used portable sleep
monitoring at home as well to confirm the diagnosis and to
identify subjects with an AHI < 5 events/hour.
Therefore, once snoring is established in a particular
patient, further diagnostic procedures need to follow and
treatment should be initiated if additional risk factors are
present.
Conflict of interest
None of the authors has a conflict of interest.
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