Abstract
We assessed the effect of four voluntary breathing conditions on maximal voluntary isometric force of large muscle groups. Ten subjects performed maximum voluntary isometric contractions (MVIC) of knee flexion and extension, shoulder abduction and adduction, and elbow flexion and extension under all breathing conditions: normal breathing, forced inhalation, forced exhalation, and the Valsalva maneuver (VM). Forced exhalation significantly increased peak force during shoulder adduction, elbow extension and knee extension MVIC tasks (p=0.001, p=0.024, p=0.002, respectively); the peak force during the Valsalva maneuver was not different from forced exhalation for all tested muscle groups. No voluntary breathing condition appeared to influence the peak force during knee flexion, elbow flexion and shoulder abduction MVIC tasks. The results demonstrate that voluntary breathing imposes a significant impact on isometric muscle strength. Given increased cardiovascular risks associated with the Valsalva maneuver, it is highly recommended that forced exhalation should be used during exercises at maximal levels, especially in repetitive repetitions.
Keywords: Maximal voluntary isometric contraction (MVIC), Muscle strength, Respiration, human
INTRODUCTION
It is a commonly held belief that exhaling forcefully against a closed glottis, the Valsalva maneuver (VM), is the optimal breathing pattern for producing maximal force. Zatsiorsky and Kraemer (21) recommended that, for ultimate force production, expiration (forced expiration or the VM) should match with the forced phase of movement, regardless of the movement direction or anatomical position, i.e., a biomechanical match. Another rationale for using the VM during maximal effort is to increase intra-abdominal and intra-thoracic pressure thus improving trunk stability and providing additional stiffness for proximal muscle attachments to improve muscle force production in the extremities (6). However, this view was not supported by a recent study, in which Hagins et al. (10) found that, although intra-abdominal pressure increased significantly with the Valsalva maneuver over other breathing conditions during a simulated maximum lifting task, this breathing pattern was not associated with increased trunk extension force production. The VM, unfortunately, imposes negative hemodynamic effects on the cardiovascular system, e.g., increased blood pressure, increased heart rate, and risk of cerebral hemorrhage (7, 11, 16–19, 22). Therefore, the VM is not recommended for strength training purposes (6), particularly in people with high systemic blood pressure (18).
Recently, Li and Laskin (13) reported that peak force of the finger flexors increased significantly from forced inspiration to forced expiration, with parallel changes in finger flexors electromyographic (EMG) activities. Interestingly, the peak forces during forced expiration were not significantly different from those produced during the VM. The authors ascribed the findings to a respiratory-motor enhancement mechanism. During forced expiration and the Valsalva maneuver, increased respiratory-related cortical neuronal activity synchronizes with, and thus enhances, the motor drive to non-respiratory muscles, e.g., the finger flexors, resulting in greater peak force. This proposed enhancement mechanism was further supported in a subsequent study (15), in which the initiation of forced expiration and inspiration was synchronized with deviation of constant isometric finger flexion force at submaximal levels. As a result, force variability was found to be increased, as compared with that measured during normal breathing.
It remains unknown, however, whether voluntary breathing could influence muscle strength of large muscles. The VM is typically used during large muscles strength training. Therefore, the purpose of this study was to examine the effect of voluntary breathing and to generalize the results observed in small hand muscles (13) to large muscles. The large muscles in this investigation include knee flexors and extensors, shoulder adductors and abductors, and elbow flexors and extensors. The hypothesis was that, as seen in small hand muscles (13), different phases (inspiration and expiration) of voluntary breathing will significantly influence muscle strength of large muscles.
METHODS
Experimental Approach to the Problem
In order to examine the experimental hypothesis of the ventilation effects on strength of large muscles, 10 subjects were recruited to participate in this investigation. Both male and female subjects without prior or current strength training experience were purposefully recruited, because our primary interest was to investigate this phenomenon and to quantify the potential effect of ventilation. Subjects were asked to perform a brief (3 – 5 s) maximum voluntary isometric contraction (MVIC) of large muscle groups, including knee flexion and extension, elbow flexion and extension, and shoulder abduction and adduction, during four different breathing conditions. The conditions were normal breathing, synchronized forced inhalation, synchronized forced exhalation, and the VM. Force and breathing data were recorded for offline measurement. The peak value of force data was used to study the effect of voluntary breathing on isometric muscle strength of large muscles. This was a within-subject study design. The treatments (conditions) were randomized to balance the presentation of treatments.
Subjects
This study had two sessions. In the lower extremity (LE) session, muscle strength of the knee joint was tested in ten healthy subjects (6 females and 4 males) with the average age of 27.8 ± 7.1 years (range 24–46 years). Another group of ten healthy subjects (N=10, 7 females and 3 males) with average age of 26.3 ± 3.5 years (range 22 –32 years) participated in the upper extremity (UE) session, in which muscle strength of the shoulder and elbow joints was tested. All subjects had no prior or current experience of strength training. The University of Montana Institutional Review Board approved this study and all subjects gave written informed consent.
Procedures
During all testing, the subjects were seated on a KinCom dynamometer chair (Model 125AP, Isokinetic International, Harrison, Tennesee) and breathed through a facemask connected to a pneumotachometer (Series 1110A; Hans Rudolph, Kansas City, Missouri) to monitor ventilation. In the LE session, the subject's trunk was restrained in the chair, arms crossed the chest, and the hips were positioned at 90° of flexion and the left leg was supported on a foot rest (Figure 1). The right knee joint was kept at 50° of flexion for both knee flexion and extension MVIC, with the knee joint axis of rotation aligned with the axis of rotation of the Kincom motor. The force transducer was secured to the lower leg at the distal third from the knee joint. The subjects were asked to keep the ankle joint of the test side was held in a neutral position to minimize variations in knee joint torque measurement (4).
Figure 1.
Experimental settings for the lower extremity session
In the UE session, the trunk was not supported or constrained, the feet were supported, hips and knees were positioned at 90° of flexion. During both the shoulder abduction and adduction MVIC tests, the left shoulder was held at 60° of abduction and 10° of flexion. The force transducer was secured to the mid-humerus. During the elbow tests, the left shoulder joint was kept in the neutral position. The left elbow was positioned at 120° of flexion with the forearm in a neutral position and the hand in a loose fist. The force transducer was secured to the distal quarter of the left forearm. Both elbow flexion and extension MVICs were measured using the same configuration. Specific instructions were given to assure there was no tilting or leaning of the trunk during the experiments. Subjects were instructed to comfortably rest the right hand on the ipsilateral lap.
Maximum voluntary isometric contractions (MVIC) of knee flexion and extension, shoulder abduction and adduction, and elbow flexion and extension were tested during four different patterns of ventilation, including
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1)
Normal breathing (MVICNML), subjects breathed in and out normally while producing as much force as they could;
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2)
Synchronized forced inhalation (MVICIN), subjects produced as much force as they could while synchronizing force production with rapid forced inhalation;
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3)
Synchronized forced exhalation (MVICOUT), subjects produced as much force as they could while synchronizing force production with rapid forced exhalation; and
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4)
Valsalva Maneuver (MVICVM), subjects produced as much force as they could while synchronizing force production with the initiation of the Valsalva maneuver.
Subjects rested and breathed normally in the above described configuration prior to each trial. Two computer-generated tones indicated the beginning of a 10-s trial. Subjects initiated force production in a self-paced manner within the first 3 s of the trial and were verbally encouraged to maintain maximal force production for the ensuing 3 to 5 s. Force production was at a self-selected rate. They did not receive any feedback on force production during the experiment. Two trials of MVIC were recorded for each condition (ventilation and muscle group). Five to eight practice trials at submaximal levels (approximately 50% MVIC) were allowed to familiarize subjects with experimental settings and instructions. The subjects were given approximately 60 s intervals between trials and conditions to minimize fatigue. Subjects always performed MVICNML tasks first for each muscle group to minimize the influence of instructions on their performance. The other three tasks were performed in a randomized order. This protocol has been used in a previous study (13).
Airflow and force signals were sampled at 1000 Hz by a 16-bit analog-to-digital converter (PCI 6229; National Instruments, Austin, Texas) using customized LabView software (National Instruments). All signals were saved for offline analysis using a customized Matlab (The MathWorks, Natick, Massachusetts) program.
The peak force was calculated as the force averaged over a 100-ms window, centered about the instance of the maximal force, after a low-pass filtering at 20 Hz. The higher peak force of two trials was selected as FMVIC (cf. 14). To compare the effect of breathing on maximal force-generating capability, FMVIC for MVICIN, MVICOUT, and MVICVM tasks were normalized to FMVIC for MVICNML tasks for each muscle group. Airflow signals were used to confirm subjects' performance for each task through visual inspection during offline analysis.
Statistical Analyses
The data from the investigation are presented as mean. The statistical analyses were performed using STATISTICA 7 (Statsoft, Inc., Tulsa, OK). A repeated-measures one-way ANOVA was used to compare the absolute value of FMVIC for each muscle group under different breathing conditions. The factor was TASK (4 levels, four tasks). To compare the effect of breathing on FMVIC of different muscle groups of the same joint, a two-way ANOVA was used to compare normalized FMIVC with the factors MUSCLE (2 levels, flexor/extensor or adductor/abductor) and BREATH (3 levels, inhalation, exhalation and VM). Post hoc Tukey's honestly significant difference tests were used when necessary. Intraclass correlation coefficients (ICC) for reliability of the dependent measures ranged from 0.85 to 0.93. For the n size used, statistical power was ranged from 0.81 to 0.88 for the variables examined in this investigation. The level of significance was set at an alpha level p≤ 0.05 for this investigation.
RESULTS
Subjects performed maximum voluntary isometric contractions (MVIC) of knee flexion and extension, shoulder abduction and adduction, and elbow flexion and extension under different breathing conditions. Overall, the influence of voluntary breathing on the peak force was muscle-specific, and respiratory phase-dependent. The peak forces are summarized in Table 1. As depicted in Figure 2, voluntary breathing dramatically influenced, e.g., isometric knee extension MVIC. On average, the peak force (FMVIC) was significantly influenced by breathing patterns during knee extension (p=0.002), elbow extension (p=0.024) and shoulder adduction (p=0.001) MVIC tasks, while FMVIC remained unchanged during knee flexion, elbow flexion and shoulder abduction MVIC tasks. Specifically, as compared to FMVIC during the knee extension MVICNML task, FMVIC significantly increased during MVICIN, MVICOUT, and MVICVM tasks (p<0.002), respectively. No significant differences in FMVIC were found among these three tasks. During elbow extension, FMVIC was significantly greater in MVICOUT and MVICVM tasks than in the MVICIN task (p<0.024); FMVIC in the MVICIN task was not different from the MVICNML task. Similarly, shoulder adduction FMVIC was significantly greater in MVICOUT and MVICVM tasks than in the MVICIN task (p<0.001). FMVIC was also greater in the MVICOUT task than in the MVICNML task (p<0.001). A consistent finding was that there was no significant difference in FMVIC between MVICOUT and MVICVM tasks for all tested muscle groups.
Table 1.
Peak forces (Newtons) averaged across 10 subjects during maximum voluntary isometric contractions (MVIC) of knee flexion (Flex) and extension (Ext), elbow flexion and extension, and shoulder abduction (ABD) and adduction (ADD) under different breathing conditions. Four breathing conditions are normal breathing (MVICNML); forced inhalation (MVICIN); forced exhalation (MVICOUT), and the Valsalva maneuver (MVICVM). Standard errors are presented in the parenthesis.
Knee | Elbow | Shoulder | ||||
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Flex | Ext | Flex | Ext | ABD | ADD | |
MVICNML | 325.3 (18.5) | 617.4 (56.8) | 255.9 (22.9) | 152.6 (13.6) | 219.0 (15.1) | 246.3 (25.5) |
MVICIN | 314.5 (16.0) | 697.8 (59.6) | 263.8 (21.3) | 144.8 (10.5) | 228.4 (13.3) | 226.0 (25.3) |
MVICOUT | 314.4 (16.3) | 672.4 (61.6) | 265.7 (22.8) | 160.5 (12.2) | 222.9 (13.7) | 274.7 (23.5) |
MVICVM | 310.7 (16.0) | 672.0 (62.1) | 268.9 (24.0) | 159.5 (12.4) | 233.8 (17.4) | 265.2 (24.4) |
Figure 2.
Typical trials during knee extension MVIC attempts under different breathing conditions: normal breathing (NORM); forced inhalation (IN); forced exhalation (OUT); and Valsalva maneuver (VM).
When normalized to FMIVC of MVICNML tasks, normalized FMIVC was used to compare the breathing effect on muscle strength of antagonist muscle groups of the same joint. In the LE session, the normalized FMIVC was significantly greater during knee extension (111.0%) than during knee flexion (96.8%) MVIC tasks (Figure 3A). A two-way ANOVA showed a main effect of MUSCLE (p=0.014). However, no differences in the normalized FMIVC were found among different breathing conditions during either knee flexion or extension MVIC tasks.
Figure 3.
The effect of breathing on muscle strength. Muscle strength (FMVIC, %) was normalized to the peak force during normal breathing. Flex: flexion; Ext: extension; ABD: abduction; ADD: adduction; IN: forced inhalation; OUT: forced exhalation; VM: Valsalva maneuver.
A different pattern was observed in the UE session. No difference in the normalized FMIVC was found between elbow flexion and extension MVIC tasks. A two-way ANOVA showed a main effect of BREATH (p=0.001) and a significant MUSCLE×BREATH interaction ( p=0.039). Post-hoc tests revealed that elbow extension FMIVC during the MVICIN task (97.6%) was significantly smaller than others, while no differences among other tasks were found (p<0.039) (Figure 3B). Likewise, no difference in the normalized FMIVC was found between shoulder adduction and abduction MVIC tasks. There was a main effect of BREATH (p=0.028) and a significant MUSCLE×BREATH interaction (p=0.004) (Figure 3C). According to post-hoc analysis, shoulder adduction FMIVC during the MVICIN task was significantly smaller than during MVICOUT and MVICVM tasks (p<0.004). There was no difference in FMIVC between MVICOUT (110.4%) and MVICVM (111.5%) tasks.
DISCUSSION
This study clearly demonstrated that voluntary breathing can influence maximal muscle strength of large lower and upper extremity muscles. By adopting the same protocol from a previous study (13), we generalized their results that demonstrated specificity of a breathing effect on peak force of finger muscles to the large muscle groups. During knee flexion and extension, shoulder abduction and adduction, and elbow flexion and extension MVIC tasks, the influence of voluntary breathing on the peak force was muscle-specific, and respiratory phase-dependent. Specifically, knee extension force significantly increased during forced inhalation, exhalation and the Valsalva maneuver as compared to the force obtained at normal breathing; both shoulder adduction and elbow extension forces were greater during forced exhalation and the VM than during forced inhalation. Voluntary breathing did not appear to influence the peak force during knee flexion, elbow flexion and shoulder abduction MVIC tasks.
Furthermore, similar to the previous study (13), no additional benefit of using the VM was observed when compared to synchronized forced exhalation during maximal isometric contraction of all tested muscle groups. Previous studies reported increased cardiovascular risks associated with the VM during forceful movements (7, 11, 16–19, 22). In contrast, forced exhalation could significantly reduce intrathoracic pressure and thus minimize the induced-hemodynamic changes. For example, arterial hypertension produced during heavy weight lifting with the VM was dramatically reduced when the exercise was performed without the VM (i.e., with an open glottis) (17). Similarly, greater increases in arterial blood pressure and heart rate were observed with voluntary breath holding than without holding during moderate abdominal exercise (7). Therefore, it is highly recommended that forced exhalation, rather than the Valsalva maneuver, should be used during maximal force production, whenever possible (cf. 21).
Forced exhalation and forced inhalation impose contrasting effects on different movements (Fig 3). As compared to forced inhalation, forced exhalation increased the peak force during knee extension, elbow extension, and shoulder adduction. The muscle-specific, phase-dependent effect of breathing on the peak force has been reported previously. For example, Hagin et al. (10) found that the Valsalva maneuver and forced exhalation led to unchanged trunk extension peak force, though significantly higher intra-abdominal pressure, during a simulated maximum lifting task. In contrast, Li and Laskin (13) reported that both forced exhalation and the Valsalva maneuver increased finger flexion peak force to the similar extent.
The observed pattern of results may be attributed to the fact that the motor drive to non-respiratory muscles could be modulated by voluntary breathing. Previous studies have demonstrated that the influence of voluntary breathing on the motor drive to non-respiratory muscles is both respiratory phase-dependent and muscle-specific (1, 2, 5, 8, 20). For instance, resistive loaded inspiration significantly enhanced tonic vibratory response in the extensor digitorum (2), but did not affect contraction of biceps brachii (8). The latency of median nerve components of somatosensory evoked potentials (SEP) was lengthened by inspiratory, but not by expiratory resistive loaded breathing, suggesting possible inhibitory effects of forceful inspiration on the wrist/finger flexors (1). Forceful inspiration, however, did not alter the magnitude of motor evoke potential (MEP) from abductor digiti minimi muscle (ADM) in a transcranial magnetic stimulation (TMS) study (5).
These findings of the ventilation effects, however, may be viewed as mechanical artifacts of voluntary breathing on the peak force on muscles. Greater shoulder adduction peak force may be related to increased activation of proximal muscles (e.g., shoulder adductor) during forced exhalation. This effect could be transferred to the distal finger flexors through a proximal-distal synergy (3, 9, 12), resulting in increased finger flexion peak force. However, using the same reasoning, an increased elbow flexion peak force during forced exhalation would be expected. In contrast, an increased elbow extension peak force was observed instead in the present study. The present pattern of results argues against mechanical artifact as a sole underlying mechanism. In combination with the aforementioned breathing effects on motor drive (1, 2, 5, 8, 20), current results are more likely due to modulated motor drive resulting from respiratory-motor interactions.
PRACTICAL APPLICATIONS
To summarize, the results demonstrate that voluntary breathing imposes a significant impact on isometric muscle strength. Both forced exhalation and the Valsalva maneuver increase maximal forces during elbow extension, shoulder adduction, and knee extension to a similar extent. Voluntary breathing did not appear to influence the peak force during knee flexion, elbow flexion and shoulder abduction MVIC tasks. Although the Valsalva maneuver is more natural during some exercises at maximal levels, especially when movements occur, given increased cardiovascular risks associated with the Valsalva maneuver, it is highly recommended that forced exhalation should be used during exercises at maximal levels, especially in repetitive repetitions.
Acknowledgements
The authors thank Dr. Woo-Hyung Park for his technical assistance. This study was supported in part by an NIH grant (1R15NS053442-01A1).
Footnotes
There is no conflict of interest.
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