J Physiol Sci (2018) 68:369–376 https://doi.org/10.1007/s12576-017-0539-7 ORIGINAL PAPER Relationships between trait and respiratory parameters during quiet breathing in normal subjects 1 1 1 • • Akae Kato Koki Takahashi Ikuo Homma Received: 29 September 2016 / Accepted: 11 April 2017 / Published online: 2 May 2017 The Author(s) 2017. This article is an open access publication Abstract Respiratory patterns are inﬂuenced and altered Introduction by various emotional changes. In the present study, we investigated how respiratory patterns differ from individual It is well known that the main function of breathing is to to individual during quiet breathing. We examined the inhale oxygen and expire carbon dioxide for maintaining State-Trait Anxiety Inventory and various respiratory life. The breathing of this function is called metabolic parameters in 16 healthy male subjects. Tidal volume was breathing and is generated in the respiratory center located signiﬁcantly larger and respiratory rate (RR) was signiﬁ- in the brainstem, particularly in the medulla and pons. cantly higher in both the higher trait (HT) and higher state However, in addition to metabolic breathing, the so-called (HS) anxiety groups compared to the lower trait and lower behavioral breathing is generated in the upper center in the state anxiety groups. Inspiratory (T ) and expiratory time brain. Behavioral breathing is generated by various internal (T ) was signiﬁcantly shorter in both the HT and HS or external environmental changes. A subtype of behav- anxiety groups. There was no signiﬁcant difference in ioral breathing, which is inﬂuenced by various emotions, minute ventilation between these two groups. End-tidal has recently been investigated and has been termed, ‘‘emotional breathing’’ . Therefore, autonomic breathing CO %, heart rate, and oxygen uptake (VO =W) also 2 2 output generated by the combination of tidal activity and showed no signiﬁcant differences. V showed a negative respiratory rhythm is not only controlled by metabolic correlation and RR showed a positive correlation with trait demands but also controlled by constantly responding scores. T and T showed a negative correlation with trait I E changes of emotions, such as fear, anxiety, sadness, and anxiety scores. However, no other respiratory parameter happiness. It is interesting that maintenance of both showed any correlation. These results suggest that the homeostasis and emotions coexist in the breathing pattern. respiratory rhythm reﬂected by RR is affected by the The center for emotional breathing may be in the limbic activity generated in the higher center in accordance with system, especially in the amygdala, which is well known as the level of trait anxiety during quiet breathing in awake the primary center for emotions [2, 3]. It has been shown in humans. an animal experiment that spontaneous burst activities recorded in the amygdala are functionally coupled to Keywords STAI Respiratory rate Trait anxiety Quiet medullary respiratory rhythm in the limbic-brainstem- breathing spinal cord preparation of a newborn rat. Electrical stim- ulation applied to the amygdala induces an inspiratory burst in the root of the phrenic nerve . Spontaneous respiratory rhythmic activities are increased by the local & Ikuo Homma application of CRF (corticotrophin releasing factor) in the email@example.com preparation . CRF is well known to integrate the global mammalian stress response [6, 7]. The relationship of Department of Judo Therapy, Tokyo Ariake University of respiratory activity and emotion has been shown in a study Medical and Health Sciences, 2-9-1 Ariake Koto-ku, on anticipatory anxiety ; the subject’s respiratory rate Tokyo 135-0063, Japan 123 370 J Physiol Sci (2018) 68:369–376 increased during the feeling of anticipatory anxiety. In an quiet for 3 min, respiratory rate per minute (RR), minute earlier study, the changes in respiratory rate were found to _ ventilation (V ), tidal volume (V ), inspiratory time (T ), E T I be positively correlated with individual trait anxiety scores, expiratory time (T ), end-tidal CO % (FetCO ) and oxygen E 2 2 and the amygdala was examined to determine the source consumption per weight (VO =W) was measured breath by generating the activity using a neuroimaging method dur- breath for 5 min. All respiratory data with heart rate (HR) ing a time of anticipatory anxiety experienced by the were stored on a laptop computer. The room temperature subject . was maintained at 22.5 ± 1 C. Concomitant changes in breathing patterns and emotions have been shown in studies of odor stimulation and in the Psychological measurements performance of Ikebana, the Japanese traditional art of ﬂower arrangement. Unpleasant odor stimulation increased The anxiety level of each subject was accessed using the respiratory rate and state anxiety scores, whereas they Spielberger’s State-Trait Anxiety Inventory (STAI) . were decreased by pleasant odor stimulation . Subjects The instrument comprises two scales, one for measuring showed a decrease in the state anxiety score and respiratory Trait, and one for measuring State anxiety level. Each scale rate after performing Ikebana. The effects were more sig- has 20 statements and anxiety levels for subjects are indi- niﬁcant in subjects with a high trait anxiety . Several cated by scores rating from 20 to 80. The trait anxiety score previous studies have examined breathing patterns not only evaluates how people feel generally, while the state anxiety in normal subjects but also in subjects with anxiety disor- score evaluates how people feel ‘right now’ in various situ- ders and found that the breathing patterns were linked to ations. Trait score is generally stable, while state score psychosomatic complains [12, 13]. changes depending on the situation . Trait scores of more A previous study of Masaoka and Homma (1997) than 44 indicate a high trait anxiety, and scores of less than 43 showed that mental stimulation decreases expiratory time reﬂect normal or low trait anxiety in men. State scores of and increases minute ventilation. They also found a nega- more than 41 indicate high state anxiety, and scores of less tive correlation between expiratory time and anxiety scores than 40 reﬂect normal or low trait anxiety in men. In this during the mental stimulation . study, subjects were asked to assess their anxiety level using It is interesting to consider whether these two parame- STAI before the start of physiological measurements. ters, breathing pattern and anxiety scores, have a close Subjects were divided into two groups based on trait relationship and also whether that relationship is different anxiety according to Spielberger’s State-Trait Anxiety in different individuals during quiet breathing. The present Inventory (STAI): higher trait anxiety (HT) group and study measured and compared breathing patterns and trait lower trait anxiety (LT) group. Trait anxiety score of the anxiety scores during quiet breathing in normal young HT subjects was greater than 44 and the score in the LT adult males. subjects was less than 43. Subjects were also divided into two groups according to state anxiety: higher state anxiety (HS) group (more than 41) and lower state anxiety (LS) Methods group (less than 40). Subjects Data analysis Sixteen healthy male subjects aged from 19 to 23 years All statistical analyses were performed with commercially (20.8 ± 1.1 mean ± SD) participated in this study. No available statistical package (JMP Pro13.0.0; SAS Institute subjects had a psychiatric, neurological or pulmonary dis- order. All subjects provided written informed consent, and Inc., Cary, NC, USA). Comparisons of all respiratory parameters with HR between HT and LT groups and the study was approved by the Ethics Committee of Tokyo Ariake University of Medical and Health Sciences. between HS and LS were analyzed using unpaired t test and non-parametric unpaired Mann–Whitney test. As the Procedure and measurements results were similar, the latter results are presented. Continuous valuables of the trait and state anxiety Subjects sat on a chair wearing a facemask with a trans- scores, which were not normally distributed, are shown as median and interquartile ranges. A p value of \0.05 was ducer connected to a respiratory monitor (AE-100i, Minato considered statistically signiﬁcant. Spearman’s nonpara- Medical Co., Ltd., Osaka) for measuring respiratory pattern metric correlation coefﬁcients (q) were used to evaluate and metabolism in a quiet room. Heart rate was also whether the trait or state anxiety score was correlated with measured by a pulse oximeter (BSM-2401, NIHON KOHDEN Co., Ltd., Tokyo). After the subjects remained any of the various respiratory parameters. 123 J Physiol Sci (2018) 68:369–376 371 correlated with trait anxiety scores (Fig. 4a, c). There was Results no signiﬁcant correlation between trait anxiety scores and STAI (Trait and State Anxiety) HR or VO =W (Fig. 5a, c). V and T were negatively 2 T E and RR was positively correlated with state anxiety scores Trait and state anxiety scores with the age of each subject _ (Table 2). Correlations between HR or VO =W and state is shown in Table 1. Trait anxiety scores varied from 31 to anxiety scores were also examined. Neither parameter 63 and the median score and interquartile range was 48.0 showed a signiﬁcant correlation with state anxiety scores (35.0–54.8) (median, 25th–75th percentiles). State anxiety (Table 2). scores also varied from 31 to 65 and the median score was 38.5 (34.0–43.8). Scores of the trait and state anxiety score were relatively similar for each subject and a positive Comparisons of respiratory parameters, HR correlation was observed between trait and state anxiety _ and VO =W in HT, LT and HS, LS groups scores (p \ 0.01) (Fig. 1a). The median of the state scores was 44.0 (41.0–52.0) and 34.0 (33.0–36.0) in HT and LT, The median of FetCO (%) was 5.11 (5.01–5.39) in HT and respectively (Fig. 1b). The state scores were signiﬁcantly 5.36 (5.22–5.42) in LT (Fig. 2d). There was no signiﬁcant higher in HT subjects (p = 0.019). difference in FetCO (%) (p = 0.397). The mean of V was 2 E Relationships between respiratory parameters, HR and 9.3 (8.81–9.88) L/min in HT and 8.39 (7.41–9.32) L/min in VO =W with trait and state anxiety 2 _ LT (Fig. 2b). There was no signiﬁcant difference in V The relationships between the various respiratory (p = 0.081). The median of V was 536.95 (493.78– _ _ parameters, FetCO , V , V , RR, T , T ,or VO =W and E 2 2 T I E 584.15) ml in HT and 699.15 (585.68–803.07) ml in LT STAI scores were examined. There was no signiﬁcant subjects (Fig. 3b). The V was signiﬁcantly larger in LT correlation between FetCO (%) and trait anxiety scores 2 subjects (p = 0.011). The median RR was 16.92 (Fig. 2c). There was no signiﬁcant correlation between V E (16.25–18.75) n/min in HT and 12.06 (8.23–16.09) n/min in and trait anxiety scores (Fig. 2a). V is determined by the LT subjects (Fig. 3d). The RR was signiﬁcantly higher in HT combination of RR and V . V was negatively and RR subjects (p = 0.005). The median of T and T were I E T T was positively correlated with trait anxiety scores 1.38 (1.29–1.59) and 2.15 (1.82–2.27) s in HT and 2.23 (1.59–3.02) and 2.71 (2.22-4.54) s in LT subjects, respec- (Fig. 3a, c). RR is based on inspiratory time (T ) and expiratory time (T ). T and T were also negatively tively (Fig. 4b, d). T and T were signiﬁcantly shorter in HT E I E I E subjects (p = 0.008 for T and p = 0.015 for T ). The I E median of VO =W was 3.82 (3.41–4.16) ml/W in HT and Table 1 STAI scores with the age of each subject 3.61 (3.28–4.19) ml/W in LT subjects (Fig. 5b). There was Subject (No.) Age (year) STAI no signiﬁcant difference in VO =W (p = 0.459). The med- Trait State ian of HR was 67.71 (60.00–83.75) beat/min in HT and 73.10 (62.77–78.54) beat/min in LT subjects (Fig. 5d). There was 120 63 65 also no signiﬁcant difference in HR between the two groups 221 54 52 (p = 1.000). There were also no signiﬁcant differences in 323 35 34 _ _ V , FetCO (%), VO =W and HR in higher state anxiety (HS) E 2 2 422 59 44 and lower state anxiety (LS) groups (Table 2). 520 55 43 621 51 41 721 32 34 Discussion 821 45 33 921 52 41 Trait and state anxiety scores were distributed from low to 10 20 60 34 high among subjects. Trait anxiety score is generally 11 20 41 31 unchangeable, but state anxiety score is changeable. As 12 23 35 34 state anxiety is measured according to how the subject feels 13 21 35 39 ‘right now’ in various situations, it is affected by various 14 20 53 49 environments and mental factors. On the other hand, trait 15 20 40 33 anxiety represents the subjective feeling in general . 16 19 31 38 However, both anxiety scores were closely related and the 20.8 ± 1.1 48.0 (35.0–54.8) 38.5 (34.0–43.8) median state anxiety score of the HT group was signiﬁ- Mean ± SD Median (25th–75th percentiles) cantly higher than that of the LT group in this study. A 123 372 J Physiol Sci (2018) 68:369–376 Fig. 1 The relationship between state and trait anxieties. a Linear in LT (*p \ 0.05). Median state anxiety in HT and LT were indicated plot of state and trait scores in normal subjects. A signiﬁcant positive with horizontal bars. The vertical bars indicate the range and the correlation was observed (q = 0.580, p \ 0.01). b Comparison of horizontal boundaries of the boxes represent the ﬁrst and third state scores in the high trait anxiety group (HT) and in the low trait quartiles anxiety group (LT). State scores were signiﬁcantly higher in HT than Fig. 2 The relationships between minute ventilation (V ), end-tidal CO % (FetCO ), E 2 2 and trait anxiety. a Linear plot of V and trait scores. No signiﬁcant correlation was observed (q = 0.384). b Comparison of V in HT and in LT. No signiﬁcant difference was observed in V . c Linear plot of FetCO and trait scores. No signiﬁcant correlation was observed (q =-0.038). d Comparison of FetCO in HT and in LT. No signiﬁcant difference was observed in FetCO . Median V and FetCO 2 E 2 in HT and LT were indicated with horizontal bars. The vertical bars indicate the range and the horizontal boundaries of the boxes represent the ﬁrst and third quartiles positive correlation was also obtained between trait and change. HR and VO =W are also changed by metabolic state anxiety scores. _ demands. There were no differences in V , HR and VO =W between the higher and lower trait anxiety groups Relationships between respiratory parameters (HT and LT) and between the higher state and lower state and STAI anxiety groups (HS and LS) (Figs. 2b, 5b, d; Table 2). There were also no signiﬁcant correlations between these It is generally agreed that breathing patterns are generated parameters and trait or state anxiety scores. This indicates in the brainstem under metabolic demands. Minute venti- that parameters changing with metabolic demands are lation (V ) reﬂects the volume demand from the metabolic independent of trait or state anxiety. Contrary to the so- 123 J Physiol Sci (2018) 68:369–376 373 Fig. 3 The relationships between tidal volume (V ), respiratory rate (RR) and trait anxiety. a Linear plot of V and trait scores. A signiﬁcant negative correlation was observed (q =-0.687, p \ 0.01). b Comparison of V in HT and in LT. V in LT was signiﬁcantly larger than in HT (*p \ 0.05). c Linear plot of RR and trait scores. A signiﬁcant positive correlation was observed in RR (q = 0.749, p \ 0.05). d Comparison of RR in HT and in LT. RR in HT was signiﬁcantly higher than in LT (**p \ 0.01). Median V and RR in HT and LT were indicated with horizontal bars. The vertical bars indicate the range and the horizontal boundaries of the boxes represent the ﬁrst and third quartiles Fig. 4 The relationship between inspiratory time (T ), expiratory time (T ), and trait anxiety. a Linear plot of T and trait scores. A signiﬁcant negative correlation was observed in T (q =-0.622, p \ 0.05). b Comparison of T in HT and in LT. T in HT was signiﬁcantly shorter than in LT (**p \ 0.01). c Linear plot of T and trait scores. A signiﬁcant negative correlation was observed (q =-0.631, p \ 0.05). d Comparison of T in HT and in LT. T in HT was signiﬁcantly shorter than in LT (*p \ 0.05). Median T and T I E in HT and LT were indicated with horizontal bars. The vertical bars indicate the range and the horizontal boundaries of the boxes represent the ﬁrst and third quartiles 123 374 J Physiol Sci (2018) 68:369–376 Fig. 5 The relationship between oxygen uptake (VO =W), heart rate (HR), and trait anxiety. a Linear plot of VO =W and trait scores. No signiﬁcant correlation was observed (q = 0.209). b Comparison of VO =W in HT and in LT. No signiﬁcant difference was observed in VO =W. c Linear plots of HR and trait scores. No signiﬁcant correlation was observed (q =-0.047). d Comparison of HR in HT and in LT. No signiﬁcant difference was observed in HR. Median VO =W and HR in HT and LT were indicated with horizontal bars. The vertical bars indicate the range and the horizontal boundaries of the boxes represent the ﬁrst and third quartiles called ‘‘metabolic breathing’’, we have so-called ‘‘behav- respiratory rate and the values of trait anxiety score ioral breathing’’ in which our breathing is inﬂuenced by (Fig. 3c). State anxiety showed signiﬁcant correlations internal or external environmental changes. Autonomic with V , RR, and T . However, these correlation coefﬁ- T E breathing is not only controlled by metabolic breathing, but cients were smaller than those in trait anxiety. This indi- also responds to changes in emotions, such as anxiety, fear, cated that these respiratory parameters are more strongly and pleasantness. More rapid breathing, shown during an correlated with trait. arousal state and during various negative emotional chan- Anxiety and other emotions are primarily generated in ges, indicates the relationships between emotions and res- the amygdala [2, 3]. Previous studies, using functional piration [14, 16–18]. Masaoka and Homma (2001) showed, neuroimaging methods, have shown the neuroanatomical in a study of anticipatory anxiety, that respiratory rate correlates of negative emotions of fear and anxiety and increases during anticipatory anxiety and that the response have revealed that the amygdala plays a crucial role in the is not related to changes in metabolic demand . They processing of these emotions. Recently, respiratory rhyth- also showed that increased respiratory rate during antici- mic neural activities were recorded from the piriform patory anxiety shows a linear positive correlation with trait cortex and amygdala using a limbic brainstem-spinal cord anxiety scores. It is well known that subjects with idio- preparation in newborn rats . The activity was syn- pathic hyperventilation or panic disorder have high trait chronized with the burst activities recorded from the spinal anxiety and increase their ventilation, which induces sus- root for the phrenic nerve and was functionally coupled to tained arterial and alveolar hypocapnia [12, 19]. There was medullary respiratory rhythm. It is generally believed that no hyperventilation observed in the present healthy sub- basic respiratory rhythm is generated in the brainstem. The jects, even in those who had higher trait anxiety during respiratory central pattern generator (RCPG) has been quiet breathing. Irregular breathing, such as that described shown to be located in the brainstem . A neuroimaging in subjects with anxiety or panic disorder [12, 20], was not study using fMRI in awake humans showed that the lim- apparent in these subjects. In the present study, we showed bic/paralimbic-bulbar circuitry plays a signiﬁcant role in that the respiratory rate during quiet breathing is inﬂuenced emotional modulation of spontaneous breathing . The by trait anxiety. Subjects who have a higher trait anxiety recent work study of Kim et al. (2013) showed that stim- showed a higher respiratory rate and those with a lower ulation of the bed nucleus of the stria terminals (BNST), trait anxiety showed a lower respiratory rate (Fig. 3d). We which is known to inﬂuence physiological manifestations also found a positive correlation between individual of anxiety, increases the respiratory rate in mice . In 123 J Physiol Sci (2018) 68:369–376 375 Table 2 Correlation of A. Trait respiratory parameters with trail (A) and (B) Circulation Differences q P HT LT P _ 0.384 NS 9.3 (8.9–9.9) 8.4 (7.4–9.3) NS V (I) FetCO (%) -0.038 NS 5.1 (5.0–5.4) 5.4 (5.2–5.4) NS V (ml) -0.687 \0.01 537.0 (493.8–584.1) 699.2 (585.7–803.21) \0.05 RR (n/min) 0.749 \0.001 16.9 (6.3–18..8) 12.1 (8.2–16.1) \0.01 T (s) -0.622 \0.05 1.4 (1.3–1.6) 2.2 (1.6–3.0) \0.01 T (s) -0.631 \0.01 2.2 (1.8–2.3) 2.7 (2.2–4.5) \0.05 0.209 NS 3.8 (3.4–4.2) 3.6 (3.3–4.2) NS VO =W (ml/min/ kg) HR (beat/min) -0.047 NS 67.7 (60.0–83.8) 73.1 (62.8–78.5) NS B. State Circulation Differences q P HS LS P _ 0.349 NS 9.3 (8.6–9.7) 8.47 (7.6–9.7) NS V (I) FetCO (%) -0.319 NS 5.1 (5.0–5.4) 5.4 (7.6–9.7) NS V (ml) -0.558 \0.05 498.9 (490.1–572.1) 655.2 (587.3–777.1) \0.01 RR (n/min) 0.582 \0.05 17.2 (16.5–19.5) 15.0 (10.1–16.2) \0.01 T (s) -0.404 NS 1.4 (1.3–1.5) 1.7 (1.5–2.7) \0.05 T (s) -0.623 \0.01 2.1 (1.8–2.2) 2.6 (2.3–3.7) \0.01 0.212 NS 3.8 (3.6–4.3) 3.6 (3.2–4.1) NS VO =W (ml/min/kg) HR (beat/min) -0.245 NS 65.8 (58.8–76.6) 76.4 (65.2–83.3) NS Differences of respiratory parameters between high (HT) and low (LT) trail and high (HS) and low (LS) state Compliance with ethical standards humans, dipoles obtained during the anticipatory anxiety were synchronized with respiration and were found to be Conﬂict of Interest The authors declare that they have no conﬂict of located in the amygdala . interests. Human and animal experiments on limbic and paral- imbic areas suggested that emotional impact is not only Open Access This article is distributed under the terms of the Creative Commons Attribution 4.0 International License (http://creative associated in neural activities in the brainstem, but also in commons.org/licenses/by/4.0/), which permits unrestricted use, distri- the limbic and paralimbic regions particularly in amygdala bution, and reproduction in any medium, provided you give appropriate in the limbic system . credit to the original author(s) and the source, provide a link to the The strong close relationship between respiratory Creative Commons license, and indicate if changes were made. rhythm and trait anxiety was also shown here in the rela- tionship between inspiratory time (T ) and expiratory time References (T ). T may contribute to the determination of RR and E E indeed T has been shown to have no correlation with trait 1. 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The Journal of Physiological Sciences – Springer Journals
Published: May 2, 2017
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