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Department of Physiology, Showa University School of Medicine, Tokyo, Japan
Submitted 20 December 2005 ; accepted in final form 24 March 2006
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ABSTRACT |
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 TOP ABSTRACT MATERIALS AND METHODSRESULTSDISCUSSIONGRANTSACKNOWLEDGMENTSREFERENCES |
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functional residual capacity; hyperinflation; inspiratory capacity
Thixotropy is a property generally shown by some materials such as gels. A thixotropic substance shows a temporary reduction in viscosity when stirred, because stirring forces disrupt bonds between molecules, which are reformed when the stirring forces cease. The substance then returns to its previous solid state. The original basic observations concerning muscle thixotropy were made on relaxed frog muscle fibers (16). Subsequent studies have shown obvious signs of thixotropy in human skeletal muscles (12, 14, 22, 26).
Thixotropy causes muscle stiffness or slackness, depending on the history of the muscle (12, 14, 22, 26). The passive response of a muscle to stretching is changed by the immediate history of muscle contraction and length changes, depending on whether the muscle was contracted immediately beforehand at a long length (hold-long) or at a short length (hold-short). This process results in stiffness of the muscle with hold-short conditioning, whereas it results in slackness of the muscle with hold-long conditioning. Stable cross bridges, which are distinguishable from actively cycling bridges, are a primary source of this history-dependent passive muscle character (32). Proske and colleagues (12, 26) proposed that stable cross bridges can be detached by stretching or by conditioning contraction, and the bridges are reformed at their length within a few seconds after detachment. If the muscle is shortened after stable cross bridges have formed at a long length (hold-long conditioning), the fibers will be unable to absorb the length change and they will fall slack; if the muscle is lengthened after stable cross bridges have formed at a short length (hold-short conditioning), no slackness develops (12, 26). Whitehead et al. (32) also showed that hold-long conditioning of a muscle reduces resting tension of the muscle.
Conditioning for developing inspiratory muscle thixotropy involves inspiratory muscle contraction at an inflated or deflated lung volume (VL) (18, 20, 27). Inspiratory muscles include the diaphragm, the external intercostals, and the parasternal intercostals, and these muscles shorten and lengthen with lung inflation and deflation, respectively (3, 5–7). Conditioning at an inflated VL, which corresponds to hold-short conditioning to increase muscle stiffness, is followed by an increase in end-expiratory position of the rib cage of subsequent breath cycles. Conditioning at a deflated VL, which corresponds to hold-long conditioning to cause muscle slackness, is followed by a reduction in end-expiratory position of the rib cage (18, 20, 27). Passive tension generated in inspiratory muscles seems an important component, particularly during expiration, because expiratory movements stretch passive inspiratory muscles to reduce VL, which may lead to dynamic changes in end-expiratory chest wall volume and thus VL. Changes in resting tension of inspiratory muscles may contribute to changes in these end-expiratory volumes.
The present study was performed to determine whether thixotropy conditioning of inspiratory muscles affects chest wall movement in normal human subjects. Changes in end-expiratory chest wall volume (Vcw) have been investigated in relation to respiratory diseases such as bronchial asthma and chronic obstructive pulmonary disease, in which the rib cage compartment, not the abdominal compartment, accounts for acute chest wall hyperinflation (2, 9, 10). The primary purpose of the present study was to test the hypothesis that thixotropic changes in end-expiratory Vcw could be shared unequally by the rib cage and abdominal components. We examined the acute effects of thixotropy conditioning of inspiratory muscles on chest wall movement, which was modeled as the sum of the rib cage and abdominal movements (21). A secondary purpose of this study was to examine the effects of thixotropy conditioning on end-expiratory VL (end-expiratory VL). We measured the effects on spirometrically determined inspiratory capacity (IC), an indirect estimate of end-expiratory VL. We also compared helium-dilution end-expiratory VL before and after conditioning. If overall chest wall inflation and deflation occur after conditioning, these should be reflected in changes in the IC and end-expiratory VL.
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MATERIALS AND METHODS |
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TOPABSTRACTMATERIALS AND METHODSRESULTSDISCUSSIONGRANTSACKNOWLEDGMENTSREFERENCES |
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The study was performed in 31 healthy men (aged 21–33 yr) with no history of chronic pulmonary or neuromuscular disease and was approved by the ethics committee of Showa University. All subjects gave their written, informed consent for participation in the study.
Experiment 1
We studied the immediate effects of thixotropy conditioning of inspiratory muscles on chest wall movements using respiratory induction plethysmography (RIP; Respitrace system, Ambulatory Monitoring, Ardsley, NY) in eight subjects (subjects 1–8). The effects of inspiratory effort and VL at which conditioning occurred on end-expiratory Vcw in five subsequent breathing cycles were studied based on measurements of the rib cage (Vrc) and abdominal volume (Vab).
Apparatus. The subject was seated on a chair during trials with their nose clipped and wearing a mouthpiece to which a transducer (AR-601G, Nihon Kohden, Tokyo, Japan) was attached for measurement of mouth pressure. A magnetically driven mouthpiece shutter was triggered manually to close the airway. We measured respiration by RIP and a respiratory flowmeter (RF-2, Minato Medical, Osaka, Japan), and we estimated the cross-sectional areas of the rib cage and the abdomen using RIP operated in the direct-current mode. Rib cage and abdominal movements during respiration changed the inductance of the bands, and changes in inductance were converted to proportional voltage changes. RIP was calibrated by the least squares method (30). All data were fed into a computerized analysis system (PowerLab, ADInstruments, Castle Hill, Australia).
Baseline IC and expiratory reserve volume (ERV) were estimated with the flowmeter at least twice before the experiment. IC was measured when the subject took a slow full inspiration with no hesitation from a position of end-tidal expiration. ERV was measured when the subject took a slow full expiration from a position of end-tidal expiration. Each measurement was performed 1 min after an inspiratory maneuver to total lung capacity (TLC maneuver). Maximal inspiratory mouth pressures at three VL levels [60% IC + end-expiratory VL of baseline breathing (EELVB), EELVB, and residual volume (RV)] were also determined.
Protocol. The protocol included six different types of thixotropy-conditioning maneuvers. The subject was instructed to make an inspiratory effort at one of the three levels of VL (60% IC + EELVB, EELVB, and RV) at one of two levels of inspiratory effort (maximal inspiratory effort and no voluntary inspiratory effort) in random order. Muscle contractions were maintained for 5 s with subsequent relaxation for 2–3 s with the airway closed. After each conditioning maneuver, the shutter was reopened and the subject resumed quiet breathing. In trials with "no voluntary inspiratory effort," no voluntary inspiratory effort was made for 7–8 s at each of the volumes before the airway was released.
The VL signal was monitored online to determine when the airway was closed during trials. A read-out of the mouth pressure enabled us to provide the subject with verbal encouragement to continue effort during conditioning. Trials were separated by rest periods of at least 3 min. The TLC maneuver preceded all tests, and the Respitrace traces were maintained in a semi-steady state for at least 1 min before the start of each trial.
For quantitative analysis, the mean end-expiratory volume of the five breaths taken immediately before each conditioning was defined as the zero level for each RIP trace. Differences in end-expiratory volume between the zero line and after each conditioning were measured over the next five end expirations in each RIP trace. We also measured mean inspiratory and expiratory tidal volume of five postrespiratory cycles, the first inspiration of which started from the first end expiration after conditioning.
Experiment 2
We examined the aftereffects of thixotropy conditioning on spirometrically determined IC. Thirteen volunteers (subjects 9–21) participated in this experiment. We measured changes in VL with the flowmeter before and after conditioning and monitored the changes online to determine when the airway was closed during trials. Before the start of this experiment, the baseline IC and ERV of each subject was measured with the flowmeter at least twice, and maximal inspiratory mouth pressures at each conditioning volume were also determined.
Protocol. Thixotropy conditioning was performed in a manner similar to that in experiment 1. After the TLC maneuver, the subject was instructed to make an inspiratory effort at one of the three levels of VL (60% IC + EELVB, EELVB, and RV) at one of two levels of inspiratory effort (maximal inspiratory effort and no voluntary inspiratory effort) in random order. In each trial, IC measurements were performed only once at one of the time points (30, 60, or 180 s) after conditioning because the IC measurement by itself would attenuate the effects of thixotropy conditioning in the subsequent breath cycles.
Experiment 3
We measured end-expiratory VL after thixotropy conditioning of inspiratory muscles using the helium-dilution method. Eleven volunteers (subjects 18–28) participated in this experiment.
Apparatus. A device designed to perform thixotropy conditioning of respiratory muscles enabled the subject to perform the conditioning at target VLs and mouth pressures (ChestTrainer, CHEST M.I., Tokyo, Japan). The apparatus consisted of a portable spirometer equipped with a mouthpiece shutter triggered manually to close the airway and with a pressure transducer to measure mouth pressure. ChestTrainer data were fed into a laptop computer, and the integrated flow signal was monitored online to determine when the airway was closed by the shutter.
Baseline IC and ERV were measured with the device at least twice before the experiment. The TLC maneuver preceded each baseline measurement. Maximal inspiratory mouth pressures at each conditioning volume were also determined. Baseline end-expiratory VL and TLC were measured with the multiple-breath helium dilution method (CHESTAC-33, CHEST M.I.) at least twice in each subject. During the measurements, oxygen was added to keep end-expiratory spirometer volume constant.
Protocol. The subject was instructed to produce maximal inspiratory effort at one of three VLs (60% IC + EELVB, EELVB, and RV) for 5 s with subsequent relaxation for 2–3 s with the airway closed. After each conditioning maneuver, the shutter was reopened and the subject resumed quiet breathing. The subject then released the mouthpiece attached to the ChestTrainer flow head and changed to another mouthpiece equipped with CHESTAC-33 as quickly and gently as possible. The subject was connected to the test gas at the end of expiration 30 s after conditioning, and helium-dilution end-expiratory VL was measured. Each conditioning maneuver was performed once in random order followed by a 10-min interval.
Experiment 4
As a complement to our analyses of shifts in end-expiratory volume, measurement of esophageal pressure (Pes), reflecting intrathoracic pressure, was performed in subjects 29–31 with a balloon catheter 100 cm in length (CHEST M.I.) positioned in the lower one-third of the esophagus with the balloon filled with 0.5 ml of air. The catheter was connected to a transducer (model AR-601G; Nihon Kohden). Changes in Pes were recorded before and after conditioning at three VLs (60% IC + EELVB, EELVB, and RV) with maximal inspiratory effort. The mean end-expiratory Pes of the five breaths taken immediately before each conditioning was defined as the zero level. Mean differences in end-expiratory Pes between the zero line and after each conditioning were measured over the next five end expirations.
Statistical Analysis
Results are expressed as means ± SE. In experiment 1, statistical inferences were made by two-way ANOVA for repeated measures to test for within-factor (inspiratory effort and breath, or inspiratory effort and conditioning volume) effects and interactions between the two effects. In experiments 2 and 3, one-way ANOVA followed by Dunnett's test was used to compare the results with baseline values. In experiment 2, mean IC values at a given time point were compared between the two levels of inspiratory effort by a paired t-test with Bonferroni correction. Significance was accepted at P < 0.05 for one- and two-way ANOVAs and P < 0.017 for the paired t-test.
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RESULTS |
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TOPABSTRACTMATERIALS AND METHODSRESULTSDISCUSSIONGRANTSACKNOWLEDGMENTSREFERENCES |
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RIP measurements showed that thixotropy conditioning of inspiratory muscles affected chest wall movements. Changes in Vrc, Vab, and Vcw for breaths before and after the conditioning maneuvers performed by a subject are illustrated in Fig. 1. The various types of conditioning are shown schematically at the bottom of the figure. Conditioning with maximal inspiratory effort was followed by shifts in end-expiratory Vcw in the opposite direction, depending on whether the lung was inflated or deflated at the time of conditioning. Both reductions and increases in end-expiratory volumes were greatest for the first breath after conditioning.
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Experiment 2
Figure 4 shows the time course of changes in IC after thixotropy conditioning of inspiratory muscles. Dunnett's tests to assess differences over time showed that conditioning at 60% IC + EELVB with maximal inspiratory effort was followed by a decrease in IC at 30 s and 60 s (both P < 0.05). However, this decrease had disappeared after 180 s. Conditioning at 60% IC + EELVB without voluntary inspiratory effort was also followed by a decrease in IC at 30 s (P < 0.05), which was not observed at 60 or 180 s. The IC decrease was more obvious after conditioning with than without maximal inspiratory effort (both P < 0.017). On the other hand, IC increased at 30, 60, and 180 s after conditioning at RV, irrespective of inspiratory effort (all P < 0.05). Differences in the IC with and without maximal inspiratory effort did not reach significance at any time point. After conditioning at EELVB with maximal inspiratory effort, a small decrease in IC was observed at 30 s compared with the baseline.
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Experiment 3
Helium-dilution end-expiratory VL at 30 s after conditioning was compared with the baseline end-expiratory VL value (3.50 ± 0.18 liters BTPS) (Fig. 5). The end-expiratory VL was higher after conditioning at 60% IC + EELVB (3.71 ± 0.16 liters BTPS; P < 0.05), whereas it was lower after conditioning at RV (3.36 ± 0.18 liters BTPS; P < 0.05). The end-expiratory VL after conditioning at EELVB (3.52 ± 0.18 liters BTPS) was similar to the baseline value. Differences between the end-expiratory VL and baseline end-expiratory VL were roughly comparable with those in end-expiratory Vcw at the fifth breath and IC at 30 s.
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Experiment 4
Traces of Vcw and Pes in subject 29 before and after conditioning at 60% IC + EELVB, EELVB, and RV with maximal inspiratory effort are shown in Fig. 6A. After conditioning at 60% IC + EELVB, end-expiratory Pes decreased with increases in end-expiratory Vcw. After conditioning at RV, the pressure increased with reductions in end-expiratory Vcw. End-expiratory Pes showed similar tendencies to decrease and increase in subjects 30 and 31. Mean differences of the three subjects in end-expiratory Pes between the zero line and after each conditioning are shown in Fig. 6B.
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DISCUSSION |
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TOPABSTRACTMATERIALS AND METHODSRESULTSDISCUSSIONGRANTSACKNOWLEDGMENTSREFERENCES |
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Rib cage movements largely accounted for the volume of chest wall inflation after conditioning at 60% IC + EELVB, whereas end-expiratory Vab hardly changed after this conditioning. This change in the chest wall shape after conditioning suggests that contribution of thixotropy to the diaphragm is smaller than that of rib cage inspiratory muscles. Although the mechanism of the difference in contribution was not identified, one possible explanation could be related to the small number of spindles in the diaphragm compared with rib cage inspiratory muscles (8). In limb skeletal muscles, intrafusal fibers of muscle spindles are found to have similar thixotropic properties as extrafusal fibers (11, 15, 26). By means of intrafusal thixotropy, hold-short conditioning of a skeletal muscle followed by stretch leads to an increase in Ia afferent discharge, which causes aftercontraction of the muscle (11, 15). Accordingly, stretch of hold-short conditioned rib cage inspiratory muscles during expiration could lead to an increase in Ia afferent discharge from their spindles. In humans, chest wall vibration on the upper rib cage causes an expansion of the rib cage by rib cage muscle contraction elicited by tonic vibration reflex (17). Aftercontraction of rib cage inspiratory muscles caused by intrafusal muscle thixotropy may partly account for the change in the rib cage inflation after conditioning at 60% IC + EELVB.
Conditioning at RV was followed by reductions in end-expiratory Vcw, which were distributed between the rib cage and abdominal compartments. This thixotropic deflation of the chest wall could be explained by not only slackness of inspiratory muscles after hold-long conditioning but also by stiffness of abdominal muscles. Using upper limb muscles, Hagbarth et al. (14) showed that forceful shortening contraction is followed by an enduring increase in stiffness of the muscle. Forceful contraction to exhale to RV could lead to stiffness of abdominal muscles, leading to the reduction in end-expiratory Vab.
Factors that could influence the thixotropic inflation and deflation of the chest wall also include respiratory reflexes mediated by vagal afferents. Lung inflation prolongs expiration in humans through vagally mediated pulmonary stretch receptors when the inflation volume exceeds a critical threshold of 40–60% IC (19). In the present study, although this reflex could affect the magnitude of the inflation after conditioning at EELVB + 60% IC, expiratory tidal volume was similar between conditionings. Exhalation to RV for conditioning may have activated the Hering-Breuer deflation reflex, which increases electrical activity in inspiratory muscles (13). This reflex could explain an increase in inspiratory tidal volume when the VL at which conditioning occurred decreased. It could also potentially decrease the thixotropic deflation of the chest wall.
Measurements of spirometrically determined IC support the view that thixotropy conditioning causes inflation and deflation of the lung during the following breathing cycles. The IC measurements also showed the time course of the aftereffect of thixotropy conditioning, suggesting that thixotropic inflation and deflation are maintained for at least 60 and 180 s, respectively. Hagbarth et al. (14) showed the lasting effect of muscle thixotropy in upper limb muscles that continues for more than 10 min, unless subsequent contractions or stretch of the muscles occurs. In the present study, the IC measurements suggest that the lasting effects of thixotropy conditioning of inspiratory muscles on end-expiratory VL were shorter than those measured in upper limb muscles, in particular after conditioning at EELVB + 60% IC.
IC measurements could not confirm enhancing effects of inspiratory effort on deflation after conditioning at RV, although this was detected by RIP measurements during the immediate breath cycles. This inconsistency could be due partly to methodological limitations of IC measurements, which are often used to detect dynamic hyperinflation during exercise in patients with chronic obstructive pulmonary disease (24, 25) based on the observation that TLC does not change during exercise (29). Because TLC may change if the force-generation capacity of inspiratory muscles is changed after thixotropy conditioning, the changes in IC might not necessarily mirror those in end-expiratory VL. Another possible explanation is that additional effects provided by the forceful inspiratory effort disappeared before IC measurements were performed. This possibility may be supported by the findings in Fig. 2A, which show that the additional effect was decreased from the first to the fifth end expiration.
Helium-dilution end-expiratory VL demonstrated the immediate effect of thixotropy conditioning on absolute VL. The changes in helium-dilution end-expiratory VL confirmed that inflation and deflation of the lung occurred after thixotropy conditioning. However, use of the helium-dilution method raises the concern that some of the volume shifts found may have been artefactual. Variations in end-expiratory VL during the measurements affect the rate at which oxygen is added to the circuit (4), which would lead to underestimation of end-expiratory VL after conditioning at EELVB + 60% IC and overestimation after conditioning at RV.
End-expiratory Pes changed after conditioning, suggesting that the inflation and deflation of the respiratory system are due to history-dependent mechanical properties of the chest wall rather than those of the lung. The TLC maneuver preceding each trial may have contributed to a reduction of the volume-history effect of the lung (23). However, because other structures in the chest wall also exhibit history dependence (1), it is necessary to obtain further evidence to clarify the magnitude of contribution of thixotropy of inspiratory muscles.
This study demonstrated that thixotropy conditioning of inspiratory muscles changes end-expiratory chest wall volume, spirometrically determined IC, and helium-dilution end-expiratory VL in normal human subjects. The partitioning of thixotropic volume changes in the chest wall compartments differed between hold-short and hold-long conditioning of inspiratory muscles.
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GRANTS |
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TOPABSTRACTMATERIALS AND METHODSRESULTSDISCUSSIONGRANTSACKNOWLEDGMENTSREFERENCES |
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ACKNOWLEDGMENTS |
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TOPABSTRACTMATERIALS AND METHODSRESULTSDISCUSSIONGRANTSACKNOWLEDGMENTSREFERENCES |
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FOOTNOTES |
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The costs of publication of this article were defrayed in part by the payment of page charges. The article must therefore be hereby marked "advertisement" in accordance with 18 U.S.C. Section 1734 solely to indicate this fact.
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REFERENCES |
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TOPABSTRACTMATERIALS AND METHODSRESULTSDISCUSSIONGRANTSACKNOWLEDGMENTSREFERENCES |
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) and without inspiratory effort (
). Values are means ± SE for 8 subjects. *Significant effect for breath, P < 0.05. #Significant effect for inspiratory effort, P < 0.05. !Significant interaction between the two effects, P < 0.05. B: mean values of the 5 end-expiratory volumes are shown. *Significant effect for conditioning volume, P < 0.05. #Significant effect for inspiratory effort, P < 0.05. !Significant interaction between the 2 effects, P < 0.05.
) and without inspiratory effort (
). Values are means ± SE for 13 subjects. *Significant difference from the baseline value, P < 0.05. #Significant difference between bars, P < 0.017.
, Mean difference. *Significant difference from the baseline value, P < 0.05.