Journal of Behavioral Medicine, Vol. 15, No. 6, 1992
Social and Behavioral Factors Associated with Episodes of Inhibitory Breathing Jennifer A. Haythornthwaite] ,2 David E. Anderson, 1 and Lisa H. Moore 1 Accepted for publication: November 18, 1991
Previous research has shown that episodes of &hibitory breathing characterized by low-frequency breathing~ occur both in laboratory animals during intervals preceding avoidance tasks and in humans in the natural environment. The present study investigated social and behavioral factors accompanying episodes of inhibitory breathing that occur in the natural environment. Breathing frequency and tidal volume of ambulatory subjects were monitored via inductive plethysmography. Information concerning location, social environment, behavior, and mood was self-recorded in a computerized diary. The percentage of episodes of inhibitory breathing was found to be significantly greater in social situations than when subjects were alone. Additional analyses eliminated talking as an explanation for these effects. Inhibitory breathing was more frequent when subjects were sedentary rather than active, and inhibitory breathing was not associated with changes in mood or appraisal. Additional research is needed to determine the nature of the social interactions that elicit inhibitory breathing its physiological concomitants, and its long-term health implications. KEY WORDS: respiration; ambulatory monitoring; psychosocial factors; stress.
INTRODUCTION Inhibition of breathing has been observed in response to novel stimuli (Sokolov, 1963), aversive conditioning procedures (Obrist, 1968), and 1Laboratory of Behavioral Sciences, National Institute on Aging, 4940 Eastern Avenue, Baltimore, Maryland 21224. 2To whom correspondence should be addressed at Johns Hopkins University School of Medicine, 218 Meyer, 600 North Wolfe Street, Baltimore, Maryland 21287-7218. 573 0160-7715/92/1200-0573506.50/0 9 1992PlenumPublishingCorporation
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reaction time tasks (Obrist et al., 1969). The physiological concomitants of inhibitory breathing have been found to include increased peripheral resistance and increased blood flow to essential organs, such as the heart and brain (Daly et aL, 1979). Rather than reflecting a resting state, this pattern of physiological change, combined with the fact that oxygen cost and mechanical work are inversely related to breathing frequency at moderate levels of ventilation (Otis, 1964), suggests that inhibitory breathing may reflect a state of physiological arousal. Longer periods of inhibitory breathing have been observed to occur in dogs during the hours preceding the onset of regularly scheduled avoidance trials (Anderson, 1981). When combined with a high sodium diet, this preavoidance response potentiated the development of an experimental hypertension (Anderson et aL, 1983), although neither avoidance conditioning alone nor a high-sodium diet alone were effective. These findings suggest that breathing inhibition may reflect a central nervous system state which affects neuroendocrine regulation of sodium balance and vascular smooth muscle function (Anderson et aL, 1987). The clinical relevance of breathing patterns to hypertension has been further demonstrated through studies of sleep apnea. Epidemiological studies of sleep apnea suggest that approximately 34% of hypertensives experience clinically significant sleep apnea, as compared to less than 2% in the general population (Jeong and Dimsdale, 1989). Sleep apnea has been associated with acute elevations in blood pressure (Tilkian et aL, 1976), and hypertensive patients with obstructive sleep apnea experienced a decrease in daytime blood pressure following corrective surgery (Guilleminault et aL, 1981). Thus, breathing inhibition at night has been associated with long-term blood pressure regulation during the day. Our laboratory has previously demonstrated that episodes of inhibitory breathing occur in most human subjects in the natural environment. The development of an ambulatory respiration monitor (Anderson and Frank, 1990) has made possible the examination of inhibitory breathing while subjects engage in their usual daily activities. We have previously operationalized inhibitory breathing (Anderson et aL, 1992b) as a respiratory frequency of less than 12 breaths/min maintained for 10 rain. This criterion was derived from analysis of differences in ventilatory patterns in the natural environment during daytime and nighttime hours. Average tidal volume and minute ventilation were found to be significantly higher during daytime hours as compared to nighttime hours, although variability during these two periods was comparable (Anderson et aL, 1992b). While average breathing frequency was similar during daytime and nighttime periods, the variability of breathing frequency was greater during the day (Anderson
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et al., 1992b). These findings suggest that variations in breathing frequency play a minor role relative to tidal volume in meeting metabolic oxygen demands associated with physical activity and that breathing frequency may be more sensitive to changes in behavioral conditions than tidal volume (Allen et aL, 1986; Hugelin et al., 1985). Our previous work also demonstrated that the mean for breathing frequency during nighttime hours was approximately 14 breaths/rain with a standard deviation of almost 2 breaths/rain (Anderson et al., 1992b). Consequently, the criterion of 12 breaths/rain was selected to be greater than one standard deviation below average sleeping levels of breathing frequency (Stradling, 1985). Episodes of inhibitory breathing identified using this criterion were found previously not to be accompanied by any consistent reduction in tidal volume (Anderson et aL, 1992b), providing further indication that these episodes were not simply reflecting a resting state. The previous study was the first to establish that these episodes occur in the natural environment, but information about the behavioral and environmental factors associated with breathing inhibition was not available. Therefore, the present study was designed to replicate the observation that most subjects demonstrate these episodes in the natural environment and to identify behavioral and environmental factors associated with these episodes. The specific hypotheses tested in the present study included (a) Are episodes of inhibitory breathing more likely to occur when subjects are at home or at work? (b) Are episodes of inhibitory breathing more likely to occur when subjects are alone or when they are in the presence of other people? (c) Are episodes of inhibitory breathing more likely to occur when subjects are engaged in sedentary behavior, such as desk work or reading, than when they are engaged in nonsedentary behavior, such as locomotor behavior or exercise? and (d) Is the subject's mood or appraisal of experiences during episodes of inhibitory breathing more negative or more positive compared to episodes of other types of breathing? A computerized diary was used to obtain information about these factors during 30-min intervals throughout the day. Subjects completed the diary while they wore a respiration monitor for approximately 12 waking hr.
METHOD Subjects Twenty-three adults, ranging in age from 20 to 57 years (M = 34.6, SD = 11.0), participated in the study. The group included 14 females and 9 males, 22 white and 1 black subjects. All denied a history of cardiovascular
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ttaythornthwaite, Anderson, and Moore
or respiratory disease, all were nonsmokers, and each performed within normal limits on a pulmonary function test. Body surface area, determined using the Dubois equation (Guyton, 1981), ranged from 1.45 to 2.10 (M = 1.8, SD = 0.2).
Apparatus Respiration bands (Ambulatory Monitoring, Inc, Ardsley, NY) were comprised of elasticized fabric, 4 in. wide, containing coils of insulated wire. The thoracic band was held in place under the arms with suspenders, and the abdominal band was held in place over the umbilicus with small adhesive strips which were fashioned with snaps that connected to the band. Bands were selected for each subject which were approximately 6-8 in. less than their thoracic and abdominal circumferences in order to maintain the slight tension necessary to record inductance changes. Depth and frequency of inspiration were recorded via inductance plethysmography in a small (3 • 10 x 19-cm), lightweight (270-g) microprocessor-based unit that was worn on a belt. The development and validation of this recording unit have been described previously (Anderson and Frank, 1990). The microprocessor contained two filters that eliminated artifactual changes due to postural shifts. One filter excluded all inductance changes occurring within 2 sec of the previously recorded breath. A second filter excluded inductance changes of more than approximately 3000 ml or less than approximately 150 ml, depending upon the calibration factor derived using the method described below. Depth of inspiration was measured as the summed change in inductance for both the thoracic and abdominal bands. Mean values of depth and frequency over 2-min intervals were stored in memory. A small light bulb on the recording unit could be activated by pressing a button, enabling subjects to periodically test the integrity of the recording system. Calibration of the recording unit was performed on a respiratory gas monitor (Ohmeda, Denver, CO) which determined tidal volume on a breath-by-breath basis while the subject wore a nose clip. The diary questionnaire, which collected information about the subject's environment and behavior, was administered using a small hand-held computer (MC-II, Corvallis Microtechnology, Inc, Corvallis, OR) that was programmed to signal subjects every 30 min. Questions were derived from diaries previously used in ambulatory monitoring studies and from standardized questionnaires and were adapted for use in the present study. The diary was designed to collect information on a variety of dimensions, while requiring only a few minutes to complete (usually less than 2 min). Ques-
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tions concerned the location of the subject (i.e., home, work, or other locations), whether they were with other people (i.e., alone vs, with other people), the behavior in which they were engaged (i.e., nonsedentary beh a v i o r - e x e r c i s e , housework, climbing stairs, moving about--vs, sedentary behavior--desk work, conversing, eating, reading, resting), posture (upright vs. reclining), mood (positive and negative), and general appraisal of the environment (the importance of events, amount of pressure experienced, how absorbed the subject was, and how undesirable events were). The seven mood items, adapted from the State-Trait Anger Scale (Spiel~ berger et al., 1983b) and the State-Trait Anxiety Scale (Spielberger et al., 1983a), and four appraisal items were rated on 4-point scales (1 = not at all to 4 = extremely) and were rated for the previous 30 min, whereas all other dimensions (e.g., location) were rated for three 10-min segments within the previous 30 min. Subjects carried the computer in a small camera bag adapted with a beeper that provided the signal to begin responding. The programming of the diary included the option for the subject to delay responding if circumstances required a delay (e.g., when driving an automobile). When a delay occurred, the subject was instructed to respond to the diary for the original recording interval unless the delay was 30 min or longer, in which case the subject was instructed to respond for the previous 30 min.
Procedure
Subjects were recruited by advertisement and screened for eligibility by telephone. A monitoring day was scheduled to ensure a typical activity pattern, which for most subjects occurred on a workday. Prior to monitoring, demographic data were obtained, the purpose of the study was explained, and informed consent was obtained. A pulmonary function test was administered which measured forced vital capacity and maximal voluntary ventilation. After fitting the subject with elasticized bands, calibration of the recording system was performed, involving simultaneous direct measurement of tidal volume (respiratory gas monitor) and indirect measurement of inspiratory depth (ambulatory respiration monitor) while the subject breathed into the gas sensor tube. Calibration was performed for 2 min in both upright and supine positions, since previous research has shown that upright ventilation is primarily thoracic and recumbent ventilation is primarily abdominal (Druz and Sharp, 1981; Sharp et al., 1975). The ratio of milliliters per breath recorded directly by the gas monitor to arbitrary inductance units recorded by the ambulatory monitor was calculated for each posture.
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Band size was selected so that calibration factors in the two positions were comparable, indicating that each band contributed proportionally to the summed inductance change per breath when subjects assumed a variety of postures during the monitoring period. Subjects were instructed in the use of the diary by displaying each of the questions on the computer screen and explaining alternative response choices. After this demonstration, subjects were asked to complete one diary recording session by themselves. The procedure for delaying responses was described, although subjects were encouraged to answer the diary in a timely fashion. Episodes of inhibitory breathing were operationalized as an average breathing frequency less than or equal to 12 breaths/min for 10 min (Anderson et al., 1992b). The data for 5 of the 23 subjects (2 females and 3 males, mean age = 30.6, SD = 14.3) were excluded because they contained an insufficient number of episodes of inhibitory breathing (fewer than six 10-min episodes) for comparative statistical analyses of the environmental and behavioral factors associated with inhibitory breathing. The final sample of 18 subjects (12 females and 6 males; 17 white and 1 black; mean age = 35.5, SD = 9.9) was studied for an average of 12.8 hr, ranging from 10 to 14.5 hr. Respiration data were edited to exclude rare disconnections (revealed on the record as an average ventilatory frequency of zero). After removing these intervals and removing 2-min intervals not associated with a diary report, an average of 12.3 hr per subject was available for analysis (range of 9.8 to 14.0 hr). Ventilatory frequency and tidal volume data were averaged over 10 min recording intervals to coincide with the diary records, yielding an average of 73.8 10-min intervals for the sample, ranging from 59 to 84. Response to the computerized diary was good, with subjects requiring only a few minutes to complete the items. Only 1% of responses were missed and only 2% were delayed across the 30-rain recording intervals.
Data Analysis Data from each of the primary dimensions (location, social environment, activity, mood, and appraisal) were analyzed independently of the other dimensions by combining across levels of the other dimensions. Because 96% of the intervals were recorded in the upright position, the information on posture (upright vs. lying down), which was collected for the purpose of calibrating the respiratory units, was not analyzed. However, the analysis of sedentary vs. nonsedentary behaviors allowed an indirect
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assessment of other postural effects, since the behaviors classified as sedentary primarily involved sitting postures, whereas the behaviors classified as nonsedentary involved primarily standing postures. Percentages, rather than absolute frequencies, were used as the unit of analysis since they control for individual differences in the time spent in different environments and activities. Two analytic strategies were used. First, the difference between the percentages for the two elements within each dimension (e.g., location: home vs. work) was categorized and chisquare analyses were performed. This analysis described the consistency of an effect across the 18 subjects within the sample. Second, the significance of the difference in mean percentage between categories was compared using paired t tests. This second analysis quantified the magnitude of the differences between categories. Two subjects were excluded from the analysis of social situations, since they reported fewer than six 10-min intervals of being alone. In order to determine whether compensatory increases in tidal volume occurred during episodes of inhibitory breathing, mean tidal volume and minute ventilation during episodes of inhibitory breathing were calculated within each category and compared using paired t tests. The mood items were combined into positive (calm, pleasant, relaxed) and negative (tense, nervous, strained, irritated) mood scales. Scores on each mood scale and the four appraisal scales (absorbed, importance, pressure, and undesirable) were standardized within subjects. This method compensated for individual differences in the use of the mood and appraisal scales (Hedges et al., 1991). The means for each scale were computed for episodes of inhibitory breathing and episodes of all other breathing and then were analyzed via paired t tests.
RESULTS Across the recording period, mean ventilatory frequency for the 18 subjects was 13.2 breaths/min (SD = 1.1), mean tidal volume was 0.54 liter/breath (SD = 0.2), and mean minute ventilation was 7.07 liters/min (SD = 2.5). The median percent of respiratory episodes classified as inhibitory breathing (ventilatory frequency less than or equal to 12 breaths/ min) was 27%. Mean percentages of recording each category within the three dimensions from the diary are presented in Table I. Although these dimensions were not mutually exclusive (i.e., social situations could occur both at home and at work), analyses were conducted on single dimensions while collapsing across the other dimensions due to the varying numbers of subjects represented in each cells (see Table II).
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Table I. Mean Percentages of Recorded Episodes Within Each Environmental and Behavioral Dimension Dimension
N
Mean
SD
Location Home Work Other
18 18 18
27.53 56.36 16.11
10.51 18.81 14.74
Social Environment Solitary Social
18 18
40.06 59.94
24.34 24.34
Behavior Nonsedentarya Heavy labor Light labor Moving about
6 18 18
45.68 6.43 13.41 33.50
14.66 5.87 7.31 16.04
Sedentaryb Desk work Conversing Reading Resting
16 17 18 8
54.32 16.80 22.45 13.01 7.40
14.66 10.35 16.88 9.55 5.33
a Heavy labor - - exercise, yard work; light l a b o r - - driving, housework, climbing two flights of stairs; moving about--combination of walking, standing, and sitting. b Desk w o r k - - paperwork, typing; c o n v e r s i n g - - talking and/or listening; reading--reading, watching TV, listening to stereo; resting--resting or sleeping.
The majority of subjects (77.8%) exhibited a greater percentage of inhibitory breathing at work than at home [Z2(1) = 5.55, p < .05]. However, due to large individual differences, the mean percentage of inhibitory breathing at work was not significantly greater than the mean percentage of inhibitory breathing at home [see Table III; t(17) = 0.96]. When subjects were at work, mean tidal volume during episodes of inhibitory breathing was not significantly different from mean tidal volume during episodes of non-inhibitory breathing [see Table IV; t(14) = 0.44]. Thus, mean minute ventilation during episodes of inhibitory breathing at work was 25% less than mean minute ventilation during episodes of noninhibitory breathing, which represented a significant decrease in minute ventilation [t(14) = 5.32, p < .01].
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Table II. Mean Percentages of Recorded Episodes by Location, Social Environment, and Behavior Dimension
N
Mean
SD
Home Solitary Nonsedentary Sedentary
9 12
0.07 0.13
0.07 0.08
Social Nonsedentary Sedentary
10 13
0.08 0.14
0.07 0.13
Work Solitary Nonsedentary Sedentary
12 11
0.08 0.13
0.07 0.10
Social Nonsedentary Sedentary
13 16
0.18 0.19
0.12 0.16
The majority of subjects (78.1%) also showed a greater percentage of episodes of inhibitory breathing in social situations than in solitary situations [X2(1) = 4.0, p _< .05]. In addition, the mean percentage of inhibitory breathing during social situations was 55% greater than the mean percentage of inhibitory breathing during solitary situations, which represented a significant increase in inhibitory breathing during social situations [see Table III; t(15) = 2.32, p < .05]. During social situations, tidal volume during episodes of inhibitory breathing was not significantly different than tidal volume during episodes of noninhibitory breathing [see Table IV; t(12) = 1.52]. Thus, in social situations, mean minute ventilation during episodes of inhibitory breathing was 32% tess than mean minute ventilation during episodes of noninhibitory breathing, representing a significant decrease in minute ventilation [t(12) = 5.10, p < .001]. It was hypothesized that the relationship between inhibitory breathing and social situations could have been due to the mechanics of talking. However, when subjects were in the presence of others, the percentage of episodes of inhibitory breathing during periods of conversing (M -- 27.23%, SD -- 25.64%) was not significantly different from the percentage of episodes of inhibitory breathing during periods when subjects were not conversing [M = 34.59%, SD -- 23.33%; t(16) = 1.03]. Although not significantly different, these means are in the opposite direc-
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582
Table III. M e a n Percentages of Inhibitory Breathing Within Environmental and Behavioral Dimensions Inhibition of Breathing Dimension
Mean
SD
Location Work Home
32.3 27.6
19.1 23.8
Social Environment Solitary Social
20.6 32.0
21.7 18.8
Behavior Sedentary Active
32.9 20.4
21.5 17.3
~
t
p
0.96 ~
ns
2.32 b
.04
2.84 ~
.01
17.
bar = 15.
tion than would be expected if inhibitory breathing episodes were due to the mechanics of talking. Neither mean tidal volume [t(16) = 0.46] nor mean minute ventilation [t(16) = 1.00] during episodes of inhibitory breathing when subjects were conversing was significantly different from tidal volume or minute ventilation during episodes of inhibitory breathing when they were not conversing. Further confirmation of the effect of social situations on inhibitory breathing was found in an analysis of subjects' home social environment. Subjects who spent at least part of their time at home with others had a significantly greater mean percentage of episodes of inhibitory breathing at home [N = 13, M = 34.17, SD = 6.97; t(16) = 2.76,p < .05] than subjects who spent all their time at home alone (N = 5, M = 11.46, SD = 9.75). A similar analysis of time spent at work was not feasible, since no subjects spent all of their time at work alone. Although 72% of the subjects showed a greater percentage of inhibitory breathing during sedentary behaviOr than during nonsedentary behavior, this frequency was not significant [X2(1) = 3.56, p > .05]. However, the mean percentage of inhibitory breathing during sedentary behavior was 61% greater than the mean percentage of inhibitory breathing during nonsedentary behavior [see Table III; t(17) = 2.84, p < .01]. During sedentary behavior, mean tidal volume during episodes of inhibitory breathing was not significantly different from mean tidal volume during episodes of noninhibitory breathing [see Table IV; t(14) = 0.59]. However, mean
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583
Table IV. Means (Standard Deviations) of Tidal Volume (Liters) and Minute Ventilation (Liters per Minute) by Type of Breathing Within Environmental and Behavioral Dimensions Breathing type Respiration measure Work environment Tidal volume Minute ventilation
Social environment Tidal volume Minute ventilation
Sedentary behavior Tidal volume Minute ventilation
Inhibitory
Other
t
p
0.53 (0.22)
0.54 (0.21)
0.44
ns
5.45 (2.15)
7.29 (2.71)
5.32
.0001
0.48 (0.19)
0.53 (0.22)
1.52
ns
4.97 (1.85)
7.28 (3.09)
5.10
.0003
0.49 (0.18)
0.51 (0.20)
0.59
ns
5.01 (1.56)
7.10 (2.70)
5.20
.0001
minute ventilation during episodes of inhibitory breathing during sedentary behavior was 29% less than mean minute ventilation during episodes of noninhibitory breathing, representing a significant decrease in minute ventilation [t(14) = 5.20, p < .01]. Positive It(17) = 0.87, p > .05] and negative [t(17) = 1.52, p > .05] moods during episodes of inhibitory breathing were not significantly different from moods during episodes of noninhibitory breathing. Similarly, no significant differences were found between appraisal ratings during episodes of inhibitory breathing and appraisal ratings during episodes of noninhibitory breathing.
DISCUSSION The present study extends previous work from our laboratory by identifying situations and behaviors in the natural environment that are
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ltaythornthwaite, Anderson, and Moore
associated with episodes of inhibitory breathing. Specifically, a greater percentage of inhibitory breathing was found in situations when other people were present and periods when subjects engaged in sedentary behaviors, which included desk work, reading, eating, and conversing. Most subjects exhibited a greater percentage of inhibitory breathing at work than at home. The importance of social stimuli was further emphasized in the finding that subjects who spent some time at home with other people had a greater percentage of inhibitory breathing at home than subjects who spent all of their time at home alone. Since many social interactions that occurred during the monitoring period were not associated with inhibitory breathing, there must have been something special about the social situations associated with these episodes. While much recent attention has been directed to the potential health benefits of social support (Cohen, 1988), other investigators have demonstrated the potentially harmful effects of certain types of social interactions in both animals (Henry and Grim, 1990) and humans (Long et al., 1982; Smith et al., 1989). These diverse results suggest that aspects of the social situation, such as the relationship between the subject and others in the environment, or the nature of their interactions, can determine the physiological response of the subject. The relationship between inhibitory breathing and social situations was not attributable to the mechanics of talking, since there was no significant relationship between conversing and inhibitory breathing. Unpublished data from our laboratory generated while subjects wore the ambulatory respiration monitor and read a neutral passage continuously for 10 min indicate that a slight, nonsignificant, reduction in breathing frequency (< .5 breath/min) occurs during continuous reading as compared to sitting quietly. Published laboratory studies of similar activity have yielded mixed findings, sometimes indicating an increase in frequency during reading (Guz et al., 1985) and sometimes demonstrating a decrease in frequency during continuous reading (Bunn and Mead, 1971). The latter study varied the complexity of pronunciation of the passages and found greater increases in ventilation when the passage included large volume consonants. Findings with minute ventilation have been more consistent, demonstrating that minute ventilation increases during continuous talking (Bunn and Mead, 1971; Guz et al., 1985). The significant decline in minute ventilation observed during episodes of inhibitory breathing that occurred in social situations further suggests that these episodes were not attributable to the mechanics of talking. Inhibitory breathing was more likely to occur when subjects were engaged in sedentary activities, such as desk work, eating, and reading, rather than more active behaviors, such as moving about, housework, climbing
Episodes of Inhibitory Breathing
585
stairs, and exercise. Although the direct effects of posture were not examined in the present study, recent data collected in our laboratory indicate that ambulatory tidal volume and minute ventilation are influenced by posture (sitting vs. standing), whereas breathing frequency is not (Anderson et al., 1992a). Episodes of inhibitory breathing were not associated with either an increase or a decrease in negative affect, such as anxiety, and neither positive mood nor appraisals were altered during episodes of inhibitory breathing. Clinical interventions targeting respiration have demonstrated that reductions in psychological distress, such as anxiety, occur when elevated respiration rates and minute ventilation are reduced to within the normal range (Grossman, 1983). In the present study, episodes of inhibitory breathing were operationalized as respiration rates below normal levels, and these episodes were not typically associated with a compensatory increase in tidal volume. Since previous work on respiration and mood has focused on either fast, shallow breathing or slow, deep breathing (Grossman, 1983), there is no precedent for predicting what mood changes, if any, might be associated with inhibitory breathing. The lack of relationship between inhibitory breathing and either mood or appraisal should not be interpreted as evidence that these episodes are not relevant to long-term physiological function and health. One recent study of cardiovascular reactivity found that subjective ratings of task difficulty and frustration were similar for blacks and whites, yet black subjects showed significantly greater heart rate reactivity (Ewart and Kolodner, 1991). This same study also found that females' higher ratings of demand were not accompanied by gender differences in heart rate or blood pressure reactivity. A longstanding challenge to psychophysiologists has been the relatively poor correlation across many studies between objective measures of physiological arousal (e.g., heart rate) and subjective ratings of emotion (Lang et al., 1972). Episodes of inhibitory breathing may represent one component of a multifaceted psychophysiological stress response. The criterion used to determine inhibitory breathing in this study was significantly below the average respiration rate observed during sleep (Stradling, 1985). Tidal volume was not significantly changed during these episodes, although minute ventilation was. Low frequency breathing requires more caloric expenditure by the lungs than high frequency breathing (Otis, 1964), and a recent study that combined ambulatory respiration and blood pressure monitoring indicated that episodes of inhibitory breathing were associated with elevations in blood pressure but not heart rate (Anderson et al., 1992a). The greater occurrence of breathing inhibition during sedentary behaviors is not inconsistent with this position, since short periods of
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Haythornthwaite, Anderson, and Moore
inhibitory breathing have been observed in response to a variety of challenging laboratory conditions, including aversive conditioning procedures (Obrist, 1968) and reaction time tasks (Obrist et al., 1969). Additionally, laboratory animals show long periods of inhibitory breathing, bradycardia, and resistance-mediated blood pressure elevations during the hours preceding an avoidance task (Anderson, 1981). Although inhibitory breathing has not been studied extensively in human psychophysiological studies, behavioral stimuli that activate the sympathetic nervous system have been demonstrated to have excitatory effects on ventilatory rate and volume (Allen et aL, 1986; Suess et al., 1980). Additional confirmation that episodes of inhibitory breathing represent an alternative psychophysiological response, potentially involving withdrawal or inhibition, that may be maladaptive awaits further delineation of the physiological concomitants of this response. These findings suggest a number of future directions for studies in both the laboratory and the natural environment. We have demonstrated that the prevalence of at least one episode of inhibitory breathing occurring during a day-long period of monitoring is very high across three samples [87% in the present study; 91-100% in others (Anderson et al., 1992a, 1992b)]. However, the rate of occurrence of episodes has been observed to vary widely among individuals (range: 0-78% of recording intervals). The results of the present study demonstrate that variability in environmental and behavioral factors may explain some of the variance across subjects in the rate of these episodes. Future work should address whether characteristics of the individual also predict this variability. Specific aspects of the social stimuli and the social interactions that are associated with inhibitory breathing need to be examined. In addition to the relationship of the person (or people) to the subject, it is also likely that the nature of the social interactions will be an important predictive factor. Further information is needed about environmental characteristics that evoke inhibitory breathing and about specific behaviors associated with inhibitory breathing. For example, previous research suggests that novel stimuli may evoke sustained inhibitory breathing (Naifeh and Kamiya, 1981; Suess et al., 1980). And finally, the physiological correlates of these episodes need to be further identified and, in turn, implicated in the pathogenesis of disease.
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Anderson, D. E. (1981). Inhibitory behavioral stress effects upon blood pressure regulation. In Weiss, S. M., Herd, J. A., and Fox, B. H. (eds.), Perspectives on Behavioral Medicine, Academic Press, New York, p. 307. Anderson, D. E., Austin, J., and Haythornthwaite, J. A. (1992a). Blood pressure concomitants of sustained inhibitory breathing in the natural environment. Psychophysiology (in press). Anderson, D. E., Coyle, K., and Haythornthwaite, J. A. (1992b). Episodes of inhibitory breathing in the natural environment. Psychophysiology (in press). Anderson, D. E., Dietz, J., and Murphy, P. (1987). Behavioral hypertension in sodium-loaded dogs is accompanied by sustained sodium retention. 3". Hypet'tens. 5: 99-105. Anderson, D. E., and Frank, L. B. (1990). A microprocessor system for ambulatory monitoring of respiration. J. Ambul. Monitor. 3: 11-20. Anderson, D. E., Kearns, W. D., and Better, W. E. (1983). Progressive hypertension in dogs by avoidance conditioning and saline infusion. Hypertension 5: 286-291. Bunn, J, C., and Mead, J. (1990). Control of ventilation during speech. J. Appl. Physiol. 31: 870-872. Cohen, S. (1988). Psychosocial models of the role of social support in the etiology of physical disease. Health Psychol. 7: 269-197. Daly, M., Angell-James, J. E., and Eisner, R. (1979). Role of carotid-body chemoreceptors and their reflex interactions in bradycardia and cardiac arrest. Lancet April 7: 764-767. Druz, W. S., and Sharp, J. T. (1981). Activity of respiratory muscles in upright and recumbent humans. Z AppL Physiol. Resp. Environ. Exercise Physiol. 51: 1552-1561. Ewart, C. K., and Kolodner, K. B. (1991). Social competence interview for assessing physiological reactivity in adolescents. Psychosom. Med. 53: 289-304. Grossman, P. (1983). Respiration, stress, and cardiovascular function. Psychophysiology 20: 284-299. Guyton, A. C. (1981). Teatbook of Medical Physiology. W. B. Saunders, Philadelphia. Guz, A., Macrae, K., Murphy, K., Shea, S., and Walter, J. (1986). The effect of opening the eyes and reading on resting ventilation in man. Z Physiol. 3: 101P. Hedges, S. M., Krantz, D. S., Contrada, R. J., and Rozanski, A. R. (1990). Development of a diary for use with ambulatory monitoring of mood, activities, and physiological function. J. Psychopathol. Behav. Assess. 12: 203-217. Henry, J. P., and Grim, C. E. (1990). Psychosocial mechanisms of primary hypertension. J. Hypertens. 8: 783-793. Hugelin, A., Virbet, J. F., Caille, D., and Foutz, A. S. (1985). Proceedings, Symposium on
Concepts and Formalizations in the Control of the BreathbTg, Solignac, France. Jeong, D. U., and Dimsdale, J. E. (1989). Sleep apnea and essential hypertension: A critical review of the epidemiological evidence for co-morbidity. Clin. Exp. Hypertens. 11(A): 1301-1323. Lang, P., Rice, D. G., and Sternbach, R. A. (1972). The psychophysiology of emotion. In Greenfield, N. S., and Sternbach, R. A. (eds.), Handbook of P~ychophysiology, Holt, Rienhart, and Winston, New York. Long, J. M., Lynch, J. J., Machiron, N. M., Thomas, S. A., and Malinow, K. L. (1982). The effect of status on blood pressure during verbal communication. Y Behav. Med. 5: 165-172. Naifeh, K. H., and Kamiya, J. (1981). The nature of respiratory changes associated with sleep onset. Sleep 4: 49-59. Obrist, P. A. (1968). Heart rate and somatic-motor coupling during classical aversive conditioning in humans. J. Expel'. Psychol. 77: 180-193. Obrist, P. A., Webb, R. A., and Sutterer, J. R. (1969). Heart rate and somatic changes during aversive conditioning and a simple reaction time task. Psychophysiology 5: 696-723. Otis, A. B. (1964). The work of breathing. In Fenn, W. O., and Rahn, H. (eds.), Handbook of Physiology, American Physiological Society, Washington, DC. Sharp, J, T., Goldberg, N. B., Druz, W. S., and Danon, J. (1975). Relative contributions of rib cage and abdomen to breathing in normal subjects. J. Appl. Physiol. 39: 608-618. Smith, T. W., Allred, K. D., Morrison, C. A., and Carlson, S. D. (1989). Cardiovascular reactivity and interpersonal influence: Active coping in a social context. J. Pers. Soc. Psychol. 56: 209-218.
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Sokolov, E. N. (1963). Perception and the Conditioned Reflex, Pergamon Press, Oxford. Spielberger, C. D., Gorsuch, R., Lushene, R., Vagg, P., and Jacobs, G. (1983a). Manual for the State-Trait Anxiety Inventory, Consulting Psychologists Press, Palo Alto, CA. Spielberger, C. D., Jacobs, G., Russell, S., and Crane, R. S. (1983b). Assessment of anger: The state-trait anger scale. In Butcher, J. N., and Spielberger, C. D. (eds.), Advances in Personality Assessment. Vol. 2. Lawrence Erlbaum Associates, Hillsdale, NJ. Stradling, J. R., Chadwick, G. A., and Frew, A. J. (1985). Changes in ventilation and it's components during sleep. Thorax 40: 364-370. Suess, W., Alexander, A., Smith, D., Sweeney, H., and Marion, R. (1980). The effects of psychological stress on respiration: A preliminary study of anxiety and hypertension. Psychophysiology 17: 535-540. Tilkian, A. G., Guilleminault, C., Schroeder, J. S., Lehrman, K. L., Simmons, F. B., and Dement, W. C. (1976). Hemodynamics in sleep-induced apnea: Studies during wakefulness and sleep. Ann. Intern. Med. 85: 714-719.
Social and Behavioral Factors Associated with Episodes of Inhibitory Breathing Jennifer A. Haythornthwaite] ,2 David E. Anderson, 1 and Lisa H. Moore 1 Accepted for publication: November 18, 1991
Previous research has shown that episodes of &hibitory breathing characterized by low-frequency breathing~ occur both in laboratory animals during intervals preceding avoidance tasks and in humans in the natural environment. The present study investigated social and behavioral factors accompanying episodes of inhibitory breathing that occur in the natural environment. Breathing frequency and tidal volume of ambulatory subjects were monitored via inductive plethysmography. Information concerning location, social environment, behavior, and mood was self-recorded in a computerized diary. The percentage of episodes of inhibitory breathing was found to be significantly greater in social situations than when subjects were alone. Additional analyses eliminated talking as an explanation for these effects. Inhibitory breathing was more frequent when subjects were sedentary rather than active, and inhibitory breathing was not associated with changes in mood or appraisal. Additional research is needed to determine the nature of the social interactions that elicit inhibitory breathing its physiological concomitants, and its long-term health implications. KEY WORDS: respiration; ambulatory monitoring; psychosocial factors; stress.
INTRODUCTION Inhibition of breathing has been observed in response to novel stimuli (Sokolov, 1963), aversive conditioning procedures (Obrist, 1968), and 1Laboratory of Behavioral Sciences, National Institute on Aging, 4940 Eastern Avenue, Baltimore, Maryland 21224. 2To whom correspondence should be addressed at Johns Hopkins University School of Medicine, 218 Meyer, 600 North Wolfe Street, Baltimore, Maryland 21287-7218. 573 0160-7715/92/1200-0573506.50/0 9 1992PlenumPublishingCorporation
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reaction time tasks (Obrist et al., 1969). The physiological concomitants of inhibitory breathing have been found to include increased peripheral resistance and increased blood flow to essential organs, such as the heart and brain (Daly et aL, 1979). Rather than reflecting a resting state, this pattern of physiological change, combined with the fact that oxygen cost and mechanical work are inversely related to breathing frequency at moderate levels of ventilation (Otis, 1964), suggests that inhibitory breathing may reflect a state of physiological arousal. Longer periods of inhibitory breathing have been observed to occur in dogs during the hours preceding the onset of regularly scheduled avoidance trials (Anderson, 1981). When combined with a high sodium diet, this preavoidance response potentiated the development of an experimental hypertension (Anderson et aL, 1983), although neither avoidance conditioning alone nor a high-sodium diet alone were effective. These findings suggest that breathing inhibition may reflect a central nervous system state which affects neuroendocrine regulation of sodium balance and vascular smooth muscle function (Anderson et aL, 1987). The clinical relevance of breathing patterns to hypertension has been further demonstrated through studies of sleep apnea. Epidemiological studies of sleep apnea suggest that approximately 34% of hypertensives experience clinically significant sleep apnea, as compared to less than 2% in the general population (Jeong and Dimsdale, 1989). Sleep apnea has been associated with acute elevations in blood pressure (Tilkian et aL, 1976), and hypertensive patients with obstructive sleep apnea experienced a decrease in daytime blood pressure following corrective surgery (Guilleminault et aL, 1981). Thus, breathing inhibition at night has been associated with long-term blood pressure regulation during the day. Our laboratory has previously demonstrated that episodes of inhibitory breathing occur in most human subjects in the natural environment. The development of an ambulatory respiration monitor (Anderson and Frank, 1990) has made possible the examination of inhibitory breathing while subjects engage in their usual daily activities. We have previously operationalized inhibitory breathing (Anderson et aL, 1992b) as a respiratory frequency of less than 12 breaths/min maintained for 10 rain. This criterion was derived from analysis of differences in ventilatory patterns in the natural environment during daytime and nighttime hours. Average tidal volume and minute ventilation were found to be significantly higher during daytime hours as compared to nighttime hours, although variability during these two periods was comparable (Anderson et aL, 1992b). While average breathing frequency was similar during daytime and nighttime periods, the variability of breathing frequency was greater during the day (Anderson
Episodes of Inhibitory Breathing
575
et al., 1992b). These findings suggest that variations in breathing frequency play a minor role relative to tidal volume in meeting metabolic oxygen demands associated with physical activity and that breathing frequency may be more sensitive to changes in behavioral conditions than tidal volume (Allen et aL, 1986; Hugelin et al., 1985). Our previous work also demonstrated that the mean for breathing frequency during nighttime hours was approximately 14 breaths/rain with a standard deviation of almost 2 breaths/rain (Anderson et al., 1992b). Consequently, the criterion of 12 breaths/rain was selected to be greater than one standard deviation below average sleeping levels of breathing frequency (Stradling, 1985). Episodes of inhibitory breathing identified using this criterion were found previously not to be accompanied by any consistent reduction in tidal volume (Anderson et aL, 1992b), providing further indication that these episodes were not simply reflecting a resting state. The previous study was the first to establish that these episodes occur in the natural environment, but information about the behavioral and environmental factors associated with breathing inhibition was not available. Therefore, the present study was designed to replicate the observation that most subjects demonstrate these episodes in the natural environment and to identify behavioral and environmental factors associated with these episodes. The specific hypotheses tested in the present study included (a) Are episodes of inhibitory breathing more likely to occur when subjects are at home or at work? (b) Are episodes of inhibitory breathing more likely to occur when subjects are alone or when they are in the presence of other people? (c) Are episodes of inhibitory breathing more likely to occur when subjects are engaged in sedentary behavior, such as desk work or reading, than when they are engaged in nonsedentary behavior, such as locomotor behavior or exercise? and (d) Is the subject's mood or appraisal of experiences during episodes of inhibitory breathing more negative or more positive compared to episodes of other types of breathing? A computerized diary was used to obtain information about these factors during 30-min intervals throughout the day. Subjects completed the diary while they wore a respiration monitor for approximately 12 waking hr.
METHOD Subjects Twenty-three adults, ranging in age from 20 to 57 years (M = 34.6, SD = 11.0), participated in the study. The group included 14 females and 9 males, 22 white and 1 black subjects. All denied a history of cardiovascular
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ttaythornthwaite, Anderson, and Moore
or respiratory disease, all were nonsmokers, and each performed within normal limits on a pulmonary function test. Body surface area, determined using the Dubois equation (Guyton, 1981), ranged from 1.45 to 2.10 (M = 1.8, SD = 0.2).
Apparatus Respiration bands (Ambulatory Monitoring, Inc, Ardsley, NY) were comprised of elasticized fabric, 4 in. wide, containing coils of insulated wire. The thoracic band was held in place under the arms with suspenders, and the abdominal band was held in place over the umbilicus with small adhesive strips which were fashioned with snaps that connected to the band. Bands were selected for each subject which were approximately 6-8 in. less than their thoracic and abdominal circumferences in order to maintain the slight tension necessary to record inductance changes. Depth and frequency of inspiration were recorded via inductance plethysmography in a small (3 • 10 x 19-cm), lightweight (270-g) microprocessor-based unit that was worn on a belt. The development and validation of this recording unit have been described previously (Anderson and Frank, 1990). The microprocessor contained two filters that eliminated artifactual changes due to postural shifts. One filter excluded all inductance changes occurring within 2 sec of the previously recorded breath. A second filter excluded inductance changes of more than approximately 3000 ml or less than approximately 150 ml, depending upon the calibration factor derived using the method described below. Depth of inspiration was measured as the summed change in inductance for both the thoracic and abdominal bands. Mean values of depth and frequency over 2-min intervals were stored in memory. A small light bulb on the recording unit could be activated by pressing a button, enabling subjects to periodically test the integrity of the recording system. Calibration of the recording unit was performed on a respiratory gas monitor (Ohmeda, Denver, CO) which determined tidal volume on a breath-by-breath basis while the subject wore a nose clip. The diary questionnaire, which collected information about the subject's environment and behavior, was administered using a small hand-held computer (MC-II, Corvallis Microtechnology, Inc, Corvallis, OR) that was programmed to signal subjects every 30 min. Questions were derived from diaries previously used in ambulatory monitoring studies and from standardized questionnaires and were adapted for use in the present study. The diary was designed to collect information on a variety of dimensions, while requiring only a few minutes to complete (usually less than 2 min). Ques-
Episodes of Inhibitory Breathing
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tions concerned the location of the subject (i.e., home, work, or other locations), whether they were with other people (i.e., alone vs, with other people), the behavior in which they were engaged (i.e., nonsedentary beh a v i o r - e x e r c i s e , housework, climbing stairs, moving about--vs, sedentary behavior--desk work, conversing, eating, reading, resting), posture (upright vs. reclining), mood (positive and negative), and general appraisal of the environment (the importance of events, amount of pressure experienced, how absorbed the subject was, and how undesirable events were). The seven mood items, adapted from the State-Trait Anger Scale (Spiel~ berger et al., 1983b) and the State-Trait Anxiety Scale (Spielberger et al., 1983a), and four appraisal items were rated on 4-point scales (1 = not at all to 4 = extremely) and were rated for the previous 30 min, whereas all other dimensions (e.g., location) were rated for three 10-min segments within the previous 30 min. Subjects carried the computer in a small camera bag adapted with a beeper that provided the signal to begin responding. The programming of the diary included the option for the subject to delay responding if circumstances required a delay (e.g., when driving an automobile). When a delay occurred, the subject was instructed to respond to the diary for the original recording interval unless the delay was 30 min or longer, in which case the subject was instructed to respond for the previous 30 min.
Procedure
Subjects were recruited by advertisement and screened for eligibility by telephone. A monitoring day was scheduled to ensure a typical activity pattern, which for most subjects occurred on a workday. Prior to monitoring, demographic data were obtained, the purpose of the study was explained, and informed consent was obtained. A pulmonary function test was administered which measured forced vital capacity and maximal voluntary ventilation. After fitting the subject with elasticized bands, calibration of the recording system was performed, involving simultaneous direct measurement of tidal volume (respiratory gas monitor) and indirect measurement of inspiratory depth (ambulatory respiration monitor) while the subject breathed into the gas sensor tube. Calibration was performed for 2 min in both upright and supine positions, since previous research has shown that upright ventilation is primarily thoracic and recumbent ventilation is primarily abdominal (Druz and Sharp, 1981; Sharp et al., 1975). The ratio of milliliters per breath recorded directly by the gas monitor to arbitrary inductance units recorded by the ambulatory monitor was calculated for each posture.
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Band size was selected so that calibration factors in the two positions were comparable, indicating that each band contributed proportionally to the summed inductance change per breath when subjects assumed a variety of postures during the monitoring period. Subjects were instructed in the use of the diary by displaying each of the questions on the computer screen and explaining alternative response choices. After this demonstration, subjects were asked to complete one diary recording session by themselves. The procedure for delaying responses was described, although subjects were encouraged to answer the diary in a timely fashion. Episodes of inhibitory breathing were operationalized as an average breathing frequency less than or equal to 12 breaths/min for 10 min (Anderson et al., 1992b). The data for 5 of the 23 subjects (2 females and 3 males, mean age = 30.6, SD = 14.3) were excluded because they contained an insufficient number of episodes of inhibitory breathing (fewer than six 10-min episodes) for comparative statistical analyses of the environmental and behavioral factors associated with inhibitory breathing. The final sample of 18 subjects (12 females and 6 males; 17 white and 1 black; mean age = 35.5, SD = 9.9) was studied for an average of 12.8 hr, ranging from 10 to 14.5 hr. Respiration data were edited to exclude rare disconnections (revealed on the record as an average ventilatory frequency of zero). After removing these intervals and removing 2-min intervals not associated with a diary report, an average of 12.3 hr per subject was available for analysis (range of 9.8 to 14.0 hr). Ventilatory frequency and tidal volume data were averaged over 10 min recording intervals to coincide with the diary records, yielding an average of 73.8 10-min intervals for the sample, ranging from 59 to 84. Response to the computerized diary was good, with subjects requiring only a few minutes to complete the items. Only 1% of responses were missed and only 2% were delayed across the 30-rain recording intervals.
Data Analysis Data from each of the primary dimensions (location, social environment, activity, mood, and appraisal) were analyzed independently of the other dimensions by combining across levels of the other dimensions. Because 96% of the intervals were recorded in the upright position, the information on posture (upright vs. lying down), which was collected for the purpose of calibrating the respiratory units, was not analyzed. However, the analysis of sedentary vs. nonsedentary behaviors allowed an indirect
Episodes of Inhibitory Breathing
579
assessment of other postural effects, since the behaviors classified as sedentary primarily involved sitting postures, whereas the behaviors classified as nonsedentary involved primarily standing postures. Percentages, rather than absolute frequencies, were used as the unit of analysis since they control for individual differences in the time spent in different environments and activities. Two analytic strategies were used. First, the difference between the percentages for the two elements within each dimension (e.g., location: home vs. work) was categorized and chisquare analyses were performed. This analysis described the consistency of an effect across the 18 subjects within the sample. Second, the significance of the difference in mean percentage between categories was compared using paired t tests. This second analysis quantified the magnitude of the differences between categories. Two subjects were excluded from the analysis of social situations, since they reported fewer than six 10-min intervals of being alone. In order to determine whether compensatory increases in tidal volume occurred during episodes of inhibitory breathing, mean tidal volume and minute ventilation during episodes of inhibitory breathing were calculated within each category and compared using paired t tests. The mood items were combined into positive (calm, pleasant, relaxed) and negative (tense, nervous, strained, irritated) mood scales. Scores on each mood scale and the four appraisal scales (absorbed, importance, pressure, and undesirable) were standardized within subjects. This method compensated for individual differences in the use of the mood and appraisal scales (Hedges et al., 1991). The means for each scale were computed for episodes of inhibitory breathing and episodes of all other breathing and then were analyzed via paired t tests.
RESULTS Across the recording period, mean ventilatory frequency for the 18 subjects was 13.2 breaths/min (SD = 1.1), mean tidal volume was 0.54 liter/breath (SD = 0.2), and mean minute ventilation was 7.07 liters/min (SD = 2.5). The median percent of respiratory episodes classified as inhibitory breathing (ventilatory frequency less than or equal to 12 breaths/ min) was 27%. Mean percentages of recording each category within the three dimensions from the diary are presented in Table I. Although these dimensions were not mutually exclusive (i.e., social situations could occur both at home and at work), analyses were conducted on single dimensions while collapsing across the other dimensions due to the varying numbers of subjects represented in each cells (see Table II).
tlaythornthwaite, Anderson, and Moore
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Table I. Mean Percentages of Recorded Episodes Within Each Environmental and Behavioral Dimension Dimension
N
Mean
SD
Location Home Work Other
18 18 18
27.53 56.36 16.11
10.51 18.81 14.74
Social Environment Solitary Social
18 18
40.06 59.94
24.34 24.34
Behavior Nonsedentarya Heavy labor Light labor Moving about
6 18 18
45.68 6.43 13.41 33.50
14.66 5.87 7.31 16.04
Sedentaryb Desk work Conversing Reading Resting
16 17 18 8
54.32 16.80 22.45 13.01 7.40
14.66 10.35 16.88 9.55 5.33
a Heavy labor - - exercise, yard work; light l a b o r - - driving, housework, climbing two flights of stairs; moving about--combination of walking, standing, and sitting. b Desk w o r k - - paperwork, typing; c o n v e r s i n g - - talking and/or listening; reading--reading, watching TV, listening to stereo; resting--resting or sleeping.
The majority of subjects (77.8%) exhibited a greater percentage of inhibitory breathing at work than at home [Z2(1) = 5.55, p < .05]. However, due to large individual differences, the mean percentage of inhibitory breathing at work was not significantly greater than the mean percentage of inhibitory breathing at home [see Table III; t(17) = 0.96]. When subjects were at work, mean tidal volume during episodes of inhibitory breathing was not significantly different from mean tidal volume during episodes of non-inhibitory breathing [see Table IV; t(14) = 0.44]. Thus, mean minute ventilation during episodes of inhibitory breathing at work was 25% less than mean minute ventilation during episodes of noninhibitory breathing, which represented a significant decrease in minute ventilation [t(14) = 5.32, p < .01].
Episodes of Inhibitory Breathing
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Table II. Mean Percentages of Recorded Episodes by Location, Social Environment, and Behavior Dimension
N
Mean
SD
Home Solitary Nonsedentary Sedentary
9 12
0.07 0.13
0.07 0.08
Social Nonsedentary Sedentary
10 13
0.08 0.14
0.07 0.13
Work Solitary Nonsedentary Sedentary
12 11
0.08 0.13
0.07 0.10
Social Nonsedentary Sedentary
13 16
0.18 0.19
0.12 0.16
The majority of subjects (78.1%) also showed a greater percentage of episodes of inhibitory breathing in social situations than in solitary situations [X2(1) = 4.0, p _< .05]. In addition, the mean percentage of inhibitory breathing during social situations was 55% greater than the mean percentage of inhibitory breathing during solitary situations, which represented a significant increase in inhibitory breathing during social situations [see Table III; t(15) = 2.32, p < .05]. During social situations, tidal volume during episodes of inhibitory breathing was not significantly different than tidal volume during episodes of noninhibitory breathing [see Table IV; t(12) = 1.52]. Thus, in social situations, mean minute ventilation during episodes of inhibitory breathing was 32% tess than mean minute ventilation during episodes of noninhibitory breathing, representing a significant decrease in minute ventilation [t(12) = 5.10, p < .001]. It was hypothesized that the relationship between inhibitory breathing and social situations could have been due to the mechanics of talking. However, when subjects were in the presence of others, the percentage of episodes of inhibitory breathing during periods of conversing (M -- 27.23%, SD -- 25.64%) was not significantly different from the percentage of episodes of inhibitory breathing during periods when subjects were not conversing [M = 34.59%, SD -- 23.33%; t(16) = 1.03]. Although not significantly different, these means are in the opposite direc-
Haythornthwaite, Anderson, and Moore
582
Table III. M e a n Percentages of Inhibitory Breathing Within Environmental and Behavioral Dimensions Inhibition of Breathing Dimension
Mean
SD
Location Work Home
32.3 27.6
19.1 23.8
Social Environment Solitary Social
20.6 32.0
21.7 18.8
Behavior Sedentary Active
32.9 20.4
21.5 17.3
~
t
p
0.96 ~
ns
2.32 b
.04
2.84 ~
.01
17.
bar = 15.
tion than would be expected if inhibitory breathing episodes were due to the mechanics of talking. Neither mean tidal volume [t(16) = 0.46] nor mean minute ventilation [t(16) = 1.00] during episodes of inhibitory breathing when subjects were conversing was significantly different from tidal volume or minute ventilation during episodes of inhibitory breathing when they were not conversing. Further confirmation of the effect of social situations on inhibitory breathing was found in an analysis of subjects' home social environment. Subjects who spent at least part of their time at home with others had a significantly greater mean percentage of episodes of inhibitory breathing at home [N = 13, M = 34.17, SD = 6.97; t(16) = 2.76,p < .05] than subjects who spent all their time at home alone (N = 5, M = 11.46, SD = 9.75). A similar analysis of time spent at work was not feasible, since no subjects spent all of their time at work alone. Although 72% of the subjects showed a greater percentage of inhibitory breathing during sedentary behaviOr than during nonsedentary behavior, this frequency was not significant [X2(1) = 3.56, p > .05]. However, the mean percentage of inhibitory breathing during sedentary behavior was 61% greater than the mean percentage of inhibitory breathing during nonsedentary behavior [see Table III; t(17) = 2.84, p < .01]. During sedentary behavior, mean tidal volume during episodes of inhibitory breathing was not significantly different from mean tidal volume during episodes of noninhibitory breathing [see Table IV; t(14) = 0.59]. However, mean
Episodes of Inhibitory Breathing
583
Table IV. Means (Standard Deviations) of Tidal Volume (Liters) and Minute Ventilation (Liters per Minute) by Type of Breathing Within Environmental and Behavioral Dimensions Breathing type Respiration measure Work environment Tidal volume Minute ventilation
Social environment Tidal volume Minute ventilation
Sedentary behavior Tidal volume Minute ventilation
Inhibitory
Other
t
p
0.53 (0.22)
0.54 (0.21)
0.44
ns
5.45 (2.15)
7.29 (2.71)
5.32
.0001
0.48 (0.19)
0.53 (0.22)
1.52
ns
4.97 (1.85)
7.28 (3.09)
5.10
.0003
0.49 (0.18)
0.51 (0.20)
0.59
ns
5.01 (1.56)
7.10 (2.70)
5.20
.0001
minute ventilation during episodes of inhibitory breathing during sedentary behavior was 29% less than mean minute ventilation during episodes of noninhibitory breathing, representing a significant decrease in minute ventilation [t(14) = 5.20, p < .01]. Positive It(17) = 0.87, p > .05] and negative [t(17) = 1.52, p > .05] moods during episodes of inhibitory breathing were not significantly different from moods during episodes of noninhibitory breathing. Similarly, no significant differences were found between appraisal ratings during episodes of inhibitory breathing and appraisal ratings during episodes of noninhibitory breathing.
DISCUSSION The present study extends previous work from our laboratory by identifying situations and behaviors in the natural environment that are
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ltaythornthwaite, Anderson, and Moore
associated with episodes of inhibitory breathing. Specifically, a greater percentage of inhibitory breathing was found in situations when other people were present and periods when subjects engaged in sedentary behaviors, which included desk work, reading, eating, and conversing. Most subjects exhibited a greater percentage of inhibitory breathing at work than at home. The importance of social stimuli was further emphasized in the finding that subjects who spent some time at home with other people had a greater percentage of inhibitory breathing at home than subjects who spent all of their time at home alone. Since many social interactions that occurred during the monitoring period were not associated with inhibitory breathing, there must have been something special about the social situations associated with these episodes. While much recent attention has been directed to the potential health benefits of social support (Cohen, 1988), other investigators have demonstrated the potentially harmful effects of certain types of social interactions in both animals (Henry and Grim, 1990) and humans (Long et al., 1982; Smith et al., 1989). These diverse results suggest that aspects of the social situation, such as the relationship between the subject and others in the environment, or the nature of their interactions, can determine the physiological response of the subject. The relationship between inhibitory breathing and social situations was not attributable to the mechanics of talking, since there was no significant relationship between conversing and inhibitory breathing. Unpublished data from our laboratory generated while subjects wore the ambulatory respiration monitor and read a neutral passage continuously for 10 min indicate that a slight, nonsignificant, reduction in breathing frequency (< .5 breath/min) occurs during continuous reading as compared to sitting quietly. Published laboratory studies of similar activity have yielded mixed findings, sometimes indicating an increase in frequency during reading (Guz et al., 1985) and sometimes demonstrating a decrease in frequency during continuous reading (Bunn and Mead, 1971). The latter study varied the complexity of pronunciation of the passages and found greater increases in ventilation when the passage included large volume consonants. Findings with minute ventilation have been more consistent, demonstrating that minute ventilation increases during continuous talking (Bunn and Mead, 1971; Guz et al., 1985). The significant decline in minute ventilation observed during episodes of inhibitory breathing that occurred in social situations further suggests that these episodes were not attributable to the mechanics of talking. Inhibitory breathing was more likely to occur when subjects were engaged in sedentary activities, such as desk work, eating, and reading, rather than more active behaviors, such as moving about, housework, climbing
Episodes of Inhibitory Breathing
585
stairs, and exercise. Although the direct effects of posture were not examined in the present study, recent data collected in our laboratory indicate that ambulatory tidal volume and minute ventilation are influenced by posture (sitting vs. standing), whereas breathing frequency is not (Anderson et al., 1992a). Episodes of inhibitory breathing were not associated with either an increase or a decrease in negative affect, such as anxiety, and neither positive mood nor appraisals were altered during episodes of inhibitory breathing. Clinical interventions targeting respiration have demonstrated that reductions in psychological distress, such as anxiety, occur when elevated respiration rates and minute ventilation are reduced to within the normal range (Grossman, 1983). In the present study, episodes of inhibitory breathing were operationalized as respiration rates below normal levels, and these episodes were not typically associated with a compensatory increase in tidal volume. Since previous work on respiration and mood has focused on either fast, shallow breathing or slow, deep breathing (Grossman, 1983), there is no precedent for predicting what mood changes, if any, might be associated with inhibitory breathing. The lack of relationship between inhibitory breathing and either mood or appraisal should not be interpreted as evidence that these episodes are not relevant to long-term physiological function and health. One recent study of cardiovascular reactivity found that subjective ratings of task difficulty and frustration were similar for blacks and whites, yet black subjects showed significantly greater heart rate reactivity (Ewart and Kolodner, 1991). This same study also found that females' higher ratings of demand were not accompanied by gender differences in heart rate or blood pressure reactivity. A longstanding challenge to psychophysiologists has been the relatively poor correlation across many studies between objective measures of physiological arousal (e.g., heart rate) and subjective ratings of emotion (Lang et al., 1972). Episodes of inhibitory breathing may represent one component of a multifaceted psychophysiological stress response. The criterion used to determine inhibitory breathing in this study was significantly below the average respiration rate observed during sleep (Stradling, 1985). Tidal volume was not significantly changed during these episodes, although minute ventilation was. Low frequency breathing requires more caloric expenditure by the lungs than high frequency breathing (Otis, 1964), and a recent study that combined ambulatory respiration and blood pressure monitoring indicated that episodes of inhibitory breathing were associated with elevations in blood pressure but not heart rate (Anderson et al., 1992a). The greater occurrence of breathing inhibition during sedentary behaviors is not inconsistent with this position, since short periods of
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inhibitory breathing have been observed in response to a variety of challenging laboratory conditions, including aversive conditioning procedures (Obrist, 1968) and reaction time tasks (Obrist et al., 1969). Additionally, laboratory animals show long periods of inhibitory breathing, bradycardia, and resistance-mediated blood pressure elevations during the hours preceding an avoidance task (Anderson, 1981). Although inhibitory breathing has not been studied extensively in human psychophysiological studies, behavioral stimuli that activate the sympathetic nervous system have been demonstrated to have excitatory effects on ventilatory rate and volume (Allen et aL, 1986; Suess et al., 1980). Additional confirmation that episodes of inhibitory breathing represent an alternative psychophysiological response, potentially involving withdrawal or inhibition, that may be maladaptive awaits further delineation of the physiological concomitants of this response. These findings suggest a number of future directions for studies in both the laboratory and the natural environment. We have demonstrated that the prevalence of at least one episode of inhibitory breathing occurring during a day-long period of monitoring is very high across three samples [87% in the present study; 91-100% in others (Anderson et al., 1992a, 1992b)]. However, the rate of occurrence of episodes has been observed to vary widely among individuals (range: 0-78% of recording intervals). The results of the present study demonstrate that variability in environmental and behavioral factors may explain some of the variance across subjects in the rate of these episodes. Future work should address whether characteristics of the individual also predict this variability. Specific aspects of the social stimuli and the social interactions that are associated with inhibitory breathing need to be examined. In addition to the relationship of the person (or people) to the subject, it is also likely that the nature of the social interactions will be an important predictive factor. Further information is needed about environmental characteristics that evoke inhibitory breathing and about specific behaviors associated with inhibitory breathing. For example, previous research suggests that novel stimuli may evoke sustained inhibitory breathing (Naifeh and Kamiya, 1981; Suess et al., 1980). And finally, the physiological correlates of these episodes need to be further identified and, in turn, implicated in the pathogenesis of disease.
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