Effect of Breathing Pattern and Posture on Abdominal Muscle Activation and Intra-abdominal Pressure

Introduction

Breathing exercises, such as maximum expiration training [1], respiratory resistance training [2], inspiratory muscle training [3–5], or Pilates [3], are well-known for enhancing core stability and physical fitness. These exercises may be effective in the prevention of low back pain in athletes [6, 7] or as therapeutic exercises for patients with low back pain with a positive lumbar instability test [2]. In addition, inspiratory muscle training improves dynamic balance for healthy older adults, which results in improved walking speed and inspiratory muscle function [4, 5]. Thus, breathing exercises can improve physical function, human behavior, and quality of life, and are not merely for the improvement of breathing function [3].

Breathing exercises are often combined with the motion of the limbs or trunk, such as with the plank, elbow-toe, and postural stability exercises. Combining exercises leads to a synergistic effect because the respiratory muscles are utilized for both respiration and postural control [8–10]. There is a trade-off between task demand and respiratory demand in the respiratory muscles (e.g., diaphragm, internal oblique, and transverse abdominal muscle), which are called the local muscles [9, 11–13]. For instance, during heavy lifting, spinal stability is the priority, at the expense of a steady breathing pattern [11, 13]. However, as respiratory demand is increased, such as in certain exercises or in cases of respiratory disease, the contribution of the transverse abdominal muscle and diaphragm to spinal stability can be compromised [9, 12]. These basic studies have led to the principle of performing exercise in conjunction with the correct posture and breathing for injury prevention and enhancement of physical function.

Similarly, some clinical practice studies have demonstrated the effect of exercises combined with breathing. For instance, abdominal draw-in lumbar stabilization exercises with respiratory resistance resulted in decreased low back pain, reduced dysfunctions, and increased muscle thickness in contraction, contraction rate, and pulmonary function [2]. When exercises were combined with breathing, increased pressure in the abdominal cavity was attributed to the strong contraction of the diaphragm and deep abdominal muscles through breathing resistance. However, Oh et al. [2] only measured the diaphragm thickness by ultrasonography and did not measure muscle activity by electromyography or intra-abdominal pressure (IAP). Another clinical practice study has shown that the activity of the abdominal muscles increased significantly when combined with maximum expiration as compared with resting expiration during side-bridge exercises [14]. In addition, inspiratory muscle training combined with the Pilates methods was found to provide an enhancement in the pulmonary function and physical conditioning of elderly patients [3]. However, whether the inspiratory or expiratory breathing pattern is more effective remains undetermined. The Pilates breathing technique involves deep exhalation through the mouth with the lips slightly pursed, followed by inhalation through the nose combined with spinal motion [15]. Although the breathing technique of the Pilates method was associated with increased electrical activity in internal oblique and transverse abdominal muscles [15], its effect on the pressurizing effort in the breathing pattern remains unclear because of the lack of breathing volume and IAP measurement. Basic and clinical practice studies have not been bridged; thus, it is necessary to understand the effect of breathing pattern and posture from a physiologic standpoint for effective exercise instruction. This study aimed to examine the association between several breathing patterns and postures on abdominal muscle activation and IAP.

Methods

Experimental Approach to the Problem

Participants

Fourteen healthy men (mean age 22.7 years [range 19–35 years], mean height 172.1 cm [range 164.0–180.0 cm], mean weight 73.3 kg [range 58.0–100.0 kg]) volunteered to participate in this study. The participants were university students majoring in physical education. The study sample comprised four football players, two rugby players, two long-distance runners, a sprinter, a tennis player, a baseball player, a volleyball player, a handball player, and a soccer player. The participants had no neuromuscular, orthopedic, or respiratory abnormalities.

All procedures involving human participants were performed in accordance with the ethical standards of the institutional and/or national research committee and the 1964 Helsinki declaration and its later amendments or comparable ethical standards. Written informed consent was obtained from each participant. The study was approved by the Human Ethics Committees of Tokai Gakuen University (study no. 24 − 19).

Procedures

Task

The participants performed four active breathing tasks: quiet breathing (Q-Bre), diaphragmatic breathing (Dia-Bre), pursed-lips forced expiration (Forced-Expi), and exertional nasal inhalation with the abdominal muscles in isometric contraction (Exertion-Inspi). Specifically, Q-Bre was normal nasal tidal breathing (as a control); Dia-Bre was a complete nasal inhalation with submaximal expansion of the abdominal wall and relaxed expiration through the mouth; Forced-Expi was a completely forced exhale with pursed lips until the abdominal wall was hollowed; and Exertion-Inspi was a complete nasal inhalation, sufficient to expand the thorax while maintaining the abdominal muscles in isometric contraction and abdominal wall expansion. The participants practiced repeatedly during a lesson from breathing exercise instructors (T.K. and J.U.). The four breathing tasks were performed in a random order in the supine (as a control posture) and elbow-toe postures for 30 s. For the elbow-toe posture, the participant performed a prone plank posture on the floor, maintaining a straight trunk and lower extremities, with only their toes and forearms touching the floor (FIGURE 1). They rested for 3 min between the tasks to eliminate the influence of fatigue.

IAP, Breathing, and Muscle Activity Measurements

Respiratory and IAP measurements were performed based on previous studies [16, 17]. Briefly, IAP was measured using a pressure transducer (MPC-500, Millar Instruments, Inc., Houston, TX, USA) placed intra-rectally [16–18]. Before the actual measurements were taken, the maximum IAP was obtained based on the maximum voluntary pressurizations produced during Valsalva maneuvers performed in a standing posture (_maxIAP). The highest value among three trials was used as the maximum. The IAP during the task was normalized using _maxIAP (%IAP). The breathing volume of all the tasks was measured with a pneumotachograph (FM-200, Arco System, Inc., Kashiwa, Japan) using a face mask covering the nose and mouth (7400, Hans Rudolph Inc., Wyandotte, MO, USA). Respiratory volume was calibrated using a syringe calibrated at 3 L (763722, Sensor Medics Corp., Yorba Linda, CA, USA).

Surface electromyogram (EMG) measurements were based on previous studies [19]. In preparation for the EMG, the surface of the skin was cleaned with alcohol and rubbed with sandpaper. Surface bipolar electrodes (Ag-AgCl, 6-mm contact diameter, 1.5-cm inter-electrode space) were placed on each of the muscles using Kinesio tape. Before the measurement and throughout the testing period, all EMG signals were monitored and checked using a real-time oscilloscope display. EMG signals from the right transverse abdominis-internal oblique muscle (TrA-IO) and the right external oblique muscle (EO) were recorded during the tasks. Electrodes for the TrA-IO were placed 2 cm inferomedial to the anterior superior iliac spine [20] at an angle following the inguinal ligament. The activity of the TrA-IO could be best assessed from this surface location [21, 22]. Electrodes for the EO were placed at the junction of a line drawn from the umbilicus to the anterior axillary line at an oblique angle following the muscle fibers. A reference electrode was placed on the right iliac crest. The EMG signals were amplified differentially using an AC amplifier (input impedance 5 MΩ, gain 1,000–2,000×, common-mode rejection ratio > 60 dB), and band-pass filtering was set at both low (time constant of 0.03 s) and high (2 kHz) cut-off filters (AB-620G, Nihon Koden, Japan). Before performing the actual tasks, all participants completed a trial of maximum voluntary contraction (MVC) of the isometric muscles in the supine and side-lying postures. To do this, they kept the area beyond their iliac crest hanging over the examination table, with their pelvis and lower leg held in place by two testers. Thereafter, they gradually increased the force they applied against the tester’s hand, trying to hold the maximum force for about 5 s as the other tester applied maximum resistance. The highest root mean square of EMG amplitude for each muscle of the 3 MVC trials or Valsalva maneuver tests was adopted as the MVC value for subsequent statistical analysis (100% MVC). The root mean square of EMG data of the MVC trial was calculated for 100 ms (between 50 ms before and after the peak IAP value was obtained).

Statistical Analysis

IAP, airflow data, and EMG data were simultaneously recorded with a computer (chart 5.3, AD Instruments, Sydney, Australia) using an analog-to-digital converter (Power-lab 8sp, AD Instruments, Sydney, Australia) at a sampling rate of 2 kHz. Representative data are shown in FIGURE 2. For each parameter, values were averaged from a series of three trials for each set of phases (inspiratory and expiratory).

A two-factor (breathing and posture) repeated-measures analysis of variance and Bonferroni testing was conducted to assess statistical significance. All statistical analyses were performed using SPSS software, version 22 (SPSS Inc., Chicago, IL, USA). A p-value < 0.05 was considered statistically significant. In addition, the magnitude of changes of the values from the reference value (Q-Bre in the supine posture) was expressed as the effect size. Each outcome was classified as a small (0.2), moderate (0.5), or large (≥ 0.8) effect [23]. Finally, the muscle activity ratio between the local and global muscles was expressed as a relative value (TrA-IO/EO).

Results

Respiratory volume was remarkably different between breathing patterns and posture during both the inspiratory and expiratory phases (Table 1). Forced-Expi was found to result in the largest respiratory volume by a notable margin, followed by Dia-Bre, in which the respiratory was higher than that of Q-Bre. No differences in volume were found between Exertion-Inspi and Q-Bre.

Table 1

Mean ± Standard deviation (95% confidence interval [CI]) respiratory volume values (liter)
	Posture	Breathing task
		a) Q-Bre	b) Dia-Bre	c) Forced-Expi	d) Exertion-Inspi	F value (p value)	p < 0.05 by Bonferroni testing
Inspiratory phase	supine	0.75 ± 0.26 (0.60–0.90)	1.51 ± 0.44 (1.25–1.76)	2.57 ± 0.76 (2.13–3.01)	0.93 ± 0.26 (0.79–1.08)	61.64 (0.001*)	c vs a, b, d b vs a, d
	elbow-toe	0.67 ± 0.40 (0.44–0.91)	1.26 ± 0.46 (0.99–1.53)	1.81 ± 0.71 (1.40–2.22)	1.12 ± 0.43 (0.88–1.37)	61.64 (0.001*)	c vs a, b, d b vs a
Posture						4.05 (0.066)
Expiratory phase	supine	0.69 ± 0.28 (0.53–0.85)	1.44 ± 0.47 (1.17–1.71)	3.33 ± 0.99 (2.76–3.90)	0.98 ± 0.33 (0.79–1.17)	69.45 (0.001*)	c vs a, b, d b vs a
	elbow-toe	0.55 ± 0.24 (0.41–0.69)	1.34 ± 0.43 (1.09–1.60)	2.31 ± 0.86 (1.81–2.81)	1.11 ± 0.51 (0.82–1.41)	69.45 (0.001*)	c vs a, b, d b vs a
Posture						7.72 (0.016*)
*p < 0.05; Q-Bre, quiet nasal breathing; Dia-Bre, nasal diaphragmatic breathing until abdominal wall expansion; Forced-Expi, completely forced expiration with pursed-lips until the abdominal wall hollowed; Exertion-Inspi, exertional nasal inhalation with abdominal muscle isometric contraction to prevent abdominal wall expansion.

TrA-IO and EO activity including IAP only had a remarkable effect on the breathing pattern and posture during the expiratory phase (Table 2). In the inspiratory phase, the breathing task remarkably affected TrA-IO activity and IAP, whereas posture affected EO activity and IAP (Table 2).

Table 2

Results of a two-factor repeated-measures analysis of variance for muscle activity and intra-abdominal pressure (IAP) development.
	Breathing task		Posture		Posture×breathing task
	F value	p value	F value	p value	F value	p value
Inspiratory phase
TrA-IO	10.878	0.002*	3.906	0.070	2.053	0.164
EO	0.286	0.835	74.904	0.001*	2.110	0.146
IAP	9.459	0.001*	54.695	0.001*	2.219	0.101
expiratory phase
TrA-IO	12.488	0.001*	0.388	0.544	6.222	0.009*
EO	6.522	0.014*	76.044	0.001*	4.258	0.011*
IAP	19.850	0.001*	5.104	0.042*	34.574	0.001*
*p < 0.05; TrA-IO: transverse abdominal and internal oblique muscle; EO: external oblique muscle

The greatest TrA-IO activity was observed in Forced-Expi at the expiratory phase (FIGURE 3). The next greatest activity exceeded 30% of the MVC in Exertion-Inspi, in both inspiratory and expiratory phases in the elbow-toe posture (Table 3). No differences were found below 20% of the MVC in Dia-Bre or Q-Bre, regardless of the posture, and in the TrA-IO during Exertion-Inspi in the supine posture (FIGURE 3, Table 3).

Table 3

Effect size (Cohen’s d) referenced by quiet nasal breathing (Q-Bre) in supine posture
	Posture	Breathing task
		Q-Bre	Dia-Bre	Forced-Expi	Exertion-Inspi
Inspiratory phase
TrA-IO	supine	ref	0.02	0.08	0.69 †
	elbow-toe	0.40	0.39	0.17	1.57 *
EO	supine	ref	0.49	1.07 *	3.07 *
	elbow-toe	21.84 *	21.14 *	21.40 *	20.12 *
IAP	supine	ref	7.49 *	6.04 *	3.69 *
	elbow-toe	7.55 *	20.01 *	15.92 *	18.57 *
Expiratory phase
TrA-IO	supine	ref	0.03	2.26 *	0.69 †
	elbow-toe	0.31	0.57 †	1.34 *	1.42 *
EO	supine	ref	0.44	12.82 *	2.51 *
	elbow-toe	20.81 *	22.34 *	26.71 *	19.60 *
IAP	supine	ref	10.53 *	53.43 *	4.94 *
	elbow-toe	10.33 *	26.20 *	30.60 *	21.07 *

EO activity in the elbow-toe posture induced 22.5–30.6% MVC regardless of the type of breathing pattern (FIGURE 3, Table 3). In contrast, EO activity in the supine posture resulted in < 5% MVC, except for the remarkably increased activity in Forced-Expi at the expiratory phase (15.8% of the MVC) (FIGURE 3).

The relative values (TrA-IO/EO) were > 1.0 for all breathing tasks in the supine posture (Table 4). In the elbow-toe posture, these values were only > 1.0 in Exertion-Inspi at both the inspiratory and expiratory phases and in Forced-Expi at the expiratory phase. In contrast, these values were < 1.0 in the other breathing tasks because of the larger increase in activity contribution with EO compared with that with TrA-IO.

Table 4

Relative value of TrA-IO and EO activity
		Posture	Breathing task
			Q-Bre	Dia-Bre	Forced-Expi	Exertion-Inspi
Inspiratory phase
TrA-IO/EO	(ratio)	supine	4.96	4.11	3.68	4.12
		elbow-toe	0.69	0.71	0.56	1.59 *
Expiratory phase
TrA-IO/EO	(ratio)	supine	4.66	3.98	3.01	4.46
		elbow-toe	0.62	0.75	1.06 *	1.46 *
* Relative value > 1.0 in elbow-toe task; TrA-IO, transverse abdominal and internal oblique muscle; EO, external oblique muscle; Q-Bre, quiet nasal breathing; Dia-Bre, nasal diaphragmatic breathing until abdominal wall expansion; Forced-Expi, completely forced expiration with pursed-lips until the abdominal wall hollowed; Exertion-Inspi, exertional nasal inhalation with abdominal muscle isometric contraction to prevent abdominal wall expansion.

The maximum IAP during the Valsalva maneuvers was 196.9 mmHg (SD 59.5, range 67.1–295.0). The relative IAP value was substantially lower in all tasks, at < 15% of the IAP (FIGURE 3, Table 3). Only Forced-Expi at the expiratory phase was notably increased in the supine posture (24.9% of the IAP).

Discussion

In this study, we presented novel findings showing an association between several combinations of breathing patterns and postures on abdominal muscle activities based on EMG and IAP, while observing respiratory volume. We found that TrA-IO and EO activity including IAP was only associated with breathing pattern and posture during the expiratory phase. Additionally, in the inspiratory phase, TrA-IO activity and IAP were remarkably affected by breathing pattern, while EO activity and IAP were affected by postural tasks. Thus, our results may fill the gap between basic and clinical practice regarding the importance of combining posture exercises with breathing tasks.

The greatest TrA-IO activity was observed in the Forced-Expi breathing pattern at the expiratory phase in the supine posture (47.6% of MVC). Even in the supine posture, the TrA-IO activity level in Forced-Expi breathing was still relatively higher than that in some of the plank exercises without breathing tasks reported in previous studies [24, 25]. TrA-IO activity was primarily affected by Forced-Expi, as evidenced by the greatest IAP development, which induced the greatest respiratory volume approximately 4–5 times, compared with that in Q-Bre (Table 1). In the qualitative observation of IAP dynamics and TrA-IO activity, Forced-Expi induced primary positive pressuring at the expiratory phase, corresponding with the phasic activity of the TrA-IO after negative pressuring at the inspiratory phase (FIGURE 2-c). According to observations of ultrasonographic visual change, the mean thickness of the IO muscle significantly increases at end-expiration phases [26]. Furthermore, TrA/IO thickness increases by approximately 1 mm—a considerable increase—after the breathing exercise of maximum expiration with the maximal abdominal contraction maneuver [1]. Forced expiration corresponding with the positive pressuring would promote concentric activity of the TrA-IO; however, we must consider the risk-benefit ratio between cardiorespiratory burden and exercise intensity. The greatest IAP value in the Forced-Expi (24.9% of IAP) was moderate and comparable with the result of 45% maximal lifting effort during isometric lifting found in a previous study [16]. If a few breathing trials did not have any issues, but were repeated several times, it was still necessary to consider the cardiorespiratory burden.

The second greatest TrA-IO activity value was observed in the Exertion-Inspi pattern throughout the inspiratory and expiratory phases in the elbow-toe posture (about 30–40% of MVC). Despite this, the respiratory volume was only about 1.2–2.0 times that of the Q-Bre (Table 1). The TrA-IO activity was triggered by the inspiratory phase rather than by the expiratory phase, contrary the pattern observed in Forced-Expi (FIGURE 2-d). The Exertion-Inspi method resembles the Pilates methods [15], which was a complete nasal inhalation while maintaining the abdominal muscles in isometric contraction. To maintain the isometric contraction, the TrA-IO activity needs to be balanced against the increasing pressure produced by the descent of the diaphragm in inhalation [27, 28]. Thus, endurance-related training is recommended for the sustenance of TrA/IO activity without being affected by the breathing event, as TrA/IO activity plays a role in respiration and the postural control effect [8–10]. Moreover, it would improve the risk-benefit ratio, because the IAP value in Exertion-Inspi was smaller (12.4% of IAP) than that in Forced-Expi. This low value allows us to sustain exercise without cardiorespiratory burden [16]. Regarding exercise instruction, because of the small respiratory volume in Exertion-Inspi, the instructor emphasized the need for isometric contraction of the TrA-IO.

Compared with the Q-Bre task, there was no increase in the activity of the TrA-IO in the Dia-Bre. TrA-IO activity in Dia-Bre in the elbow-toe posture was only about 20% of the MVC, which was the same as that of some of the plank exercises without breathing in previous studies [24, 25]. Even if we focus on the large inspiration pattern, which induced a 2.0–2.4-fold respiratory volume in Dia-Bre compared with that in Q-Bre, the relaxed-deep breathing (Dia-Bre) resulted in insufficient TrA-IO activity. In this breathing pattern, the abdominal muscles only expanded passively, contrary to what was observed in Exertion-Inspi. Although the IAP value in Dia-Bre was low, the elasticity of the passive expansion of abdominal muscles nullified the IAP produced by the descent of the diaphragm during inhalation [27, 28]. Thus, the Dia-Bre pattern did not affect TrA-IO activity and IAP dynamics, and only promoted the passive expansion of the abdominal muscles, even in the elbow-toe posture.

EO activity was affected by the posture tasks. The activity was 3–6 times larger in the elbow-toe posture than it was in the supine posture, regardless of the type of breathing pattern. This result is in accordance with the results of previous studies [24, 25], although it is impossible to compare them directly because of the different MVC trials and a lack of supine posture data in the previous studies [24, 25]. Imai et al. [24] and Okubo et al. [25] found that EO activity increased in several additional postural tasks in addition to the elbow-toe posture, rather than in the local muscles. These results in combination with ours suggest that EO activity contributes more to posture tasks than to breathing-related tasks.

We found a unique result regarding the relative values of TrA-IO and EO activity. The TrA-IO/EO ratio of < 1.0 in the elbow-toe posture indicated that the contribution of EO activity was higher than that of TrA-IO activity. Conversely, a ratio > 1.0 in Exertion-Inspi at the inspiratory-expiratory phase and in Forced-Expi at the expiratory phase indicated that the TrA-IO was also a contributor, together with the EO. Performing the dual task of posture and breathing may be useful in activating all the abdominal muscles. The dual task is also likely to have an effect on muscle strength and physical performance. Additional research is required to determine the training effect on physical performance and the synergistic effect of muscle function.

There are several limitations to this study. First, the participants were university students majoring in physical education who were not accustomed to routine practice of the breathing methods used, such as the Pilates method. The abdominal muscles may be activated to a higher extent in people practicing controlled breathing. Second, we used surface EMG rather than fine-wire EMG. Nonetheless, the muscle activity of the TrA-IO and EO significantly differed among several breathing patterns and postural tasks. Thus, our goal was achieved. Lastly, we could not assess the activity of the diaphragm because of technical reasons, although its activity plays an important role in IAP development.

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