Chest ACCP Education Calendar
HOME HELP FEEDBACK SUBSCRIPTIONS ARCHIVE SEARCH TABLE OF CONTENTS
QUICK SEARCH:   [advanced]


     

Guest Access | Sign In via User Name/Password
This Article
Right arrow Abstract Freely available
Right arrow Full Text (PDF) Free
Right arrow Submit a response
Right arrow Alert me when this article is cited
Right arrow Alert me when eLetters are posted
Right arrow Alert me if a correction is posted
Right arrow Citation Map
Services
Right arrow Email this article to a friend
Right arrow Similar articles in this journal
Right arrow Similar articles in ISI Web of Science
Right arrow Similar articles in PubMed
Right arrow Alert me to new issues of the journal
Right arrow Add to My Personal Article Archive
Right arrow Download to citation manager
Right arrow reprints & permissions
Citing Articles
Right arrow Citing Articles via HighWire
Right arrow Citing Articles via ISI Web of Science (11)
Right arrow Citing Articles via Google Scholar
Google Scholar
Right arrow Articles by Lahrmann, H.
Right arrow Articles by Zwick, H.
Right arrow Search for Related Content
PubMed
Right arrow PubMed Citation
Right arrow Articles by Lahrmann, H.
Right arrow Articles by Zwick, H.
(Chest. 1999;116:1593-1600.)
© 1999 American College of Chest Physicians

Neural Drive to the Diaphragm After Lung Volume Reduction Surgery*

Heinz Lahrmann, MD, MSc; Monika Wild, MD; Theodor Wanke, MD; Edda Tschernko, MD; Wilfried Wisser, MD; Walter Klepetko, MD, FCCP and Hartmut Zwick, MD, FCCP

* From the Neurological Department Kaiser Franz Josef Hospital, Vienna (Dr. Lahrmann), Ludwig Boltzmann Institute for Environmental Pneumology, Lainz Hospital, Vienna (Drs. Wild, Wanke, and Zwick), Clinic of Anesthesiology (Dr. Tschernko) and Clinic of Surgery, University Vienna (Drs. Wisser and Klepetko), Austria.

Correspondence to: Heinz Lahrmann, MD, Msc, Neurological Department, Kaiser Franz Josef Hospital, Kundratstraße 3, A-1100 Vienna, Austria.


   Abstract
TOP
 Abstract
Introduction
 Materials and Methods
 Results
 Discussion
 References
 
Study objectives: The aim of this study was to investigate prospectively the changes in neural drive to the diaphragm in the first year after lung volume reduction surgery (LVRS) in patients with COPD.

Patients and methods: In 14 patients with severe emphysema (mean ± SD; age, 53.7 ± 8.3 years; FEV1, 0.64 ± 0.18 L; residual volume [RV], 5.33 ± 1.25 L; PaO2, 62.3 ± 9.0 mm Hg; PaCO2, 39.0 ± 6.0 mm Hg), we assessed lung function, arterial blood gases, maximal exercise capacity (Wmax), and oxygen uptake (O2max); intrinsic positive end-expiratory pressure (PEEPi); diaphragmatic strength (transdiaphragmatic pressure, Pdisniff) and endurance capacity (tlim); central diaphragmatic drive assessed by root mean square analysis of the esophageal electromyogram (rmsdia); and isotime dyspnea during loaded breathing tests (BS).

Results: Despite a significant increase (expressed as a percentage of baseline) in FEV1 (40.6%) and a decrease in RV (30.0%) and PEEPi (75.7%) 1 month after LVRS, the improvements in Wmax (31.2%) and O2max (13.7%); Pdisniff (25.4%) and tlim (64.9%); rmsdia (34.6%); and BS (21.7%) did not reach statistical significance (p < 0.05) until 6 months after LVRS. Arterial blood gases did not change significantly. Significant correlations were found between decrease in rmsdia and changes in PEEPi (r = 0.69), Wmax (r = -0.56), Pdisniff (r = -0.65), tlim (r = -0.59), and BS (r = 0.71) 6 months after LVRS.

Conclusions: Our results show that LVRS is able to increase the efficacy of the respiratory pump and by this way reduce ventilatory drive and respiratory effort sensation.

Key Words: diaphragm • dyspnea • electromyography • lung volume reduction surgery • neural drive


   Introduction
TOP
 Abstract
 Introduction
Materials and Methods
 Results
 Discussion
 References
 
Severe strain is imposed on respiratory muscles in patients with COPD. Increased airflow resistance and a reduced dynamic pulmonary compliance increase resistive and elastic loads. As a consequence, inspiratory muscles have to generate a greater negative pleural pressure (measured as esophageal pressure, Pes) than normal during each inspiration. End-expiratory airflow is decreased as a result of a loss of driving pressure and premature airway collapse. This results in dynamic pulmonary hyperinflation in many patients with severe COPD. The intrinsic positive end-expiratory pressure (PEEPi) adds an extra load on the inspiratory muscles.1 Moreover, emphysematous changes in the lung cause pulmonary hyperinflation and thoracic distension. Severe impairment of the efficacy of the respiratory pump as an inspiratory pressure generator is the consequence, because inspiratory muscles have to operate at shorter than normal length.2 To overcome these disadvantages, the neural drive to the respiratory muscles is increased. This has been demonstrated to be the case for the parasternal intercostal and scalene muscles.3 Druz and Sharp4 recorded greater diaphragmatic electrical activity in patients with COPD than in normal subjects using esophageal electrodes. Gorini and collaborators5 reported a high neural respiratory drive in patients with COPD using chest wall electrodes. By inserting needle electrodes into the costal diaphragm, De Troyer and coworkers6 measured higher discharge frequencies from diaphragmatic motor units during resting breathing in COPD than in normal subjects. Disabling dyspnea, closely related to respiratory muscle function, particularly to neural respiratory drive, is the consequence.7 8

Lung volume reduction surgery (LVRS) has emerged as a promising strategy to relieve dyspnea in patients with severe lung emphysema, who have no further benefit from medical treatment or rehabilitation programs.9 Lung function, exercise capacity, dyspnea indexes, and quality-of-life scores have served as estimates for the outcome of LVRS.9 The positive effects of LVRS on respiratory muscle function and ventilatory mechanics have been assessed by some authors.10 11 12 13 14 15 Teschler and colleagues10 investigated respiratory muscle function and ventilatory drive after LVRS using inspiratory mouth occlusion pressure (P0.1). Celli and coworkers16 reported a decrease in ventilatory drive (P0.1) and ventilatory response to CO2 after LVRS. A relationship between improvements in ventilatory mechanics after resection of emphysematous lung tissue and increase in respiratory muscle function and decrease of neural respiratory drive and dyspnea has not been established so far.

In a prospective study, we investigated the hypothesis that neural respiratory drive and dyspnea on effort decrease after LVRS as a result of the improvement in ventilatory mechanics and diaphragmatic strength and endurance capacity. By examining the patients before and at 1, 6, and 12 months after LVRS we were able to establish the chronological order and the strength of correlation between improvements in neural drive to the diaphragm and lung function, exercise capacity, ventilatory mechanics, inspiratory muscle function, and dyspnea on effort.


   Materials and Methods
TOP
 Abstract
 Introduction
 Materials and Methods
Results
 Discussion
 References
 
Selection of Patients
Fourteen consecutive patients with severe nonbullous emphysema and dyspnea on minimal exertion participated in the study (5 males and 9 females; mean ± SD; age, 53.7 ± 8.3 years). Informed consent was obtained from all patients before investigation, and the study was approved by the local board of ethics. Significant functional limitation (10% < FEV1 < 40% of predicted value) with severe hyperinflation (residual volume [RV] > 300% of predicted value) and dyspnea despite optimized medical therapy provided the basis for patient selection. Exclusion criteria were a mean pulmonary arterial pressure at rest above 39.9 mm Hg and bullae measuring > 5 cm in diameter shown on high-resolution CT scans. None of the patients was hypercapnic (PaCO2, 39.0 ± 6.0 mm Hg) whereas all of them were hypoxemic (PaO2, 62.3 ± 9.0 mm Hg) before LVRS. Two patients had {alpha}1-antitrypsin deficiency. The dosage of oral corticosteroids (prednisone) was < 12.5 mg/d in all patients at least for the last 6 months before LVRS and for the rest of the study period. Four patients received long-term oxygen therapy preoperatively. No patient participated in any rehabilitation program for limb muscles or underwent specific respiratory muscle training either pre- or postoperatively. Two patients had undergone median sternotomy whereas all others had been operated by means of video endoscopic techniques. All patients were operated bilaterally.

Measurements
All patients (n = 14) were examined both preoperatively and 1 and 6 months after surgery; 8 of the 14 patients had already a 12-month follow-up at the end of the study.

  1. Lung function analysis consisted of spirometry, using an open system with integration of the flow, and whole-body plethysmography, performed by the constant volume method (Jaeger; Würzburg, Germany). The following variables were assessed: FEV1, FVC, RV, and total lung capacity (TLC); breathing frequency at rest (BF); and tidal volume (VT). Arterial blood gas values were measured at rest (Radiometer; Copenhagen, Denmark). Reference values for lung-function analysis were the normal values proposed by the European Community of Coal and Steel.17
  2. During progressive incremental exercise tests performed on a cycle ergometer (the work rate increased by 10 W at 2-min intervals), maximal work rate (Wmax), minute ventilation (Emax), and oxygen uptake (O2max) were measured (EOS Sprint; Jaeger) by using standardized methods.18
  3. PEEPi was measured during tidal breathing using the BICORE CP-100 monitor (BICORE Monitoring Systems; Irvine, CA). A balloon catheter was inserted via the nose and positioned in the mid-esophagus to record the esophageal pressure swings. Airflow was measured using a tightly fitting mask with a flow sensor in the single outlet. PEEPi was calculated as the negative deflection in Pes from the start of inspiratory effort to the onset of inspiratory flow. Start of inspiratory flow was extrapolated from flow measurements taken at 50 and 100 mL/s after zero flow, which occurred during the transition from expiration to inspiration. All measurements were performed with the patients sitting in an upright position and quietly breathing room air.
  4. Sniff-induced maximal esophageal pressure (Pessniff) and transdiaphragmatic pressure (Pdisniff), which is equal to maximal sniff-induced gastric pressure (Pgasniff) minus Pessniff values measured from functional residual capacity, served as estimates for global inspiratory muscle and diaphragmatic strength, respectively. Pressures were recorded by means of a flexible water-perfused catheter system with four lumens for simultaneous measurements of Pga, Pes, and bipolar electromyogram (EMG) (Ing. Zickler GesmbH; Pfaffstätten, Austria).19 It was introduced transnasally and fixed to the nose with adhesive tape after it had been advanced to the point at which the EMG signal amplitude was greatest. We made sure that the patients reached a constant and reproducible plateau of Pdisniff values before taking the mean of five values (within a range of 5%). Inspiratory muscle endurance capacity was defined as the time that elapses until total exhaustion (tlim) during a fatiguing loaded breathing test (LBT). Inspiration was loaded by a threshold device similar to that proposed by Nickerson and Keens.20 The inspiratory leg of the two-way valve was connected to a plunger to which weights could be added externally (SEGADAT; Vienna, Austria). Expiration was unloaded. Before each test the weights were individually selected such that the patient had to generate at least 70% of their individual and actual Pdisniff with each inspiration to overcome a threshold load. To help the patients reach this goal, Pdi was continuously displayed on a video screen placed in front of them, with the 70% line being marked. To rule out any changes in breathing pattern, which would result in spurious improvement in endurance, the subjects were given sound signals for breathing at a constant frequency (BF), which corresponded to the patient’s resting frequency, and inspiratory time (TI) and expiratory time (TE) were adapted to the patient’s duty cycle. The individual BF, TI, and TE were kept constant during all the LBT runs. Oxygen-dependent patients additionally received their usual dosage of O2. During LBT, we did not instruct the patients as to how to generate their Pdi; they were free to choose their own pattern of inspiratory muscle activation. Because each patient exhibited similar Pdi/Pdisniff ratios in all examinations, the mechanical loads imposed pre- and postoperatively were amenable to comparison. To make certain that patients did not become increasingly hyperinflated, we evaluated end-expiratory esophageal pressures (Pesend) throughout LBT. The tests were stopped when the patients were no longer able to tolerate the effort or were unable to achieve and sustain the predetermined 70% of Pdisniff for at least three consecutive breaths despite strong encouragement on the part of the investigating team. A decrease of the mean power frequency of the diaphragmatic EMG > 20% of the baseline and a maximal dyspnea rating on a Borg category scale at the end of LBT indicated total inspiratory muscle exhaustion.21
  5. The EMG from the crural part of the diaphragm was recorded by means of esophageal electrodes. Two gold ring electrodes at a distance of 20 mm were mounted on the esophageal catheter. The ground electrode was placed over the right epicondyle. Muscle action potentials were differentially amplified and passed through an anti-aliasing filter (2 to 500 Hz; SEGADAT). The EMG channel and the pressures were digitalized on-line with a sampling rate of 2000 Hz per channel and a digital resolution of 12 bits by using a data acquisition card (DAS-20; Keithley; Taunton, MA) installed in a personal computer, and stored on hard disk for further analysis. The inspiratory fall of the Pes curve was taken as the trigger point for EMG data acquisition. As muscle action potentials can be seen before the onset of pressure generation, EMG data sampling started 200 ms before the trigger was released. The neural phrenic drive to the diaphragm during LBT was assessed by means of a root mean square analysis of the esophageal EMG (rmsdia). The root mean square (rmsdia = 1/N · ({sum}ixi2 )1 with the EMG amplitudes xi and i = 1, ... , N), represents a statistically valid measure of the amplitude behavior of the EMG, and thus describes the level of global muscle fiber excitation. Furthermore, it is characterized by a very good signal resolution.22 To minimize the intersubject variability of EMG measurements (effects of electrode configuration, tissue filtering, temperature, etc.) we normalized rmsdia to the average values recorded during the first three loaded breaths. All software involved was developed by using ASYST (ASYST Software Technologies; Rochester, NY) and Borlands C++ (Borland Inc; Scotts Valley, CA).
  6. Every minute patients were asked to grade their intensity of dyspnea by pointing to a number from 0 (nothing at all) to 10 (maximal), according to a modified Borg scale (BS).23 We compared intraindividual preoperative and postoperative rmsdia and BS values at isotime, which is defined as the time when the preoperative run was stopped.

Statistical Analysis
Statistical comparisons between pre- and postoperative measurements were made by means of analysis of variance for repeated measurements using Bonferroni’s correction.24 A p < 0.05 was considered statistically significant. Spearman’s coefficient of correlation was used for assessing the associations between the relative improvements (percentage of baseline) in neural drive to the diaphragm (rmsdia) as the independent variable and lung function (FEV1, RV, PEEPi), exercise capacity (Wmax, Emax), inspiratory muscle strength (Pdisniff, Pessniff), endurance capacity (tlim), and dyspnea on effort (BS) as the dependent variables.24 All values included in the text and tables are expressed as mean ± SD.


   Results
TOP
 Abstract
 Introduction
 Materials and Methods
 Results
Discussion
 References
 
Preoperative baseline data and changes at 1, 6, and 12 months after LVRS are presented in Tables 1 and 2 .


View this table:
[in this window]
[in a new window]

  		Table 1.. Lung Function and Exercise Capacity Before and After LVRS

 
Lung Function Testing and Arterial Blood Gas Values
One month after LVRS, a significant increase in FVC of 11.0% and in FEV1 of 40.6% were seen. A significant decrease of 28.1% was seen in RV, and 19.1% in TLC, 1 month after LVRS. A nonsignificant decline of these values toward baseline was found in the following examinations. BF and VT at rest did not change significantly after LVRS. One month after surgery, changes in PaO2 from 62.3 ± 9.0 mm Hg to 61.5 ± 9.0 mm Hg and in PaCO2 from 39.0 ± 6.0 mm Hg to 39.0 ± 4.5 mm Hg were not significant statistically. In the 6- and 12-month follow-up, no significant changes were found.

Ergometer Exercise Tests
Wmax increased significantly by 28.9%, O2max by 13.7%, and Emax by 15.4% 6 months after LVRS with an insignificant decline thereafter (for absolute values, see Table 1 ).

Ventilatory Mechanics
A significant decrease in PEEPi of 75.7% was found in the follow-up 1 month after LVRS, and the values remained within these ranges for the study period.

Respiratory Muscle Function
A significant improvement in Pdisniff, Pessniff, and tlim by 25.4%, 15.4%, and 65.1%, respectively, was observed for the first time 6 months after surgery. These values improved even more at the 12-month follow-up, but this further improvement did not reach statistical significance. None of the patients showed any appreciable changes in Pesend during a fatiguing run, either before or at any examination after LVRS. This suggests that the end-expiratory lung volume remained constant throughout the tests.

Neural Drive to the Diaphragm
Normalized rmsdia, computed at isotime, was seen to have decreased significantly by 34.6% at the 6-month examination and remained within this range at the 12-month follow-up.

Dyspnea on Effort
The decrease in BS computed at isotime became significant 6 months after LVRS, and BS dropped to 21.7% of baseline after 6 months. Values were seen to improve further at the 12-month follow-up.

Correlations
The coefficients of correlation between the relative improvement at 6 months vs baseline of neural drive to the diaphragm (rmsdia) at isotime as the independent variable and the relative changes vs baseline of the following variables were derived: FEV1, -0.20; RV, 0.25; TLC, 0.54; PEEPi, 0.69; Wmax, -0.56; Emax, -0.79; Pdisniff, -0.65; Pessniff, 0.61; tlim, -0.59; and BS, 0.71.

These correlations were significant except for FEV1 and RV. Figures 1 through 3 present individual data (n = 14) on the relationship of relative improvement of rmsdia vs relative changes of endurance capacity (tlim), Pdisniff, and TLC 6 months after LVRS.



View larger version (11K):
[in this window]
[in a new window]
[Download PPT slide]
  		Figure 1.. Relative improvement of neural diaphragmatic drive (rmsdia) at isotime vs relative change of tlim 6 months after LVRS, both expressed as a percentage of baseline. Straight line represents linear fit; r = -0.59; significant at p < 0.05, n = 14.

 

   Discussion
TOP
 Abstract
 Introduction
 Materials and Methods
 Results
 Discussion
References
 
This prospective study showed that, in patients with severe lung emphysema, neural drive to the diaphragm during fatiguing LBTs is significantly lower after LVRS than before. This is attributed to the observed increase in the efficacy of inspiratory muscles caused by a decrease in hyperinflation and ventilatory load. Decreased dyspnea on effort and increased exercise capacity are the consequences.

The evaluation of diaphragmatic activation is technically difficult, and the interpretation is full of pitfalls. Direct recordings of diaphragmatic muscle action potentials using needle electrodes have been described.6 In respiratory studies, chest wall and esophageal recording techniques have been used more extensively. However, any direct inter- and intraindividual comparison is debatable, because the recording conditions vary under influence of temperature, muscle-to-electrode distance, electrode configuration, skin-electrode interface, etc. To overcome these difficulties, several investigators have normalized diaphragmatic EMG activity to resting or maximal values.5 6 Normalizing to values recorded during tidal breathing bears the disadvantage of introducing data with poor signal-to-noise ratio. Normalization to values during TLC maneuvers relies on the patient’s cooperation and further assumes that patients have an identical muscle recruitment pattern during full inspiration before and after LVRS, which may not be true.6 By taking the mean rmsdia value of the first three loaded breaths for normalization, the signal resolution and recruitment pattern are comparable to the rest of the time series.

It has been demonstrated in isolated diaphragmatic strips from dogs and in human subjects for different lung volumes that EMG activity increases when muscle length decreases independently of neural drive.25 26 Because of hyperinflation, the diaphragm in patients with COPD is shorter and flatter than normal, and EMG activity is overestimated when comparison is made with normal subjects.6 Any reduction in diaphragmatic EMG activity found in our study thus might be attributed to the effect of LVRS on diaphragmatic muscle length. However, we did not compare the raw diaphragmatic EMG activity, but rather normalized rmsdia values at isotime of fatiguing resistive breathing tests. Additionally, we ruled out any increase in hyperinflation, which might have further decreased diaphragmatic muscle length, by monitoring Pesend throughout LBT. Therefore, we may conclude that there was less electrical diaphragmatic activity after LVRS than at the time when the pre-LVRS run was stopped (isotime).

Changes in breathing pattern after LVRS may result in spurious improvements of endurance capacity.27 To minimize this effect, the TI/TE ratio and the BF were kept constant throughout LBT, and they were individually reproduced for each patient in pre- and postoperative LBT by means of sound signals. The pressure threshold device used, in combination with a feedback of Pdi and respiratory timing, ensured achievement of the predetermined load with each breath.28 In addition, this threshold device ensured that inspiratory pressure was independent of inspiratory flow over a wide range of pressures.20

Several factors may contribute to the decrease in inspiratory muscle function in patients with COPD when compared with normal subjects.5 6 10 16 First, the intrinsic force-length properties of the diaphragm are impaired in COPD. Several animal and human studies have shown that the drive to the diaphragm is very well adjusted to account for changes in diaphragmatic mechanical efficiency.29 30 In COPD, the diaphragm becomes shorter and flatter because of lung hyperinflation, causing it to contract from a fiber length that is shorter than normal and therefore more unfavorable. Furthermore, diaphragmatic flattening increases the radius of its curvature, and according to Laplace’s law, the tension developed in the contracting diaphragm is poorly converted into Pdi in this state, which is reflected before LVRS by a lower Pdisniff value than thereafter. Resection of emphysematous lung tissue brings the diaphragm into a more normal position, restoring its force-length properties and curvature. Second, PEEPi, which has to be offset before inflating the lung, imposes an additional threshold load on the inspiratory muscles.1 Third, by increasing chest wall elastic recoil pressure, large operating volumes result in an increase of elastic loads. The effect of LVRS on these factors has been demonstrated empirically by Gelb and collaborators11 and theoretically by Hoppin.15

The decrease of electrical activity of the diaphragm, measured by esophageal EMG, throughout LBTs supports the hypothesis that less neural drive is necessary to perform the same relative task after LVRS. This corresponds to the fact that the diaphragm is less fatiguable after LVRS, reflected by a significant increase in the Tlim. Thus, LVRS is able not only to improve the elastic properties of the lung and reduce the intrinsic load on the diaphragm, but also to improve its neuromechanical coupling by restoring the physiologic force-length properties.

Improvements in ventilatory mechanics and lung function occurred as early as 1 month after surgery, whereas the development of improvements in respiratory muscle function, ventilatory drive, dyspnea on effort, and exercise tolerance took significantly longer. This is in contrast to the results of Teschler and coworkers10 , who reported a significant increase in inspiratory muscle function variables within 1 month after LVRS. We argue, however, that 1 month after surgery the patients were still in the recovery period, and the optimum performance of voluntary maneuvers, such as Pdisniff, LBT (tlim, BS), and exercise testing (Wmax, Emax) was still impaired. Farkas and Roussos31 have shown in emphysematous hamsters that the remodeling of the diaphragm by dropout of sarcomeres in series to reduce their optimal functional length takes time. Thus, it may be speculated that the inverse process after LVRS takes time, too.

Reduction of dyspnea was among the first published results of LVRS by Cooper’s group.9 But little is known about the physiologic effects that make LVRS such a success in reducing dyspnea. Sciurba and coworkers12 have demonstrated that the increase in lung elastic recoil pressure leads to improvements in dyspnea and exercise tolerance. O’Donnell and associates14 attributed a reduced exertional breathlessness after LVRS to a combination of reduced thoracic distension, reduced BF, and reduced mechanical constraints on lung volume expansion. Benditt and colleagues32 attributed the reduction of breathlessness to changes in breathing pattern and ventilatory muscle recruitment caused by improvements of the mechanics of breathing after LVRS. Martinez and collaborators13 have provided evidence that the decrease of dyspnea and the increase in exercise capacity may be attributed to improvements in lung recoil, respiratory muscle function, and dynamic hyperinflation. Killian and coworkers7 proposed the existence of cortical interneurons, which mediate the sensation of ventilatory effort and dyspnea between the motor and the sensory cortex. However, the changes in central motor output to the respiratory muscles and the relation to improvements in dyspnea on effort, exercise capacity, and lung function induced by LVRS have not been assessed.

Teschler and colleagues10 used P0.1 to assess ventilatory drive in 17 patients with COPD before and 1 month after LVRS. They reported a decrease of 24% in P0.1 after LVRS, which remained above the upper limit of normal. They did not find any significant correlations of changes in P0.1 with 6-min walking distance, lung function, or blood gas values. In contrast with our results, they found no correlation between the reduction in ventilatory drive (P0.1) and dyspnea score, despite a significant decrease of both measurements after LVRS. Hyperinflation impairs the conversion of ventilatory drive to inspiratory pressure generation.33 The preoperative P0.1 may thus be underestimated. Moreover, P0.1 depends on end-expiratory lung volume and consequently on PEEPi,33 which we have shown to decrease after LVRS. Gorini and coworkers5 argue that the EMG is a more precise method than P0.1 in assessing the ventilatory drive in COPD patients. Celli and coworkers16 described a decrease in central drive (P0.1) and ventilatory response to CO2 to normal values 5 months after LVRS. They found no correlation between changes in P0.1 and blood gas values or lung function. They did not report dyspnea, ventilatory mechanics, or inspiratory muscle function in this study. Thus, the precise mechanism by which ventilatory drive is reduced after LVRS remains undetermined.16 Criner and coworkers34 reported significant improvements in lung function and diaphragmatic strength in 20 patients with lung emphysema 3 months after LVRS. The magnitude of these improvements in lung function were comparable to our results. The increase in Pdisniff was more pronounced than in our study, which might be attributed to the fact that their baseline values were 30% lower than ours. They reported that RV and trapped gas at functional residual capacity were strong determinants of postoperative increase in maximal inspiratory mouth pressure, which confirms our own results. Comparing their results obtained 3 months after LVRS and ours at 1 and 6 months after LVRS, we conclude that the improvement in diaphragm function occurs 3 to 6 months after LVRS.

By analyzing esophageal EMG during fatiguing exercise tests, we have provided evidence that the reduction in dyspnea after LVRS may be attributed to a reduced central ventilatory drive. After LVRS, hyperinflation is reduced, and respiratory muscles are put in a more favorable position for generating negative inspiratory pressure. Moreover, intrinsic ventilatory load induced by PEEPi is decreased. In this manner, the capacity of the respiratory pump to generate inspiratory pressure and to sustain fatiguing loads is increased, and less central ventilatory drive is necessary for generating the same relative inspiratory pressures. This contributes to the increase in exercise tolerance and the decrease in dyspnea on effort seen after LVRS.


View this table:
[in this window]
[in a new window]

  		Table 2.. Respiratory Muscle Function, Neural Drive to the Diaphragm, and Dyspnea Before and After LVRS

 


View larger version (12K):
[in this window]
[in a new window]
[Download PPT slide]
  		Figure 2.. Relative improvement of neural diaphragmatic drive (rmsdia) at isotime vs relative change of Pdisniff 6 months after LVRS, both expressed as a percentage of baseline. Straight line represents linear fit; r = -0.65; significant at p < 0.05, n = 14.

 


View larger version (11K):
[in this window]
[in a new window]
[Download PPT slide]
  		Figure 3.. Relative improvement of neural diaphragmatic drive (rmsdia) at isotime vs relative change of TLC 6 months after LVRS, both expressed as a percentage of baseline. Straight line represents linear fit; r = 0.54; significant at p < 0.05, n = 14.

 

   Footnotes
 
Abbreviations: BF = breath frequency; BS = Borg score; EMG = electromyogram; LBT = loaded breathing test; LVRS = lung volume reduction surgery; P0.1 = inspiratory mouth occlusion pressure; Pdisniff = maximal sniff induced transdiaphragmatic pressure; PEEPi = intrinsic positive end-expiratory pressure; Pesend = end-expiratory esophageal pressure; Pessniff = maximal sniff-induced esophageal pressure; Pgasniff = maximal sniff-induced gastric pressure; rmsdia = root mean square of esophageal diaphragmatic electromyogram; RV = residual volume; TE = expiratory time; TI = inspiratory time; TLC = total lung capacity; tlim = endurance time; Emax = maximal minute ventilation; O2max = maximal oxygen uptake; VT = tidal volume; Wmax = maximal exercise capacity

Received for publication May 21, 1998. Accepted for publication July 22, 1999.


   References
TOP
 Abstract
 Introduction
 Materials and Methods
 Results
 Discussion
 References
 

  1. Dal Vecchio, L, Polese, G, Poggi, R, et al (1990) Intrinsic positive end-expiratory pressure in stable patients with chronic obstructive pulmonary disease. Eur Respir J 3,74-80[Abstract]
  2. Rochester, DF (1985) The diaphragm; contractile properties and fatigue. J Clin Invest 75,1397-1402
  3. Gandevia, SC, Leeper, JB, McKenzie, DK, et al (1996) Discharge frequency of parasternal intercostal and scalene motor units during breathing in normal and COPD subjects. Am J Respir Crit Care Med 153,622-628[Abstract]
  4. Druz, WS, Sharp, JT (1982) Electrical and mechanical activity of the diaphragm accompanying body position in severe chronic obstructive pulmonary disease. Am Rev Respir Dis 125,275-280[ISI][Medline]
  5. Gorini, M, Spinelli, A, Ginanni, R, et al (1990) Neural respiratory drive and neuromuscular coupling in patients with chronic obstructive pulmonary disease (COPD). Chest 98,1179-1186[Abstract/Free Full Text]
  6. De Troyer, A, Leeper, JB, McKenzie, DK, et al (1997) Neural drive to the diaphragm in patients with severe COPD. Am J Respir Crit Care Med 155,1335-1340[Abstract]
  7. Killian, K, Jones, N (1988) Respiratory muscles and dyspnea. Clin Chest Med 9,237-248[ISI][Medline]
  8. O’Donnell, DE (1994) Breathlessness in patients with chronic airflow limitation. Chest 106,904-912[Free Full Text]
  9. Cooper, JD, Trulock, EP, Triantafillou, AN, et al (1995) Bilateral pneumonectomy (volume reduction) for chronic obstructive pulmonary disease. J Thorac Cardiovasc Surg 109,106-119[Abstract/Free Full Text]
  10. Teschler, H, Stamatis, G, El-Raouf Farhat, AA, et al (1996) Effect of surgical lung volume reduction on respiratory muscle function in pulmonary emphysema. Eur Respir J 9,1779-1784[Abstract]
  11. Gelb, AF, McKenna, RJ, Brenner, M, et al (1996) Contribution of lung and chest wall mechanics following emphysema resection. Chest 110,11-17[Abstract/Free Full Text]
  12. Sciurba, FC, Rogers, RM, Keenan, RJ, et al (1996) Improvement in pulmonary function and elastic recoil after lung-reduction surgery for diffuse emphysema. N Engl J Med 34,1095-1099
  13. Martinez, FJ, Montes de Oca, M, Whyte, RI, et al (1997) Lung-volume reduction improves dyspnea, dynamic hyperinflation, and respiratory muscle function. Am J Respir Crit Care Med 155,1984-1990[Abstract]
  14. O’Donnell, DE, Webb, KA, Bertley, JC, et al (1996) Mechanisms of relief of exertional breathlessness following unilateral bullectomy and lung volume reduction surgery in emphysema. Chest 110,18-27[Abstract/Free Full Text]
  15. Hoppin, FG, Jr (1997) Theoretical basis for improvements following reduction pneumoplasty in emphysema. Am J Respir Crit Care Med 155,520-525[Abstract]
  16. Celli, BR, Montes de Oca, M, Mendez, R, et al (1997) Lung reduction surgery in severe COPD decreases central drive and ventilatory response to CO2. Chest 112,902-906[Abstract/Free Full Text]
  17. European Community for Steel, and Coal. Standardized lung function testing. Eur Respir J 1993; 6(suppl 16):25–27
  18. Dillard, TA, Piantadosi, S, Rajagapal, KR (1989) Determinants of maximum exercise capacity in patients with chronic airflow obstruction. Chest 96,267-271[Abstract/Free Full Text]
  19. Wanke, T, Schenz, G, Zwick, H, et al (1990) Dependence of maximal sniff generated mouth and transdiaphragmatic pressures on lung volume. Thorax 45,352-355[Abstract]
  20. Nickerson, BG, Keens, TG (1982) Measuring ventilatory muscle endurance in humans as sustainable inspiratory pressure. J Appl Physiol 52,768-772[Abstract/Free Full Text]
  21. Clanton TL. Respiratory muscle endurance in humans. In: Roussos C, ed. The thorax, 2nd ed. part B. New York, NY: Marcel Dekker, 1995; 1199–1230
  22. O’Brien, MJ, van Eykern, LA, Prechtl, HFR (1983) Monitoring respiratory activity in infants: a non-intrusive diaphragm EMG technique. Rolfe, P eds. Non-invasive measurements, vol 2 ,132-177 Academic Press London.
  23. Borg, GAV (1982) Psychophysical basis of perceived exertion. Med Sci Sports Exerc 14,377-381[ISI][Medline]
  24. Altman, DG (1991) Practical statistics for medical research. Chapman & Hall London, UK.
  25. Kim, MJ, Druz, WS, Sharp, JT (1985) Effect of muscle length on electromyogram in a canine diaphragm strip preparation. J Appl Physiol 53,1602-1607
  26. Gandevia, SC, McKenzie, DK (1986) Human diaphragmatic EMG: changes with lung volume and posture during supramaximal phrenic stimulation. J Appl Physiol 60,1420-1428[Abstract/Free Full Text]
  27. Roue, C, Mal, H, Sleiman, C, et al (1996) Lung volume reduction in patients with severe diffuse emphysema. Chest 110,28-34[Abstract/Free Full Text]
  28. Belman, MJ, Shadmehr, R (1988) Targeted resistive ventilatory muscle training in chronic obstructive pulmonary disease. J Appl Physiol 65,2726-2735[Abstract/Free Full Text]
  29. Banzett, RB, Inbar, GF, Brown, R, et al (1981) Diaphragm electrical activity during negative lower torso pressure in quadriplegic man. J Appl Physiol 51,654-659[Abstract/Free Full Text]
  30. Cheesema, M, Revelette, WR (1990) Phrenic afferent contribution to reflexes elicited by changes in diaphragm length. J Appl Physiol 51,640-647
  31. Farkas, GA, Roussos, C (1981) Diaphragm in emphysematous hamsters: sarcomere adaptability. J Appl Physiol 54,1635-1640
  32. Benditt, JO, Wood, DE, McCool, FD, et al (1997) Changes in breathing and ventilatory muscle recruitment patterns induced by lung volume reduction surgery. Am J Respir Crit Care Med 155,279-284[Abstract]
  33. Grassino, A, Goldman, MD, Mead, J, et al (1978) Mechanics of the human diaphragm during voluntary contraction: statics. J Appl Physiol 44,829-839[Abstract/Free Full Text]
  34. Criner, G, Cordova, FC, Leyenson, V, et al (1998) Effect of lung volume reduction surgery on diaphragm strength. Am J Respir Crit Care Med 157,1578-1585[Abstract/Free Full Text]



This article has been cited by other articles:


Home page
 Proc Am Thorac SocHome page
D. E. O'Donnell
Hyperinflation, dyspnea, and exercise intolerance in chronic obstructive pulmonary disease.
Proceedings of the ATS, January 1, 2006; 3(2): 180 - 184.
[Abstract] [Full Text] [PDF]

Home page
 Am. J. Respir. Crit. Care Med.Home page
R. B. Gorman, D. K. McKenzie, J. E. Butler, J. F. Tolman, and S. C. Gandevia
Diaphragm Length and Neural Drive after Lung Volume Reduction Surgery
Am. J. Respir. Crit. Care Med., November 15, 2005; 172(10): 1259 - 1266.
[Abstract] [Full Text] [PDF]

Home page
 Chronic Respiratory DiseaseHome page
Z J McKeoughl, J A Alison, M S Bayfield, and P T.P Bye
Supported and unsupported arm exercise capacity following lung volume reduction surgery: a pilot study
Chronic Respiratory Disease, April 1, 2005; 2(2): 59 - 65.
[Abstract] [PDF]

Home page
 ChestHome page
T. Takayama, C. Shindoh, Y. Kurokawa, W. Hida, H. Kurosawa, H. Ogawa, and S. Satomi
Effects of Lung Volume Reduction Surgery for Emphysema on Oxygen Cost of Breathing
Chest, June 1, 2003; 123(6): 1847 - 1852.
[Abstract] [Full Text] [PDF]

Home page
 ChestHome page
F. Bellemare, M.-P. Cordeau, J. Couture, E. Lafontaine, P. Leblanc, and L. Passerini
Effects of Emphysema and Lung Volume Reduction Surgery on Transdiaphragmatic Pressure and Diaphragm Length*
Chest, June 1, 2002; 121(6): 1898 - 1910.
[Abstract] [Full Text] [PDF]

Home page
 ChestHome page
J. B. Shrager, D.-K. Kim, Y. J. Hashmi, H. H. Stedman, J. Zhu, L. R. Kaiser, and S. Levine
Sarcomeres Are Added in Series to Emphysematous Rat Diaphragm After Lung Volume Reduction Surgery
Chest, January 1, 2002; 121(1): 210 - 215.
[Abstract] [Full Text] [PDF]

Home page
 J. Thorac. Cardiovasc. Surg.Home page
J. B. Shrager, D.-K. Kim, Y. J. Hashmi, E. B. Lankford, P. Wahl, H. H. Stedman, S. Levine, and L. R. Kaiser
Lung volume reduction surgery restores the normal diaphragmatic length-tension relationship in emphysematous rats
J. Thorac. Cardiovasc. Surg., February 1, 2001; 121(2): 0217 - 224.
[Abstract] [Full Text] [PDF]

Home page
 ChestHome page
R. M. Rogers, H. O. Coxson, F. C. Sciurba, R. J. Keenan, K. P. Whittall, and J. C. Hogg
Preoperative Severity of Emphysema Predictive of Improvement After Lung Volume Reduction Surgery : Use of CT Morphometry
Chest, November 1, 2000; 118(5): 1240 - 1247.
[Abstract] [Full Text] [PDF]

This Article
Right arrow Abstract Freely available
Right arrow Full Text (PDF) Free
Right arrow Submit a response
Right arrow Alert me when this article is cited
Right arrow Alert me when eLetters are posted
Right arrow Alert me if a correction is posted
Right arrow Citation Map
Services
Right arrow Email this article to a friend
Right arrow Similar articles in this journal
Right arrow Similar articles in ISI Web of Science
Right arrow Similar articles in PubMed
Right arrow Alert me to new issues of the journal
Right arrow Add to My Personal Article Archive
Right arrow Download to citation manager
Right arrow reprints & permissions
Citing Articles
Right arrow Citing Articles via HighWire
Right arrow Citing Articles via ISI Web of Science (11)
Right arrow Citing Articles via Google Scholar
Google Scholar
Right arrow Articles by Lahrmann, H.
Right arrow Articles by Zwick, H.
Right arrow Search for Related Content
PubMed
Right arrow PubMed Citation
Right arrow Articles by Lahrmann, H.
Right arrow Articles by Zwick, H.

HOME HELP FEEDBACK SUBSCRIPTIONS ARCHIVE SEARCH TABLE OF CONTENTS