Environmental Noise and Sleep-A Study of Arousals, Cardiac Arrhythmia and Urinary. - Catecholamines.
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1 Sleep. 17(4): American Sleep Disorders Association and Sleep Research Society Environmental Noise and Sleep-A Study of Arousals, Cardiac Arrhythmia and Urinary Catecholamines *N. L. Carter, ts. N. Hunyor, tg. Crawford, td. Kelly and *A. J. M. Smith *National Acoustic Laboratories, Chatswood, Sydney, Australia; troyal North Shore Hospital, St. Leonards, Sydney, Australia; and *CSIRO Division of Mathematics and Statistics, Macquarie University, Australia Summary: Nine adult subjects with documented cardiac arrhythmia were studied during 4 nights of sleep in a laboratory. A sleep polygraph and single-channel electrocardiogram were recorded continuously throughout each night. After the 1 st night's familiarization, the subjects were presented with 1 night each of 50 calibrated aircraft or truck noise events. One other night was noise-free. Intervals containing noise and paired quiet intervals were examined for sleep stage at interval onset, number of sleep stage changes and ventricular premature contractions (VPCs). Overnight urinary catecholamines were also assayed. It was found that noise increased the likelihood of arousal responses to the same extent in all sleep stages (p < 0.05). Four subjects showed frequent VPCs during the experiment. These VPCs were significantly related to sleep stage (p < 0.05) but not to noise events. Excretion of urinary catecholamines did not differ between noise and quiet nights. Key Words: Sleep-Noise-Cardiac arrhythmia - Catecholamines. For some time now it has been suggested that transportation (aircraft and traffic) noise may affect the cardiovascular system. Many studies have been carried out, some with positive findings (1), but the results have not been accepted universally because of apparent flaws in methodology (2). This research is continuing (3), but it is doubtful whether all the right questions are being asked. For example, should we be studying effects of transportation noise on people who already have heart disease? Should we be looking at mechanisms that in the long run could increase the risk of heart disease, such as sympathetic tone or raised serum catecholamines? How can other factors that affect sympathetic tone and serum catecholamines, such as interpersonal reactions, be excluded or controlled in these studies? One approach is to examine these possibilities under controlled and safe conditions in the laboratory and, when it is established that acute reactions occur, carry out similar measures in the field, preferably over a Accepted for publication February Address correspondence and reprint requests to Dr. N. L. Carter, National Acoustic Laboratories, 126 Greville Street, Chatswood, Sydney, 2069, Australi 298 prolonged period using established epidemiological de SIgns. The present laboratory study took aggravation of cardiac arrhythmia and changes in urinary catecholamine levels as starting points. Both have health implications. Cardiac arrhythmia has prognostic significance in people with heart disease, whereas raised serum catecholamine levels may be related to increased blood pressure and risk of heart disease. These variables were studied in people during sleep because (i) very large numbers of people are exposed to noise exceeding recommended levels many times per night over many years (4); (ii) there are documented effects of noise on sleep quality; and (iii) sleep minimizes interpersonal reactions and physical and mental task demands, the effects of which can mask or be confounded with those caused by noise. Cardiac arrhythmia Cardiac arrhythmia is very common in the adult population (5-8) and has prognostic significance in those with underlying heart disease or high cardiac risk factors (9-12). The reasons for the appearance of arrhythmic events such as ventricular premature contractions (VPCs) at particular times are not well known.
2 SLEEP, AROUSALS, VPCS AND CATECHOLAMINES 299 However, it is believed that some activities and states are typically associated with reduced frequency and/ or severity of cardiac arrhythmia, whereas in others they are increased. In people with cardiac arrhythmia, quite mild psychological stress, such as driving a motor vehicle, participating in a stress interview or carrying out mental tasks, can increase heart rate and the frequency and severity of arrhythmias (13-16). Sleep is typically accompanied by reduced frequency and grade of ventricular premature beats (17), as well as reduced heart rate and blood pressure (18,19). Some data suggest that there are variations in the likelihood of arrhythmia that depend on sleep stage or sleep stage change. Rosenblatt et al. (20) found that arrhythmias were more common in rapid eye movement (REM) sleep and in stages 3 and 4 than in other sleep stages. Skinner (21) found that in animals (pigs) stage 4 sleep is a period of increased vulnerability to ventricular arrhythmias, although in humans the situation may be more complex, due to a different pattern of sympathetic and vagal innervation of the heart and a wider variety of underlying lesions within the myocardium. Some studies of cardiac arrhythmia during sleep have indicated that arrhythmia is more common on awakening or when sleep stage is changing (20,22,23). Otsuka et al. (24) studied a subpopulation of arrhythmic patients in whom 70% or more of arrhythmias detected in a 24-hour period occurred during sleep ("night-type" arrhythmias). Patients with paroxysmal tachyarrhythmia showed an increase in arrhythmias during REM sleep, whereas patients with grade 2 VPCs showed an increase during stage 4 sleep. Otsuka et al. postulated that there were two types of arrhythmia influenced by sleep. The first comprised the tachyarrhythmias and were facilitated by an increase in sympathetic tone during REM sleep. The second type consisted of repetitive ventricular premature beats occurring during bradycardia and were related to an increase in vagal tone during slow-wave sleep. Noise during sleep and cardiac arrhythmia Wellens et al. (25) reported that self-limiting ventricular fibrillation resulted when a patient with congenital long Q-T syndrome was awakened by sudden loud noise from an alarm clock. Carter et al. (26) studied the appearance of cardiac arrhythmia in elderly males living close to a busy highway by simultaneously recording indoor and outdoor noise, sleep and a singlechannel electrocardiogram (ECG) (26). Some evidence was found for an association during slow-wave sleep between the noise of truck passbys and the frequency of ventricular beats seconds later. Some research suggests that heart rate is also responsive to environmental noise events during sleep, the response consisting of an increase in heart rate followed by a decrease (27-30). Positive correlations between noise level and heart rate have been found in healthy people exposed to traffic noise while sleeping in their own homes (31-35). These responses appeared not to habituate, even after some years of exposure, and occurred regardless of the type of noise or the person's subjective sensitivity to noise (30). The most likely reason for the effects of noise on heart rate during sleep and the association of cardiac arrhythmia with stress in awake people is an increase in sympathetic nervous tone (36). In the report by Wellens et al. (25), the fibrilla tory response to the alarm clock was prevented by propranolol, a sympathetic nervous inhibitor. Noradrenaline is the main sympathetic neurotransmitter in the heart. Adrenaline, primarily an adrenal medullary hormone, also affects heart function. Concentrations of circulating catecholamines normally reach their nadir during sleeping hours (37). Noradrenaline release in the heart and the secretion rate of adrenaline are susceptible to mental challenge, as is heart rate, even by relatively mild stressors (38). Because noise affects heart rate during sleep, it is conceivable that serum catecholamine levels are also increased by noise-induced arousal during sleep. High values of adrenaline and noradrenaline can have harmful effects on the heart, including changes in cardiac muscle tone due to minute hemorrhages, rhythm disturbances and spasm of the coronary arteries. However, little or nothing is known of the effects of chronic elevations of catecholamines during states of rest such as sleep. It is conceivable that if sleep is compromised by environmental factors such as noise, and if this is accompanied by an increase in catecholamine level, cardiac arrhythmias or both, the risk of harmful sequelae could be increased. In summary, the effect of common environmental noises on heart rate during sleep in healthy people, the association of increased heart rate and arrhythmia with psychological stress in cardiac patients, and the precipitation of ventricular fibrillation in a patient with long Q-T interval syndrome by sudden loud noise suggest that environmental noise could facilitate the appearance of cardiac arrhythmia in susceptible people during sleep. Noise can cause arousals and change in sleep stage and can increase the total number of sleep stage changes during the night (39-41), and could, therefore, also affect the frequency or grade ofarrhythmias indirectly, by way of arousals or a change in sleep stage (20,22,23). Frequent arousals due to noise could also increase total autonomic nervous system activity, which would be indicated by increased excretion of urinary catecholamines overnight, with possible longterm health effects. Sleep. Vol. 17. No
3 300 N. L. CARTER ET AL. Our aims in this study were to carry out a laboratory study of the relations between noise events, arousals, sleep stage and frequency of VPCs and to determine whether total overnight excretion of urinary catecholamines is increased by exposure to noise during sleep and to relate this to the first aim. INSTRUMENTATION AND METHODS Subjects. The subjects were nine outpatients who presented to the Cardiology Department of the Royal North Shore Hospital, Sydney, with a history of cardiac arrhythmi One subject was 26 years old. The ages of the other eight subjects ranged from 46 to 75 years with a mean of 61 years. Each subject slept in a laboratory at the hospital for 4 nonconsecutive nights. The 1 st night was used to familiarize them with the test environment and procedure. The 2nd, 3rd and 4th nights consisted of 1 "quiet" and 2 "noise" nights (1 night with truck noise and I night aircraft noise) in counterbalanced order between subjects. Noise type and level. The truck noises were generated by replaying stereophonic recordings of truck passbys recorded in a previous study (26). The aircraft noise tapes were recordings of aircraft types frequently using major airports. The tapes were replayed into the room where the subject was sleeping, using a Nakamichi 1000 ZXL computing cassette deck (Nakamichi Research Inc., Tokyo, Japan), Technics stereo amplifier Type SU-7300 (Matsushita Electric Industrial Co., Osaka, Japan) and Marconi MF attenuators Type TF 2162 (Marconi Instruments Ltd., St. Albans, England). The output of the attenuators was fed to two Audiosound Laboratories' SO Series Linz S066A Studio Monitor loudspeakers, placed in two comers of the room and directed at the diagonally opposite comers. The noises delivered into the test room were monitored by means ofa Bruel and Kjaer Ih-inch condenser microphone Type 4165 with a Bruel and Kjaer Type 2807 microphone power supply, B & K Type 2204 sound level meter, B & K Type 2120 frequency analyzer and B & K level recorder Type 2307 (Brue! and Kjaer Ltd., Naerum, Denmark). The A-weighted levels and the time histories of all noises presented to the subject were traced on the chart of the level recorder, which ran continuously throughout the experiment. The output of the frequency analyzer was also fed to 2 Neotrace Type ZEF chart recorder (Neotrace Systems, Sydney, Australia) so that the time course of the recorded aircraft or truck noise was traced simultaneously with the physiological dat Responses to the noise events were assessed by comparing electroencephalogram (EEG), electrooculogram (EOG), electromyogram (EMG) and ECG responses during the noise with those occurring during paired quiet periods of the same duration. The overnight background noise level in the test room was established before the experiment commenced. The equivalent continuous A-weighted noise level (L Aeq ) was logged for every minute from 10 p.m. to 7 m. using a Bruel and Kjaer Type 2231 sound level meter fitted with a Bruel and Kjaer Type 4155 Ih-inch condenser microphone under the control of a Sharp PC 1600 computer. All except nine I-minute L Aeq were less than 30 db; the highest was 32 db. Noise exposure. Fifty aircraft or truck noises were scheduled for each noise night. The intervals between noise presentations were randomized and ranged from 3 to 20 minutes. The maximum levels of noise were varied between 65 and 72 dba max Average durations were 24 seconds for aircraft noise and 17.S seconds for traffic noise. The choice of noise levels was based on experimental work by Thiessen (42), who reported that in subjects years of age the probabilities of disturbance and awakening by truck noises of 65 dba peak were 0.55 and 0.25, respectively. With a mixture of males and females, and middle-aged and older subjects, the anticipated probabilities for awakening and disturbance were 0.4 and 0.6, respectively. Polygraphic monitoring of sleep. Vertex (C3-A2) EEG, right and left EOG, submental EMG and the time course and level of the noise were amplified using Neo Medix Type NT 464 and Type NT SIO amplifiers and recorded continuously on the eight-channel polygraph chart. Sleep stage and arousal responses to the noises were visually scored as follows. A point was marked on the chart 2 seconds before onset of each noise. A second point was marked 2 seconds after offset of the noise. A third point was marked on the chart corresponding to 20 seconds after the second mark (noise offset). The sleep polygraph in the interval between the first and third marks was then examined for (i) sleep stage at commencement of the interval; (ii) presence/absence of alpha frequency (S-12 Hz) during the interval; (iii) total duration of alpha; (iv) appearance of alpha after commencement of the interval (called an alpha response); (v) alpha onset latency, measured in seconds after commencement of the interval; (vi) number of sleep stage changes; and (vii) direction of any sleep stage change. Sleep stage was assessed visually using standard methods (43) applied in 10-second epochs. A 10-second epoch length was used to enable both a more precise definition of sleep stage at onset of noise and paired quiet intervals and a more detailed account of changes in sleep stage than would be permitted by 20-second, 30-second or I-minute epochs (43). Alpha frequency and sleep stage change frequently Sleep. Vol. 17. No
4 SLEEP, AROUSALS, VPCS AND CATECHOLAMINES 301 occur in older people in the absence of noise (44). To study the effects of noise and distinguish them from spontaneous arousals and sleep stage changes, the same scoring procedure was carried out on an equal number of paired quiet intervals, each commencing 2 minutes before noise onset. The duration of each quiet interval was the same as its corresponding noise interval. Cardiac arrhythmi Two ECG channels were recorded on cassette by means of a Holter monitor (Oxford Medilogger Type 4000, Oxford Medical Instruments, St. Albans, England) with the electrodes fitted to the chest. One ECG channel was fed to the Neotrace chart recorder and recorded concurrently with the time history of the noise and the sleep polygraph. Measurement of urinary catecholamines. Catecholamines released in the body but not subject to re-uptake by the sympathetic nerves are ultimately excreted in the urine in their native form or as metabolites, which occur in the same proportions as the native forms (45). Therefore, measurement of urinary catecholamines serves as a good indicator of the average overall sympathetic nervous tone during the night. Subjects voided before retiring. All urine subsequently passed was saved, with a final collection in the morning. Noradrenaline, adrenaline and dopamine were extracted with alumina and cation exchange columns and then were separated by high-pressure liquid chromatography, using a C18 column and electrochemical detection (46). Arousals RESULTS Presence or absence of alpha response. Transient arousals with implications for daytime sleepiness can occur without concomitant body movement, respiratory events or sleep stage changes (47). We defined an arousal as the appearance of alpha frequency in the vertex EEG (i) if the subject was asleep at commencement of the interval and (ii) if an episode of alpha frequency began during the interval (noise or quiet). The presence or absence of alpha response was recorded for each noise interval and its corresponding paired quiet interval for both noise nights for each subject. Sleep stage at onset of each noise and paired quiet interval was also recorded. Table 1 gives the proportions of noise and quiet intervals containing alpha responses for each sleep stage at interval onset. These proportions are from data pooled across all subjects and the two noise nights. Fifty-three percent of the noise intervals where the subject was asleep at interval onset showed an arousal response, whereas only 11 % of the quiet intervals did so. TABLE 1. Mean arousal responses per interval Sleep stage at interval onset Inter- All vals Stage 1 Stage 2 Stage 3 Stage 4 REM sleep Noise Quiet A generalized linear model (48) was fitted to the data on the assumption that (i) in each time interval for a given subject there is a probability (p) that an alpha response will occur and (ii) that this probability depended on sleep stage at interval onset and whether or not an aircraft or truck noise was presented. It was found that both sleep stage and noise were related to the probability of an arousal response (p < 0.05), but that there was no significant interaction between the two factors. The probability of an alpha response decreased from stages 1 to 4. There was no significant difference between the probabilities of an alpha response in stages 3 and 4, although this may have been due to the limited amount of data for stage 4 sleep. The probability of an arousal response to noise in REM sleep was similar to that in stage 2 sleep. Clearly noise facilitated an arousal (alpha) response less effectively during slow-wave sleep than when the subjects were in other sleep stages. However, there was also less likelihood that an alpha response would appear spontaneously in quiet intervals commencing in stages 3 and 4 than quiet intervals commencing in stages 1, 2 or REM. The ratios of the probabilities of alpha responses appearing in noise and quiet intervals were similar regardless of sleep stage at interval onset. Duration of alpha responses. An episode of alpha frequency in the EEG may be of very short duration (47). It is possible that alpha responses (due to noise) would be longer than spontaneous arousals. Figure 1 shows box plots of alpha response duration in seconds (again derived from pooled data across subjects) by sleep stage for both noise and paired quiet intervals. In this figure the tapered sections of all the box plots overlap, indicating that the differences between sleep stages and between noise and quiet intervals were not statistically significant (p 0.05) (49). The duration of alpha within the specified intervals was not, therefore, a distinguishing feature of the response to noise. Latency of alpha response. Alpha response latency (time of alpha onset in seconds after start of the noise or quiet interval) may be a key characteristic of the alpha response. Examination of the latency data indicated that the distributions were skewed to the right. A logarithmic transformation was applied and a twoway analysis of variance carried out with noise/quiet and sleep stage at interval onset as the factors. Both main effects were significant (p < 0.05), but their in- Sleep. Vol. 17, No.4, 1994
5 302 N. L. CARTER ET AL. e (a) Noise Intervals (b) Quiet Intervals III 60 I- :J r Cl I, SO - Q),-, (11 (11 40 o Q) 0.(11 30 (11'--' ~ Q) 0:: 20 III. : 10.~ a: 0 ~ I I t ~ REM REM Sleep Stage at Interval Onset FIG. 1. Box plots of the durations of arousal (alpha) responses in noise and paired quiet intervals, by sleep stage at interval onset. Data are from all nine subjects and all noise nights. teraction was not significant (p 0.05). Latencies in stages 3 and 4 were not significantly different but were different from latencies in other sleep stages. These results also are illustrated by box plots in Fig. 2. The notches in the box plots of alpha onset latency for noise and quiet intervals do not overlap, indicating that overall alpha response latency was significantly shorter in noise than in quiet intervals. In Fig. 3, box plots are shown for the same data as in Fig. 2, broken down into sleep stage at onset of the noise and paired quiet intervals. Figure 3 confirms that when the subjects were in stages 1, 2 or REM at noise onset, alpha onset latencies were significantly shorter than when alpha appeared in a quiet interval. However, when the subject was in slow-wave sleep (stages 3 and 4) at noise onset, alpha onset latencies were not significantly different from those occurring in quiet intervals. Sleep stage change. The number of sleep stage changes that occurred in noise and quiet intervals in this series ranged from one to seven. A log-linear model was applied to the number of sleep stage changes per interval. :n (a) Noise (b) Quiet Intervals U 50 Interval s e Q)... CO 40..J Q),-, (11 (11 c u o Q) 30-0.(11 (11,--, 20 Q) 0:: = iiiiiii III. : 10 cr: 0 ~ All Sleep Stages FIG. 2. Box plots of arousal (alpha) response latency in noise and paired quiet intervals, for all sleep stages at interval onset. Data are from all nine subjects and all noise nights. :n U (8) 50 Noise Intervals (b) Quiet Intervals e "r Q)... r CO 40..J " Q),-, (11 (11 30 e u o Q) 0.(11 (11,--, Q) :: = CO -. : 10 cr: 0 I ~ ~ REM REM j ~ Sleep Stage at Interval Onset FIG. 3. Box plots of arousal (alpha) response latency in noise and paired quiet intervals, by sleep stage at interval onset. Data are from nine subjects. Analysis of deviance showed that both noise and sleep stage at interval onset were related to the number of sleep stage changes during the interval, with reliably more sleep stage changes in noisy than in quiet intervals (p < 0.05). These results confirm that the experimental noise events produced arousals and sleep stage changes in addition to those occurring spontaneously, and that their likelihood varied with sleep stage at noise onset. Arrhythmia The nine subjects in this study were selected because they had presented with cardiac arrhythmia that had been confirmed by 24-hour Holter monitoring performed some months previously. Despite this selection, only four of the subjects gave evidence offrequent nighttime VPCs during this study. The numbers of ventricular premature beats occurring in noise and paired quiet intervals averaged over noise nights were 78, 22.5, and 65.5 per night, respectively, for these four subjects. The presence and number ofvpcs was obtained by examining the polygraph charts for each noise session of each subject. With the exception of one subject with frequent couplets, complex arrhythmias were rare, and scoring consisted of counting VPCs within the noise and their paired quiet intervals. The data for both noise nights of each subject were pooled. Figure 4 is a plot of the mean number ofvpcs per interval across subjects for noise and quiet conditions and for each sleep stage. Figure 4 suggests that although there may be no systematic noise effect, VPCs may be more common in slow-wave sleep than in the other sleep stages. Figure 5 plots the mean VPC per interval by presence or absence of alpha response and sleep stage at interval onset. Figure 5 again suggests that VPCs may be more.~ ~ "r Sleep. Vol. 17. No.4, 1994
6 SLEEP, AROUSALS, VPCS AND CATECHOLAMINES 303 3, , 3, , ttl \- 2 Ql... l: H \ Ql III 1 U Q... ttl ~ 2... l: H \ QJ III 1 U Q... Alpha Response Present O~--_ r_------_ _--~ Stage 1 Stage 2 SIIS REM Sleep Stage at Interval Onset FIG. 4. Mean number ofvpcs per interval by sleep stage for noise and paired quiet intervals. Data are from four subjects r------r------,-----~r_----~ a Stage 1 Stage 2 SIIS REM 5 Sleep Stage at Interval Onset FIG. 5. Mean number of VPCs per interval by sleep stage and whether or not the intervals contained an alpha response. Data are from four subjects. likely during slow-wave sleep than in other sleep stages. It also suggests that VPCs are more likely if an alpha response does not occur than if it does. Figure 6 plots the mean VPCs/interval by noise condition and number of sleep stage changes per interval. Although complex, this figure suggests that the frequency ofvpcs is inversely proportional to the number of sleep stage changes in the interval. An analysis of variance was carried out to test the significance of these trends. Because the frequency of ventricular premature beats were "count" data, a generalized linear model assuming a Poisson distribution was applied. Frequency of VPCs was the dependent variable. Independent variables included presence or absence of noise, subject, sleep stage at noise onset (stages 3 and 4 were again differentiated for this analysis), presence or absence of alpha response, and number of sleep stage changes. VPC count was found to be related to sleep stage (p < 0.05). No other main effect or any of the higher order interactions were significant (p 0.05). On follow-up tests, stage 4 and REM sleep differed significantly in frequency of VPCs. Catecholamines The means of the assays of noradrenaline, adrenaline, dopamine for the first ("trial") night and for each noise/quiet night are plotted in Fig. 7. A two-factor analysis of variance, with noise/quiet nights as one factor and catecholamine the other, was carried out. The noise effect was not significant (p 0.05), and there was no significant interaction between noise treatment and catecholamine type. All individual catecholamine values were within normal limits. Arousals DISCUSSION The measurements of arousals and sleep stage changes in this study were carried out to document the effect of the experimental noise events on sleep and to determine whether any effect of noise on cardiac arrhythmia depended on its arousal effect. As shown in Table I, 53% of all noise intervals included an arousal (alpha frequency) response. In spite of differences of method, this figure is similar to that given by Thiessen (42) for the probability of sleep disturbance (downward shifts in sleep stage assessed by the amplitude of alpha frequency) in response to truck noise of similar sound pressure level. In comparison, ttl ~ 2... l: H \ QJ III 1 u Q... 3, ~ Quiet Noise r------r------,------,r_----~ a a 2 3 or more 5 Number of Sleep Stage Changes per Interval FIG. 6. Mean number of VPCs per interval by number of sleep stage changes in the interval. Data are from four subjects. Sleep, Vol. 17, No.4, 1994
7 304 N. L. CARTER ET AL O. 3 0 E :J Dopam!ne Noradrenal! ne Adrenal! ne 0 Tr!al Qu! et AC No! se TR No! se 5 Experimental (Noise) Condition FIG. 7. Mean overnight excretion of adrenaline, noradrenaline and dopamine for each experimental condition. All nine subjects underwent all conditions. 11 % of quiet intervals showed arousal responses, demonstrating that although spontaneous arousals are indeed characteristic of the sleep of the elderly (44), environmental noise at levels of dba can increase the frequency of these arousals about five-fold. It can also be seen in Table 1 that the likelihood of an arousal response in both noise and quiet depends on sleep stage, with the frequency of alpha responses progressively decreasing from stage 1 to stage 4. This may be related to the trend toward greater energy in the low frequencies in the spectral composition of the vertex EEG. If so, REM sleep is again "paradoxical" in that although its EEG is closest to the awake EEG, the likelihood of an arousal response is very similar to that of stage 2 sleep. Table 1 also indicates that while the effect of noise was greater for stage I than stage 2, 2 than 3 and 3 than 4, noise increased the likelihood of an arousal by the same ratio regardless of sleep stage. Thus, whatever the baseline propensity to arousal at any time during sleep may be, the effect of transportation noise was to increase that propensity five-fold. The results regarding whether or not there is a continuum of depth of sleep corresponding to sleep stage are of interest. As Williams (50) pointed out, early definitions of sleep stages (51) included a behavioral component related to a continuum of the arousability or depth of sleep as well as to characteristics of the EMG, EOG and EEG. Williams also cited later research that suggested that this continuum applied only to behavioral awakening, in which the subjects were instructed to press a button or otherwise indicate that they were awake. As he put it, "When awakening is defined as full EEG arousal [only], the awakening thresholds in stages 2 through 4 and REM are appar- ently nearly identical" (50). Williams concluded that the apparently higher thresholds for behavioral awakening in, for example, stage 4 sleep were due to processes involved in the "organisation and control of motor responses" (SO). Research by Lukas (39) appeared to confirm that noise-induced behavioral awakening was more likely in stages 2 and REM than stage 4. However, he also concluded that arousal responses to noise were more likely in stage delta than during stage 2 or REM. The apparent contradiction between the research cited by Williams (50) and Lukas (39) and Dement and Kleitman (51) on the relation between frequency of arousal response to noise and sleep stage at noise onset could be due to confusion as to which of the following two questions is being asked. (i) Is noise-induced arousal more frequent in some sleep stages than others, or (ii) does noise increase the probability of an arousal response by an equal ratio for each sleep stage? Our data, from paired noise and quiet intervals in the same record, suggest that noise operates on a basic propensity to arousal (which varies with sleep stage) and that sleep responds proportionately. The longer latency of the alpha response to noise in stage 4 sleep in our data also appears to reflect a difference in this propensity to arousal. "Depth" of sleep seems a reasonable way to describe this tendency. Arrhythmia The hypothesis that VPCs may be facilitated by transportation noise during sleep was based on five findings: (i) mental challenge can increase heart rate and ventricular ectopic beats (13-16), (ii) ventricular fibrillation occurred in a patient with long Q-T interval syndrome when awakened by an alarm clock (25), (iii) transportation noise was associated with increases in heart rate during sleep in "healthy" people (27-35), (iv) traffic noise caused shifts in sleep stage and (v) cardiac arrhythmia was associated with sleep stage change. The extensive sympathetic nervous innervation of the heart (36) and the capacity of noradrenaline to induce arrhythmias suggested that such arrhythmias would be influenced by increased sympathetic nervous tone. Wellens et al. 's successful treatment of a patient with long Q-T interval syndrome with propranolol (25), a sympathetic nervous system inhibitor, also supported this view. The present data have shown that noise from truck passbys and passenger aircraft does not increase the frequency of VPCs in patients with heart disease and moderately frequent, but low grade, VPCs. However, our Figs. 4 and 5 clearly show an association of arrhythmia with slow-wave sleep, confirmed by statistical tests of significance. Also, Fig. 5 suggests that Sleep, Vol. 17, No.4, 1994
8 SLEEP, AROUSALS, VPCS AND CATECHOLAMINES 305 arousals during slow-wave sleep could be associated with reduced cardiac arrhythmi Failure of the latter to reach statistical significance may have been due to the small number of subjects and the relatively small number of intervals in slow-wave (especially stage 4) sleep (beta error). A trend toward fewer VPCs with increased number of sleep stage changes was suggested by Fig. 6 but also failed to reach statistical significance. Our findings on the association of sleep stage with arrhythmia is consistent with previous work by Skinner et al. (21) and Otsuka et al. (24). The former maintained that ventricular arrhythmias were related to combined high sympathetic and parasympathetic nervous tone. They stated that environmental (cognitive) events can induce cardiac arrhythmia by triggering a process in the frontal cortex, which in turn leads to activity in the inferior thalamic peduncle and the frontocortical-brainstem pathway. The latter then leads to high dual parasympathetic and sympathetic outflow, which inhibits homeostatic reflexes and prepares the subject for a stress response, but also makes the subject vulnerable to arrhythmias. They presented evidence that dual high sympathetic and parasympathetic outflow is characteristic of stage 4 sleep and that noise that caused a pig's sleep to shift from stage 4-while exhibiting cardiac arrhythmia-to REM sleep was associated with cessation of the arrhythmi Skinner et al. suggested that their findings may not be entirely applicable to humans because of different patterns of autonomic innervation in the pig and human heart and the variable locations of ischemia and necrosis in individual human hearts. However, in our data there was a significant main effect associated with the subject variable but no interaction between subject and sleep stage, indicating a consistent pattern of susceptibility to arrhythmia in the various sleep stages. Our findings from patients with predominantly grade 2 VPCs also showed an association between slow-wave sleep and frequency of VPCs, agreeing with Otsuka et al.'s (24) data from grade 2 VPC patients with nighttype arrhythmias. Taken together, the present data, those by Otsuka et al. showing substantial differences between night-type arrhythmias as a function of sleep stage and Wellens et al.'s data on cardiac responses to noise in patients with long Q-T interval syndrome indicate that our initial hypothesis was too limited. Data are also needed on the effects of noise from passenger aircraft and road traffic on patients with tachyarrhythmias, including malignant arrhythmias such as ventricular tachycardia and fibrillation. Also, environmental noise can include noise events that are of sudden onset and high intensity, for example noise from low-flying military aircraft and Very Fast Trains. Noise from low-flying military aircraft has been shown to induce acute increases in blood pressure in elderly (awake) patients. These increases averaged 23 mm Hg (systolic) and 13 mm Hg (diastolic), with individual systolic blood pressure responses as high as 40 mm Hg (52). Such noise could induce arrhythmias in patients with long Q-T syndrome and possibly in other patients with tachyarrhythmias, especially when in stage REM at noise onset (24). We suggest the following questions for further research. Can noise from passenger aircraft, road traffic, low-flying military aircraft or Very Fast Trains trigger arrhythmia in patients with long Q-T syndrome? Are patients with complex ventricular arrhythmias (ventricular fibrillation, ventricular tachycardia and tachyarrhythmias) susceptible to such noise during sleep? Can sudden onset sounds from alarms, low-flying military aircraft or Very Fast Trains induce cardiac arrhythmia during sleep in patients with low-grade ventricular arrhythmias? To what extent do these effects, if any, depend on sleep stage at noise onset? It is well known that attitude to the noise source is an important factor in annoyance reactions to environmental noise (53). Similarly, the meaning of sounds is a factor in sleep disturbance (54). Cognitive factors such as these, as well as the acoustical nature of the noise and the underlying heart disorder, also require research because they may condition the likelihood of harmful effects of noise and arousal during sleep in cardiac patients. Catecholamines The results given above and in Fig. 7 indicate that the overnight excretion of adrenaline, noradrenaline and dopamine is not affected by up to 50 noise events during the night, even though 53% of these events are shown to have elicited arousal responses. From the point of view of environmental noise control these results are reassuring, but they should be treated as a first step. Overnight urinary catecholamines represent the total catecholamines released and not taken up by sympathetic nerve endings, and as such may be more reliable indicators of total catecholamine secretion than relatively brief measures of plasma catecholamines. However, they cannot reflect short-term increases (surges) in the peak levels of circulating catecholamines and the temporal relationship of these peaks with bursts of noise, if such occur in response to noise events during sleep. Detection and measurement of such peak noradrenaline, adrenaline or dopamine levels would require plasma measures taken within 30 seconds of noise onset. A second limitation of assays of overnight urinary catecholamines for estimating potential effects on the heart is that the sympathetic nervous system is not an Sleep, Vol. 17, No.4, 1994
9 306 N. L. CARTER ET AL. "all or nothing system" (38). For example, large regional and organ-specific differences in noradrenaline release have been demonstrated in response to mental challenge. In these studies norepinephrine spillover from the heart was increased by a factor of three, but was only negligibly increased in skeletal muscle in the forearm (38). The same regional effects could apply to noradrenaline release from the heart in response to noise-induced arousal from sleep, but not be detected by measures reflecting only total spillover of noradrenaline, adrenaline or dopamine. To settle this question, further research using invasive methods such as assays of plasma noradrenaline in the coronary sinus is necessary. Acknowledgements: Technical support from P. Ingham is acknowledged. This work was carried out in a laboratory on the premises of the Royal North Shore Hospital. REFERENCES 1. Cohen S, Evans GW, Krantz DS, Stokols D. Physiological, motivational, and cognitive effects of aircraft noise on children. Am Psychologist 1980;35: Thompson SJ. Epidemiology feasibility study: effects of noise on the cardiovascular system. Appendix B-annotated bibliography. Washington: Environmental Protection Agency, Babisch W, Elwood PC, Ising H. Road traffic noise and heart disease risk: results of the epidemiological studies in Caerphilly, Speedwell and Berlin. In: Vanet M, ed. Proceedings of the Sixth International Congress on Noise as a Public Health Problem. Nice vol. I: 23. Bron: L'Institut National de Recherche sur les Transports et leur Securite, Organisation for Economic Co-operation and Development. Fighting noise. Paris: OECD Publications Service, Clarke JM, Hamer J, Shelton JR, Taylor S, Venning GR. The rhythm of the normal human heart. Lancet 1976; Brodsky M, Wu D, Denes P, Kanakis C, Rosen KM. 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