The human physiological response to “maximal” breath holding can be characterized by two distinct phases (22). The first phase resembles a quiescent period where an individual’s respiratory neuromuscular output is inhibited, the glottis is voluntarily closed, and no significant movement of the thorax occurs (i.e., the easy-going phase). Throughout this period, the individual experiences a growing “urge to breathe,” which most likely arises from a combination of psychogenic, humoral, and mechanical stimuli (3,16). When the intensity of air hunger becomes too great, the individual begins to produce respiratory efforts against their closed glottis (i.e., the struggle phase). The individual continues to “struggle” for the remainder of the breath hold (BH) until the break point is reached, upon which the glottis opens and respiratory contractions reward the individual with unobstructed airflow. Although it is generally accepted that respiratory contractions increase in magnitude and frequency during the struggle phase of a truly “maximal” BH (22,39), the precise role that inspiratory and expiratory muscles play in affecting these efforts is unclear. Moreover, the relative “intensity” or energetic demands of respiratory contractions during breath holding is yet to be determined.
Some investigators have reported that respiratory contractions during maximal breath holding are achieved primarily via inspiratory action of the diaphragm with no discernible recruitment of expiratory muscles (1), whereas others have documented reciprocating activation of inspiratory (diaphragm and inspiratory intercostals) and expiratory muscles (expiratory intercostals and abdominal muscles) (20,32,33). It appears from the above findings that both inspiratory and expiratory muscles are progressively recruited during the struggle phase; however, there exists no study that describes the relative patterns of pressure development within these muscle groups during this phase of a maximal BH (e.g., inspiratory rib cage muscles vs diaphragm).
The evolution of respiratory neuromuscular output during the struggle phase appears qualitatively similar to that observed during heavy elastic loaded breathing, insofar as net inspiratory pressure development rises over time, despite the respiratory mechanical load remaining constant (38). The contribution of the rib cage muscles to inspiratory movements of the chest wall steadily increases during elastic loaded breathing, commensurate with increasing pressure development of the abdominal muscles during expiration (23). If one considers the respiratory contractions performed against a closed glottis during breath holding analogous to breathing against an infinitely large elastic load, one might expect to observe a similar pattern of respiratory muscle recruitment during the struggle phase of a maximal BH.
We sought to determine the patterns of respiratory pressure development of the diaphragm, rib cage, and abdominal muscles during the struggle phase of maximal breath holding in trained apnea divers. Respiratory contractions were assessed via measurement of esophageal, gastric, and transdiaphragmatic pressures. The energetic demands of inspiratory muscle contraction were estimated using the pressure–time index (6,41). We hypothesized that inspiratory rib cage muscle pressure development would increase at a rate exceeding that of the diaphragm during the struggle phase. It was also expected that expiratory rib cage and abdominal muscle pressures would progressively rise throughout the struggle phase.
Subjects and ethical approval
Eight trained male divers (28 ± 2 yr, 182 ± 2 cm, 76 ± 8 kg) volunteered to participate in the present study and provided written informed consent. The subjects underwent a preparticipatory health screening to ensure they were physically active nonsmokers, with no history of cardiac or pulmonary disease. The present study conformed to the principles outlined in the Declaration of Helsinki and was approved by the institutional Human Research Ethics Committee. We purposely chose to recruit trained apnea divers because these individuals are accustomed to extended periods of breath holding and, perhaps most importantly, are familiar with the respiratory contractions that arise toward the end of maximal apnea (i.e., struggle phase).
The participants arrived at the laboratory approximately 30–40 min before the start of the experiment. Subjects performed some pulmonary function and respiratory muscle performance tests in the upright and supine postures, after which they were instructed to remain supine for a further 10 min before performing the BH maneuvers (i.e., baseline period). The subjects were encouraged to completely relax during the early period of the BH (easy-going phase) and, should the urge arise, allow respiratory contractions to develop “naturally.” No further explanation of the nature of respiratory contractions was provided. The BH maneuvers commenced after full inflation to total lung capacity (TLC) while wearing a nose-clip and the glottis closed. Subjects were asked to refrain from performing preparatory hyperventilation and were not allowed to perform glossopharyngeal insufflations before the maneuver. The subjects completed two practice trials followed by two to three experimental breath holds, separated by at least 7–10 min.
Pulmonary function, arterial O2 saturation, and respiratory pressures
Before each experiment, subjects performed a forced vital capacity (FVC) and slow vital capacity maneuver while in the upright and supine postures (Quark PFT; Cosmed, Rome, Italy). The slow vital capacity test was used to determine the subject’s resting inspiratory capacity (IC). All pulmonary function testing was performed and reported in accordance with American Thoracic Society guidelines (25). Arterial saturation of oxyhemoglobin (SaO2) was measured via finger pulse oximetry (Poet II; Criticare Systems, Waukesha, WI). Esophageal (Poes) and gastric pressures (Pga) were measured using two latex balloon-tip catheters (Ackrad Laboratories, CooperSurgical, Trumbull, CT) advanced through the nose into the esophagus and stomach, respectively (24). The catheter balloons were then inflated with 1 mL of air. The “occlusion” test (5) was performed to ensure correct placement of the esophageal catheter (i.e., lower third of the esophagus). Ideal placement of the gastric catheter was confirmed when Pga rose during inspiration and fell throughout a relaxed expiration. Each catheter was connected to a differential pressure transducer (PX138-005D5V; Omega Engineering Inc., Stamford, CT). The transducers were calibrated before each test using a hand-held manometer (HHP-90, Omega Engneering Inc.).
Before the experimental trials, the subjects were instructed to perform a number (two to three trials) of maximal static inspiratory efforts at TLC. Maximal inspiratory esophageal pressure was obtained during a Mueller maneuver performed against a closed glottis, with specific emphasis placed on using the muscles of the “upper chest” while keeping the “belly” muscles relaxed. In this maneuver, the maximal inspiratory swing in the Poes signal is assumed to predominantly reflect pressure development of the inspiratory rib cage muscles. Transdiaphragmatic pressure (Pdi) was calculated via subtraction of Poes from the Pga signal. The maximal inspiratory Pdi was obtained during a Mueller maneuver combined with an expulsive effort (6). Visual feedback of the Poes and Pdi signal traces was provided during the maximal inspiratory efforts using computer display. Maximal inspiratory Poes and Pdi were reported as the absolute difference between peak values obtained during the mentioned maneuvers minus the elastic “recoil” pressure at TLC (see succeeding data).
Respiratory pressure signals were sampled continuously at 1000 Hz (Powerlab 16SP; ADInstruments Inc., Castle Hill, Australia) and stored on a personal computer for off-line analyses. These signals were low-pass filtered at 10 Hz to minimize the effect of cardiogenic oscillations on the Poes and Pga traces. The onset of inspiratory effort was defined as the rapid downswing in Poes simultaneous with an upswing in Pdi. The end of inspiratory effort was determined as the minima and maxima of the Poes and Pdi traces, respectively. The time elapsed between these two points represented the duration of inspiratory effort (TI) (27). The duration of expiratory effort (TE) was calculated as the time elapsed between inspiratory efforts. From these data, the number of respiratory efforts, inspiratory duty cycle (TI/TTOT), and respiratory frequency (fR) were determined.
Surface electromyography (sEMG) was continuously recorded from the right sternocleidomastoid, parasternal intercostal (PSIC), external oblique, and rectus abdominis muscles during the experiment (15). The direct current offset of sEMG data was removed and the signals filtered with a 53- to 1000-Hz digital band-pass filter. The monitoring of respiratory sEMG activity indicated that subjects’ respiratory muscles were relaxed (or nearly so) during the initial 5–20 s of the easy-going phase (Fig. 1). From these observations, it was reasoned that respiratory pressures observed during this phase of the BH were representative of elastic “recoil” and not active pressures developed by the respiratory muscles. The elastic recoil pressures on the esophageal, transdiaphragmatic, and gastric pressure signal traces were calculated as the respective mean over a 5- to 10-s window during the early easy-going phase with the least respiratory sEMG activity (Fig. 1).
The active pressures developed by the rib cage muscles during inspiration (Prcm,i) and expiration (Prcm,e) were determined using the two-compartment rib cage model proposed by Ward et al. (37) and further developed by others (19). In brief, the pressure at the pleural surface (Ppl) is determined by the balance of pressures acting across the rib cage directly apposed to the surface of the lungs: Ppl = Prc,p − Prcm, where Prc,p is the elastic recoil of the pulmonary apposed rib cage. When Prcm is nil during relaxation, then Ppl = Prc,p. At any instant where Ppl ≠ Prc,p, the rib cage muscles are presumed to be active, where Prcm = Prc,p − Ppl; and if Ppl is approximated by esophageal pressure, then Prcm = Prc,p − Poes. For clarity, we have reported Prcm,i and Prcm,e as absolute magnitudes, and distortive forces acting on the pulmonary rib cage are neglected. It is cautioned, however, that the given derivations do not imply that rib cage muscles are the sole modulators of Ppl swings during respiratory efforts. The two-compartment model of rib cage mechanics states that Prcm is also equal to the sum of Pdi plus the tension developed by the diaphragm in the caudal direction (i.e., the insertional component, let this be xPdi), minus the fraction of abdominal muscle pressure development acting to deflate the rib cage (let this be yPabm). Thus, Prcm = (x + 1)Pdi − yPabm (for further description of this model, see Refs. (19,37)). The pressures developed by the diaphragm during inspiration (Pdi,i) and those of the abdominal muscles during expiration (Pabm,e) were calculated as the difference between values observed at the end of inspiration and expiration, respectively, and the corresponding recoil pressure obtained during the early easy-going phase. The inspiratory pressure–time index of the rib cage (PTIrcm) and diaphragm (PTIdi) were calculated using the equation
is the mean pressure obtained during inspiration and Pmax is the maximal pressure achieved during the forceful inspiratory maneuvers described earlier (minus the recoil pressure at TLC).
The data obtained in the present study were averaged across repeated trials. Then, data were averaged into five time-locked bins representing 20% epochs of the struggle phase duration. Apart from the elastic recoil pressures obtained during the early period of breath holding, data from the easy-going phase were not formally investigated. Two-way ANOVA were used to determine the effect of time (i.e., percentage of struggle phase) and muscle group (e.g., inspiratory rib cage vs diaphragm) on respiratory pressure development and pressure–time indices during the struggle phase. Pairwise comparisons were assessed using the Bonferroni post hoc adjustment. Results are presented as mean ± SEM and were analyzed using SPSS 17.0 (SPSS, Inc., Chicago, IL). Statistical analyses were considered significant if P < 0.05.
The subjects demonstrated normal pulmonary function in both upright and supine postures (Table 1). There was a small but significant decline in forced expiratory volume in 1 s when individuals performed FVC maneuvers in the supine compared with the upright position (P < 0.05). Resting IC values were significantly greater when subjects were supine compared with upright (P < 0.05). Resting end-expiratory Poes, Pdi, and Pga were −1.7 ± 0.2, 8.1 ± 0.8, and 6.5 ± 1.6 cm H2O, respectively. These values were taken to represent elastic “recoil” pressures at functional residual capacity in the supine position. End-inspiratory values of Poes and Pdi were −5.9 ± 0.7 and 16.3 ± 1.3 cm H2O, respectively. Accordingly, Prcm,i and Pdi,i, while resting supine, were 4.2 ± 0.8 and 8.2 ± 1.6 cm H2O, respectively. Prcm,e and Pabm,e were nil by nature of the calculations involved. The subjects’ average BH duration was 209 ± 15 s. The group mean duration of the easy-going and struggle phases was 115 ± 13 s (55% ± 4% of total BH) and 94 ± 9 s (45% ± 4% of total), respectively. All subjects displayed significant (P < 0.05) arterial oxyhemoglobin desaturation during the BH maneuver, with values decreasing from rest (99% ± 1%) to a nadir (82% ± 4%) occurring approximately 30 s after the end of breath holding.
Table 2 reports the timing of respiratory contractions at rest and during the struggle phase. The duration of inspiratory effort (i.e., TI) was significantly shorter than resting values by the 60% epoch of the struggle phase (P < 0.05), whereas the duration of expiratory effort (i.e., TE) had significantly shortened below resting values by the 40% epoch (P < 0.05). Both TI and TE continued to decrease after these time points during the struggle phase (P < 0.05). The mentioned changes in the timing of respiratory contractions mediated a sustained increase in the inspiratory duty cycle (i.e., TI/TTOT) and fR throughout this phase of the BH (P < 0.05).
The average “recoil” pressures obtained at TLC for Poes, Pdi, and Pga signals were 8.2 ± 1.9, 6.3 ± 1.0, and 14.4 ± 1.9 cm H2O, respectively. Figure 2 displays the raw Poes, Pdi, and Pga tracings of a representative individual performing a maximal BH at TLC. It is noted that the inspiratory (downward) and expiratory (upward) swings in Poes increased in both frequency and magnitude over the duration of the struggle phase. Moreover, the inspiratory and expiratory peaks of the Pdi and Pga tracings became progressively more positive (larger) over the same period. These changes were typical of the entire subject group. Figure 3 illustrates the average time-course changes in respiratory pressure development during the struggle phase. Prcm,i and Pdi,i continuously increased from the beginning of the struggle phase until the break point (20% through to 100% epoch, P < 0.05). Pdi,i was systematically higher than Prcm,i throughout the struggle phase (P < 0.05). Net inspiratory pressure development was primarily contributed by the diaphragm at the start of the struggle phase but had shifted toward that of the inspiratory rib cage muscles by the end of the BH, evidenced by the decline in the Pdi,i/Prcm,i ratio by the 60% epoch of the struggle phase (P < 0.05).
Both Prcm,e and Pabm,e increased with time at a relatively late stage of the struggle phase (80% epoch, P < 0.05). The absolute level of Pabm,e was significantly higher than Prcm,e during the early struggle phase (20% and 40% epochs, P < 0.05); thereafter, no difference in pressures between these expiratory muscles were observed. In a similar fashion to the inspiratory muscles, the Pabm,e/Prcm,e ratio had significantly decreased by the 60% epoch of the struggle phase (P < 0.05), suggesting that expiratory rib cage muscles were progressively increasing their contribution to net expiratory pressure development toward the end of maximal breath holding.
The maximal static inspiratory Poes and Pdi obtained at TLC while resting supine were −47.9 ± 7.4 and 68.2 ± 7.4 cm H2O, respectively, after elastic “recoil” was taken into account. Figure 4 displays the time-course changes in mean pressures and pressure–time indices of the diaphragm and rib cage muscles during inspiration (i.e., PTIdi and PTIrcm). Mean pressures (expressed relative to maximum) and pressure–time indices of the diaphragm and inspiratory rib cage muscles progressively increased during the struggle phase (P < 0.05). The increase in PTIrcm was greater than the rise in PTIdi from the 60% epoch of the struggle phase onward (P < 0.05).
The major findings of the present study were that i) pressure development of the inspiratory and expiratory muscles progressively increases during the struggle phase, ii) the muscles of the rib cage appear to increase their contribution to net inspiratory/expiratory pressure output by the end of maximal breath holding, and iii) the energetic demand of muscular contractions produced by the diaphragm and inspiratory rib cage muscles rises by approximately 5- and 15-fold, respectively, from the beginning to the end of the struggle phase.
It is reported that the frequency and magnitude of respiratory contractions augments over the duration of the struggle phase (22,39). However, the precise involvement of inspiratory and expiratory muscles during such contractions is much less certain. The weight of available evidence accrued from separate investigations suggests that the diaphragm, inspiratory rib cage, and expiratory abdominal muscles are progressively recruited during the struggle phase of a maximal BH (1,20,32,33,39). Our data support these findings, insofar as Pdi,i, Prcm,i, Pabm,e, and Prcm,e progressively increased over the struggle phase duration (Figs. 2 and 3). It has been suggested that such a distinctive “crescendoing” pattern of respiratory neuromuscular output during breath holding is qualitatively similar to that observed during elastic loaded breathing (38). We did observe not only that expiratory muscle pressure development increased during the struggle phase, but also that Pdi,i/Prcm,i and Pabm,e/Prcm,e ratios declined by the end of breath holding (Fig. 3). These findings indicate that the rib cage muscles had increased their contribution to net inspiratory/expiratory pressure development toward the end of the struggle phase. Parthasarathy et al. (26) reported a similar pattern of respiratory muscle recruitment during failed weaning trials from mechanical ventilation, wherein larger than normal sternomastoid/rib cage muscle recruitment was observed soon after weaning had begun, and expiratory pressure development increased only toward the latter stages of the failed weaning trials. It is thought that preferential recruitment of inspiratory rib cage muscles during failed weaning trials represents a compensatory response to a high mechanical load to breathing (particularly the elastic component of inspiratory work). Indeed, heavy elastic loaded breathing is associated with a preferential recruitment of inspiratory rib cage muscles relative to that of the diaphragm, commensurate with increasing expiratory activation of the abdominal muscles (23). Based on our findings and those mentioned, the “extradiaphragmatic” shift of inspiratory muscle recruitment during the struggle phase, together with the progressive increases in Prcm,e and Pabm,e, may represent an extreme loading response to breathing against a heavy elastance (e.g., closed glottis). The mechanisms responsible for this characteristic recruitment pattern during breath holding are unclear, although it is probably mediated by cortical inputs and reflexes originating from the inspiratory intercostal and accessory muscles during quasi-isometric contraction (34,35).
From a teleological viewpoint, the shifting of heavy respiratory loads from the diaphragm to the rib cage/accessory muscles may serve as an “adaptive” strategy to delay the onset of diaphragmatic fatigue (21,30,40). In the case of breath holding, however, one cannot discount the possibility that the increasing contribution of rib cage muscles to inspiratory efforts may simply reflect the characteristic recruitment patterns observed during progressive hypercapnia (28). Whatever the reasons for this “extradiaphragmatic” shift in respiratory muscle recruitment, one may pose the following question: Does this observation imply that the rib cage muscles develop inspiratory pressures at levels progressively encroaching upon maximal values during breath holding? If so, what are the energetic consequences for these muscles, and of the diaphragm for that matter, during the struggle phase of a maximal BH?
The tension– or pressure–time index is closely related to the O2 consumption and energy utilization of the active muscle (9,14). That is, an increase in the pressure–time index corresponds to a rise in the energetic demands of muscular contraction. Accordingly, we estimated the energetic demand of inspiratory muscle contraction by calculating the pressure–time indices of the diaphragm (PTIdi) and rib cage muscles (PTIrcm) as others have done (6,9,41). It was observed that PTIdi and PTIrcm increased by approximately 5- and 15-fold, respectively, over the duration of the struggle phase. Moreover, PTIrcm was significantly higher than PTIdi toward the end of breath holding (Fig. 4). These findings suggest that not only did the energetic demands of the inspiratory muscles increase inexorably over the struggle phase, but also energy expenditure of the rib cage muscles was most probably higher than that of the diaphragm.
It is curious that PTIdi and PTIrcm values at the break point were, on average, similar to those known to cause task failure of the diaphragm and rib cage muscles. Bellemare and Grassino (6) determined that the likelihood of diaphragm task failure greatly increases when PTIdi exceeds 0.15, whereas Zocchi et al. (41) reported that this “critical” value for PTIrcm occurred at 0.30. Certainly, the subjects of the present study were hypoxemic by the break point (i.e., SaO2 <85%), suggesting the respiratory muscles suffered inadequate O2 delivery toward the end of breath holding. Under hypoxic conditions, it can be reasoned that the threshold of contractile fatigue, as approximated by a “critical” pressure–time index, would be lower for any given skeletal muscle group (4,31). Indeed, the prevalence of diaphragmatic fatigue is higher during spontaneous breathing under hypoxic compared with normoxic conditions (18,29,36). In addition to the above findings, it is reported that inspiratory muscle fatigability is increased at relatively high end-expiratory lung volumes (i.e., hyperinflation), consequent to a reduced mechanical advantage and muscle fiber shortening (7,30). It is therefore reasonable to suggest that the “critical” pressure–time index for inspiratory muscle task failure, and thus contractile fatigue, was also lower for our subjects while breath holding because end-expiratory lung volume remained close to TLC (i.e., extreme hyperinflation).
Although our data do not provide direct evidence of fatigue per se, the aforementioned rationale does suggest that both the diaphragm and rib cage muscles were developing potentially “fatiguing” contractions by the end of the struggle phase. We reason that the relatively high values for PTIdi and PTIrcm observed during the struggle phase may contribute to a “fatiguing” work history of the inspiratory muscles, causing contractile fatigue to develop after some breath holds are performed in rapid succession. This last point may be particularly important for recreational and experienced apnea divers, who experience repeated episodes of prolonged breath holding during subaquatic events such as spearfishing competitions. Future studies using direct measurements of respiratory muscle contractility (e.g., supramaximal stimulation techniques) are required to determine whether repetitive maximal breath holding induces significant fatigue of the respiraory muscles in trained apnea divers. Moreover, it would be of interest to ascertain whether such fatigue (if indeed it exists) contributes to the growing “urge to breathe” during the struggle phase, thereby lending insight into the genesis of dyspnea under circumstances where the energetic demands of respiratory muscles are high and systemic O2 delivery is low or impaired (e.g., heart failure (8)).
Critique of methods
The inferences drawn from our data rely heavily on the accurate determination of elastic recoil and maximal inspiratory pressures obtained at TLC. It is acknowledged that alveolar gas exchange continues while breath holding, reducing thoracic volume and changing the elastic recoil pressures used in the calculation of active respiratory pressures (2). In addition, the pressure-generating capacity of the diaphragm and inspiratory rib cage muscles increases with decreasing lung volume (10,11). The rate of decline in thoracic volume during breath holding may be approximated at 124 mL·min−1 for trained divers (12,13,17). It is estimated that our subjects’ lung volume decreased by roughly 335 ± 25 mL or 5% ± 1% of vital capacity by the end of breath holding. This relatively small decline in lung volume is unlikely to have significantly affected our measures of respiratory muscular effort and therefore would not have changed the trends observed in our data. Nevertheless, future works may circumvent these concerns by monitoring changes in chest wall volume during breath holding via inductance or optoelectronic plethysmography.
The trained divers of the present study were examined under dry conditions in the laboratory—an environment far removed from the subaquatic conditions of free-diving/spearfishing etc. When diving to depth, thoracic gas volume decreases consequent to the rising extrathoracic pressure exerted by the surrounding water (i.e., Boyle’s law). This decrease in thoracic volume would facilitate the inspiratory muscles by increasing their pressure-generating capacity (see previous data), which may, in turn, affect a different pattern of respiratory muscle pressure development to that observed in the present study. Therefore, our data may not readily transfer to breath holding under water at depth. Moreover, each participant reported that they were familiar with the development of strong “diaphragmatic” contractions during their dives. There exists the possibility that the characteristic patterns of respiratory pressure development observed in these divers may have been “learned” over the course of many repeated apneas. Future studies should explore the influence of breath holding experience (e.g., naive vs trained participants) on the pattern of respiratory muscle recruitment during the struggle phase and determine whether these respiratory contractions are truly “involuntary” or can be modulated by “conscious” effort.
This study is the first to characterize the pattern of diaphragm, rib cage, and abdominal muscle pressure development during maximal breath holding in trained apnea divers. We report that inspiratory rib cage pressure development increases at a rate exceeding that of the diaphragm during the struggle phase, commensurate with rising expiratory pressures contributed by the rib cage/abdominal muscles toward the latter stages of breath holding. These observations support the notion that maximal breath holding evokes a pattern of respiratory muscle recruitment (and pressure development) that is qualitatively similar to breathing against extremely heavy elastic loads. Moreover, the energetic demand of diaphragmatic and inspiratory rib cage muscle contractions rises during the struggle phase, to the extent that PTIdi and PTIrcm values approach potentially “fatiguing” levels by the break point. Whether repeated maximal breath holding, with the attendant struggle phase, induces contractile fatigue of the inspiratory muscles remains to be determined.
This study was supported by the Croatian Ministry of Science, Education and Sports Grant No. 216-2160133-0130. TJC was supported by an Australian Postgraduate Award and a Griffith University International Exchange Incentive Scheme Grant.
The authors thank each subject for their enthusiastic participation in the present study. The authors are also grateful for the skillful advice provided by Dr. J. Kavanagh during the preparation of this manuscript.
The authors declare no conflict of interest.
The results of the present study do not constitute endorsement by the American College of Sports Medicine.
1. Agostoni E. Diaphragm activity during breath holding: factors related to its onset. J Appl Physiol
. 1963; 18: 30–6.
2. Agostoni E, Rahn H. Abdominal and thoracic pressures at different lung volumes. J Appl Physiol
. 1960; 15: 1087–92.
3. Banzett RB, Lansing RW, Brown R, et al.. ‘Air hunger’ from increased PCO2
persists after complete neuromuscular block in humans. Respir Physiol
. 1990; 81: 1–17.
4. Bark H, Supinski G, Bundy R, Kelsen S. Effect of hypoxia on diaphragm blood flow, oxygen uptake, and contractility. Am J Respir Crit Care Med
. 1988; 138: 1535–41.
5. Baydur A, Cha EJ, Sassoon CS. Validation of esophageal balloon technique at different lung volumes and postures. J Appl Physiol
. 1987; 62: 315–21.
6. Bellemare F, Grassino A. Effect of pressure and timing of contraction on human diaphragm fatigue. J Appl Physiol
. 1982; 53: 1190–5.
7. Collett PW, Engel LA. Influence of lung volume on oxygen cost of resistive breathing. J Appl Physiol
. 1986; 61: 16–24.
8. Cross TJ, Sabapathy S, Beck KC, Morris NR, Johnson BD. The resistive and elastic work of breathing during exercise in patients with chronic heart failure. Eur Respir J
. 2012; 39: 1449–57.
9. Crow MT, Kushmerick MJ. Chemical energetics of slow- and fast-twitch muscles of the mouse. J Gen Physiol
. 1982; 79: 147–66.
10. De Troyer A, Wilson TA. Effect of acute inflation on the mechanics of the inspiratory muscles. J Appl Physiol
. 2009; 107: 315–23.
11. DiMarco AF, Romaniuk JR, Supinski G, Kowalski KE. Effects of lung volume on parasternal pressure-generating capacity in dogs. Exp Physiol
. 2000; 85: 331–7.
12. Ferretti G. Extreme human breath-hold diving. Eur J Appl Physiol
. 2001; 84: 254–71.
13. Ferretti G, Costa M, Ferrigno M, et al.. Alveolar gas composition and exchange during deep breath-hold diving and dry breath holds in elite divers. J Appl Physiol
. 1991; 70: 794–802.
14. Field S, Sanci S, Grassino A. Respiratory muscle oxygen consumption estimated by the diaphragm pressure–time index. J Appl Physiol
. 1984; 57: 44–51.
15. Gandevia SC, McKenzie DK, Plassman BL. Activation of human respiratory muscles during different voluntary manoeuvres. J Physiol
. 1990; 428: 387–403.
16. Godfrey S, Campbell EJ. The control of breath holding. Respir Physiol
. 1968; 5: 385–400.
17. Hong SK, Lin YC, Lally DA, et al.. Alveolar gas exchanges and cardiovascular functions during breath holding with air. J Appl Physiol
. 1971; 30: 540–7.
18. Jardim J, Farkas G, Prefaut C, Thomas D, Macklem PT, Roussos C. The failing inspiratory muscles under normoxic and hypoxic conditions. Am Rev Respir Dis
. 1981; 124: 274–9.
19. Kenyon CM, Cala SJ, Yan S, et al.. Rib cage mechanics during quiet breathing and exercise in humans. J Appl Physiol
. 1997; 83: 1242–55.
20. Kulik AM. Electric activity of the respiratory muscles in man during breath holding. Biull Eksp Biol Med
. 1964; 13: 27–33.
21. Laghi F, Topeli A, Tobin MJ. Does resistive loading decrease diaphragmatic contractility before task failure? J Appl Physiol
. 1998; 85: 1103–12.
22. Lin YC, Lally DA, Moore TO, Hong SK. Physiological and conventional breath-hold breaking points. J Appl Physiol
. 1974; 37: 291–6.
23. Mengeot PM, Bates JH, Martin JG. Effect of mechanical loading on displacements of chest wall during breathing in humans. J Appl Physiol
. 1985; 58: 477–84.
24. Milic-Emili J, Mead J, Turner JM, Glauser EM. Improved technique for estimating pleural pressure from esophageal balloons. J Appl Physiol
. 1964; 19: 207–11.
25. Miller MR, Hankinson J, Brusasco V, et al.. Standardisation of spirometry. Eur Respir J
. 2005; 26: 319–38.
26. Parthasarathy S, Jubran A, Laghi F, Tobin MJ. Sternomastoid, rib cage, and expiratory muscle activity during weaning failure. J Appl Physiol
. 2007; 103: 140–7.
27. Parthasarathy S, Jubran A, Tobin MJ. Assessment of neural inspiratory time in ventilator-supported patients. Am J Respir Crit Care Med
. 2000; 162: 546–52.
28. Pengelly LD, Tarshis AM, Rebuck AS. Contribution of rib cage and abdomen–diaphragm to tidal volume during CO2
rebreathing. J Appl Physiol
. 1979; 46: 709–15.
29. Radell PJ, Eleff SM, Nichols DG. Effects of loaded breathing and hypoxia on diaphragm metabolism as measured by 31
P-NMR spectroscopy. J Appl Physiol
. 2000; 88: 933–8.
30. Roussos C, Fixley M, Gross D, Macklem PT. Fatigue of inspiratory muscles and their synergic behavior. J Appl Physiol
. 1979; 46: 897–904.
31. Roussos CS, Macklem PT. Diaphragmatic fatigue in man. J Appl Physiol
. 1977; 43: 189–97.
32. Sempik A, Patrick JM. The effect of thoracic vibration on ventilation and breath-holding in man. Respir Physiol
. 1981; 44: 381–91.
33. Sempik AK. An electromyographic study of intercostal muscle activity in man during breath-holding [proceedings]. J Physiol
. 1978; 276: 10P–11P.
34. Shannon R Reflexes from respiratory muscles and costovertebral joints. In: Cherniack NS, Widdicombe JGeditors. Handbook of Physiology. Section 3. The Respiratory System
. Washington (DC): American Physiological Society; 1986. pp. 431–47.
35. Similowski T, Raux M, Straus C, et al.. Electroencephalographic evidence for pre-motor cortex activation during inspiratory loading in humans. J Physiol
. 2007; 578: 569–78.
36. Vogiatzis I, Georgiadou O, Koskolou M, et al.. Effects of hypoxia on diaphragmatic fatigue in highly trained athletes. J Physiol
. 2007; 581: 299–308.
37. Ward ME, Ward JW, Macklem PT. Analysis of human chest wall motion using a two-compartment rib cage model. J Appl Physiol
. 1992; 72: 1338–47.
38. Whitelaw WA, Derenne J, Noble S, McBride B. Similarities between behavior of respiratory muscles in breath-holding and in elastic loading. Respir Physiol
. 1988; 72: 151–61.
39. Whitelaw WA, McBride B, Amar J, Corbet K. Respiratory neuromuscular output during breath holding. J Appl Physiol
. 1981; 50: 435–43.
40. Yan S, Lichros I, Zakynthinos S, Macklem PT. Effect of diaphragmatic fatigue on control of respiratory muscles and ventilation during CO2
rebreathing. J Appl Physiol
. 1993; 75: 1364–70.
41. Zocchi L, Fitting JW, Majani U, Fracchia C, Rampulla C, Grassino A. Effect of pressure and timing of contraction on human rib cage muscle fatigue. Am J Respir Crit Care Med
. 1993; 147: 857–64.
Keywords:©2013The American College of Sports Medicine
RESPIRATORY; MECHANICS; PRESSURES; APNEA