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(Chest. 1999;115:1285-1292.)
© 1999 American College of Chest Physicians

Reduction in Ventilator Response to CO2 With Relaxation Feedback During CO2 Rebreathing in Normal Adults*

Jerome E. Holliday, PhD and Chris Veremakis, MD

* From the Department of Critical Care Medicine, St. John's Mercy Medical Center, St. Louis, MO.

Correspondence to: Jerome E. Holliday, PhD, VA Medical Center, Medicine Service 111-JC, 915 N Grand Blvd, St. Louis, MO 63106


   Abstract
TOP
 Abstract
Introduction
 Materials and Methods
 Results
 Discussion
 References
 
Background: Previous studies have shown that relaxation biofeedback reduced time on the ventilator for the difficult-to-wean patients.

Objective: To test the hypothesis that the underlying mechanism of biofeedback ventilator weaning was the reduction of neural respiratory drive (NRD).

Design: Prospective, linear regression analysis.

Setting: Critical care medicine department in tertiary health care hospital.

Subjects: Fifteen healthy adult volunteers were randomly assigned to the biofeedback group, and 15 healthy adult volunteers were randomly assigned to a control group.

Interventions: Relaxation feedback was administered while a single variable, PaCO2, was inputted to the respiratory control system and the output measured. While rebreathing 7% CO2/93% O2, the biofeedback group received a baseline session and a relaxation feedback session and the control group received a baseline session and a no feedback session.

Measurements and results: During relaxation feedback, there was a significant (p < 0.001 to p < 0.05) reduction in the slope of minute ventilation (I), mean inspiratory flow (VT/TI), occlusion pressure in 0.1 s from onset of inspiration (P100), respiration rate (RR), and diaphragm (DA) EMG compared to baseline. We also found the above breathing parameters decreased significantly for relaxation feedback (p < 0.001–0.05), compared to baseline, at maximum end-tidal CO2 (64 ± 1.2 mm Hg) (all data are expressed as mean ± SE). The decrease for I = -4.65 ± 1.17 L/min, DA EMG = -0.4 ± 0.21 µV, P100 = -1.13 ± 0.56 cm H2O, VT/TI = -144 ± 82.91 ml/s, and RR = -3.1 ± 0.79 breaths/min. No significant changes occurred in these parameters for the control group.

Conclusions: We conclude that the addition of the behavioral input of relaxation feedback results in decreasing the values of respiratory parameters that reflect NRD.

Key Words: biofeedback • CO2 rebreathing • neural respiratory drive • respiration


   Introduction
TOP
 Abstract
 Introduction
Materials and Methods
 Results
 Discussion
 References
 
Previous investigators1 2 3 have described the influence of respiratory drive on weaning from mechanical ventilation. These reports indicated that ventilator weaning was more difficult if neural respiratory drive (NRD) as measured by the change in endotracheal occlusion pressure 0.1 sec from onset of inspiration (P100)4 5 6 was > 4 cm H2O. In a randomized study, using biofeedback, Holliday and Hyers7 showed that biofeedback can reduce ventilator-weaning time in a group of ventilator-dependent patients by 12 days. This study suggested that reduced time on the ventilator might the result of relaxation biofeedback reducing neural respiratory drive NRD. Studies by Bulow8 and by Wolkove and coworkers9 showed that drowsy and meditative states reduced response to CO2 compared to the normal waking state. Asmussen10 reported that by merely closing the eyes there was an 8% to 14% reduction in minute ventilation (I) during CO2 rebreathing.

A depressed drive has also been implicated in failure to wean. Haake et al11 reported that a ventilator patient who failed weaning had a depressed central drive manifested by hypopnea with increasing PaCO2. Thus, difficulty with weaning could be due to either failure to maintain blood gases due to decreased drive, problems with lung function or muscle strength, or due to respiratory distress where high drive is involved. The present study focuses on the latter.

To determine the effect of biofeedback on NRD, we studied the effects of biofeedback during CO2 rebreathing. We hypothesized that during hypercapnic challenge, relaxation feedback would reduce values of ventilatory parameters I, P100, mean inspiratory flow (VT/TI), and diaphragm (DA) electromyogram (EMG) which reflect NRD.


   Materials and Methods
TOP
 Abstract
 Introduction
 Materials and Methods
Results
 Discussion
 References
 
After the study was approved by the Institutional Review Board of St. John's Mercy Medical Center, 15 healthy volunteers (10 males, 5 females) with mean age of 38.7 ± 2.42 years (all data are expressed as mean ± SE) were randomly assigned to the biofeedback group. Fifteen volunteers (8 males, 7 females) with mean age of 33.3 ± 2.13 years were randomly assigned to the control group. Vital capacity and FEV1 measurements were obtained on each subject. Subjects with vital capacity or FEV1 < 80% of predicted were not included in the study. The subjects were not informed as to outcome, hypothesis, or expected results of the research. Each subject was informed that they would have two sessions of rebreathing CO2 and a rest period between each session to allow time for the computer to record data on a disk. If for any reason they could not continue with the session, they were told to raise a hand and the procedure would be stopped. After the first CO2 rebreathing session, the subjects in the biofeedback group were given relaxation feedback. The control group was not but was given a second CO2 session without relaxation called a no feedback (FB) session to control habituation effects. Neither group was given sympathy, encouragement, or coaching.

Since the relaxation feedback required the subjects' eyes be opened to receive the visual feedback,7 the present study would have to be performed with eyes opened for both baseline and relaxation feedback sessions. A subgroup of the study population underwent an additional study to assess the effect of eyes open and eyes closed on CO2 rebreathing. With these tests, we could directly compare our results with the previous studies of Bulow8 and Wolkove and coworkers,9 whose subjects had their eyes closed. Twelve of our 30 subjects volunteered for a separate study to redo Asmussen's10 work. Each volunteer had two sessions of rebreathing CO2 with the second session following directly after the first. During the first CO2 rebreathing session, the eyes were opened, and during the second session, the subjects' eyes were closed. To control for the relaxation variable, during the eyes-closed session, the subjects were told not to relax but to try to stay awake, a maneuver used by Shea and coworkers.12

A schematic drawing of the hypercapnic challenge (Read13 ) breathing circuit showing the CO2 rebreathing bag, the biofeedback system, and the two-way valve with balloon for occluding the airway for P100 measurements (Hans Rudolph; Kansas City, MO; model 9326) is shown in Figure 1 . To prevent subjects from consciously controlling P100, the valve opening the balloon was placed in a soundproof container. The P100 was measured every 20 seconds during CO2 rebreathing (approximately every third or fourth breath). Tidal volume (VT) was measured by integrating the output of a heated pneumotach (Hans Rudolph model 3700) that was calibrated before each session. The output of the pneumotach was fed into a computer that performed the integration.



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  		Figure 1. A schematic diagram showing the placement of IC and DA EMG electrodes, the relaxation and VT feedback monitor, and the threshold line T and CO2 rebreathing circuit. The CO2 circuit shows the rebreathing bag, the pneumotach, and the two-way valve and balloon for measuring P100. BK = background; E = expiration; I = inspiration; AMP = amplifier.

 
Surface EMG electrodes on the DA and upper intercostal muscles (IC) are shown in Figure 1 . The EMG's were measured with a J&J model M-57 (J&J Co.; 22797 Holgar Ct. N.E.; Poulsbo, WA) which measures integrated EMG in µV. The electrodes were placed according to the method of Gross and coworkers14 on the sixth and seventh IC space 1 cm from the costal margin to ensure reproducibility of measurements. Upper IC muscle EMG for relaxation feedback was obtained by electrodes placed on the IC muscles between the third and fourth ribs.

Each subject sat in a comfortable chair and breathed room air through a mouthpiece until end-tidal CO2 (ETCO2) concentration reached a steady state and the subject was accustomed to breathing through the mouthpiece. The ETCO2 was measured with an infrared monitor (Puritan Bennett Datex No 125; Los Angeles, CA) which was calibrated before each session. A 5-L rebreathing bag was used to ensure rapid mixing of gas between the bag and lungs at the onset of rebreathing. The subjects in each group received two 3-min sessions of rebreathing 7% CO2/93% O2. The mean ETCO2 at the start was 48 ± 0.86 mm Hg and increased after 3 minutes of rebreathing CO2 to 64 ± 1.2 mm Hg. The mean increase of 16 mm Hg in ETCO2 is considered adequate for stimulating respiratory drive. The rate of increase of ETCO2 was 5.19 mm Hg/min, which was within the limits considered satisfactory by Read13 (3–6 mm Hg/min). In addition to ETCO2, the respiratory parameters measured during each hypercapnic challenge in both groups were VT, I, P100, VT/TI, respiration rate (RR), DA EMG, heart rate (HR), and O2 saturation (pulse oximeter model 3700; Ohmeda). The data were recorded on computer and on an audiotape by a FM recording adapter (A. R. Vetter Co.; Rebersburg, PA; model 3) and recorded on 6-channel Dynograph recorder (Sensormedics; CA; model R611). The P100 was obtained from the Dynograph recorder of occlusion pressure as a function of time.

The pre- and post-CO2 rebreathing measurements of the above-mentioned breathing parameters were taken while the subjects were breathing room air (21% O2) for 5 minutes. This was done to show that the parameters reflecting NRD of the two groups were within normal limits and returned to normal value after CO2 rebreathing. After each session, the subject completed two Borg scales. The first was the Borg scale15 for measuring shortness of breath (SOB), and the second, a modified Borg scale for measuring anxiety.

The first CO2 rebreathing session served as a CO2 baseline for both groups. In the second CO2 rebreathing session, the biofeedback group was taught to passively relax their chest muscles (an important maneuver in biofeedback control) at the same time they received visual feedback (a line displayed on the computer monitor) and auditory feedback (a sound heard from the speaker) from EMG measurements from the 3rd IC muscles (Fig 1) . The sound was heard whenever the line went above threshold line T, a point of reference that was initially set at a level slightly below their resting background muscle tension (BK) EMG (Fig 2 ).



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  		Figure 2. An integrated IC EMG showing the contraction and relaxation rhythm of the IC muscles during breathing and the underlying muscle tension. BK = background.

 
In order for the line on the computer monitor to reflect BK EMG, rather than IC EMG tidal breaths, the relaxing and contraction rhythm of the IC muscles that occurs during breathing were subtracted from the total EMG of the IC muscles (Fig 2) . The visual and auditory feedback was thus proportional to the BK EMG muscle tension. This assured that constant muscle tension would be reduced and the subject would not shift breathing activity in the IC muscles to the abdominal muscles, which would change the breathing pattern during the relaxation feedback session. The subjects were told to relax their chest and shoulders whenever a beep sound was heard so the line would drop below threshold T and the sound would stop. As indicated above, the control group received no FB in the second CO2 rebreathing session.

The slope of each respiratory parameter, as a function of ETCO2, was determined by the method of least squares. The differences between baseline and the relaxation feedback session in the biofeedback group and the baseline and no FB sessions in the control group were compared for significance with a paired t test. All differences were considered significant at p < 0.05.


   Results
TOP
 Abstract
 Introduction
 Materials and Methods
 Results
Discussion
 References
 
The pilot study examining the effects of eyes open vs eyes closed showed that with eyes open {Delta}I/{Delta}ETCO2 was 1.92 ± 0.08, and at maximum ETCO2 of 64 mm Hg I was 28.87 ± 3.8 L/min and RR was 14.42 ± 1.73. With eyes closed, {Delta}I/{Delta}ETCO2 was 1.90 ± 0.07, I was 33.14 ± 3.59 L/min, and RR was 14.79 ± 1.63 at 64 mm Hg. Although a 15 percent increase in I occurred for eyes closed, as compared to eyes open, none of the above changes were statistically significant. There were also no significant changes in {Delta}P100/{Delta}ETCO2 or for P100 at 64 mm Hg between eyes open and eyes closed. The results of the pilot study allow comparisons with the studies of Bulow8 and Wolkove and coworkers.9

The mean baseline value of P100 for breathing room air for the biofeedback group was 1.64 cm H2O,16 and this was in close agreement with the control group's mean P100 value of 1.47 cm H2O. This shows the reproducibility of the P100 data. In addition, for the pre- and postbaseline breathing room air there was no significant difference in I, DA EMG, P100, VT/TI, and RR, showing that room air baseline measurements are stable reference values. The validity of the diaphragm EMG is shown by the plot of VT as a function of diaphragm EMG, for a typical subject, in Figure 3 . The least-squares plot shows the VT increasing with the diaphragm EMG. An unpaired t test for possible intertest difference between the biofeedback and control groups is shown in Table 1 . There were no significant differences between the baselines of the two groups, indicating no intertest differences.



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  		Figure 3. The raw data points of VT as a function of DA EMG for a typical subject. A linear regression line shows the increase in VT with the increase in DA EMG.

 

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  		Table 1. Mean Values From Raw Data of I DA EMG, P100, VT/TI, VT, and RR at an ETCO2 of 64 ± 1.2 mmHg for Baseline of Biofeedback Group Compared to Baseline of Control Group*

 
Table 2 compares the mean slopes of the {Delta}I/{Delta}ETCO2, {Delta}DA EMG/{Delta}ETCO2, {Delta}P100/{Delta}ETCO2, {Delta}I/TT/{Delta}ETCO2, {Delta}VT/{Delta}ETCO2, and {Delta}RR/{Delta}ETCO2 slopes for CO2 rebreathing between baseline and relaxation feedback (the biofeedback group) and baseline and no FB session (the control group). There was a significant (p < 0.001 to p < 0.05) reduction in the slopes of {Delta}I/{Delta}ETCO2, {Delta}DA EMG/{Delta}ETCO2, and {Delta}P100/{Delta}ETCO2, {Delta}VT/TI/{Delta}ETCO2, {Delta}RR/{Delta}ETCO2 with CO2 rebreathing between baseline and relaxation feedback. No significant differences appeared in the mean slopes of these breathing parameters between baseline and no FB sessions for the control group. The slope reductions (composite linear regression curves for the 15 biofeedback subjects) for I, VT/TI, P100, and diaphragm EMG as a function of ETCO2 for baseline compared to biofeedback sessions can be seen on the four plots in Figure 4 . The points are the mean values of the 15 biofeedback subjects between 44 ± 0.56 mm Hg ETCO2 and 64 ± 1.2 mm Hg ETCO2. The curves show a linear plot from 48 ± 0.9, the value of ETCO2 for the mixed venous plateau, and ETCO2 of 64 ± 1.2 mm Hg. The vertical lines at each point show the SE.


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  		Table 2. Mean Slopes of I, DA EMG, P100, VT/TI, VT, and RR as a Function of ETCO2 for CO2 Rebreathing During Relaxation Feedback Compared to Control Group*

 


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  		Figure 4. I, P100, VT/TI, and DA EMG (µV) amplitude above the background EMG, as a function of ETCO2 for baseline and relaxation feedback for the biofeedback group during CO2 rebreathing.

 
A significant (p < 0.001 to p < 0.05) reduction occurred in the mean values of I, DA EMG, P100, VT/TI, and RR during relaxation feedback compared to baseline at maximum ETCO2 (64 ± 1.2 mm Hg) as shown in Table 3 and Figure 4 . The significant reduction in RR, but the lack of any for VT, shows that the significant reduction in I is due to a reduction in RR and not due to reduction in VT. The reductions in I of - 4.65 ± 1.17 L/min, DA EMG of - 0.4 ± 0.21 µV, P100 of - 1.13 ± 0.56 cm H2O, VT/TI of - 144 ± 82.91 ml/s, and in RR of - 3.1 ± 0.79 breaths/min, reflecting NRD, shows clinical significance as well as mathematical significance. No significant change occurred for the control group between baseline and no FB sessions in the above parameters at maximum ETCO2; therefore, these results show that relaxation feedback is reducing the subjects' I, DA EMG VT/TI, and P100 (which reflect NRD) response to CO2. In addition, these results show that this decrease is not due to reduced responsiveness to CO2 the second time it is rebreathed; in other words, there is no practice effect.


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  		Table 3. Mean Values From Raw Data of I, DA EMG, P100, VT/TI, VT, and RR at an ETCO2 of 64 ± 1.2 mm Hg for Relaxation Feedback Compared to Baseline and Control Group*

 
Evidence that the subjects were actually relaxing during the relaxation feedback is shown by the measurements in Table 4 . There was a significant (p < 0.01) reduction in HR for the biofeedback group of 8.6 beats/min for CO2 rebreathing between the baseline and relaxation feedback: 75.8 ± 3.08 vs. 67.2 ± 1.95 beats/min, respectively. There was no significant change in HR for the control group between baseline and no FB sessions. There was also a significant (p < 0.001) reduction in self report of anxiety from the modified Borg scale during relaxation feedback. The subjects also reported significantly (p < 0.01) less feeling of SOB during relaxation feedback. The control group had no significant changes in anxiety or SOB between baseline and the no feedback session. The significant reduction in HR, self report of anxiety, and SOB indicates that relaxation feedback is producing relaxation and a reduction in anxiety.


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  		Table 4. Effect of Relaxation Feedback on HR, Feelings of Anxiety and SOB During CO2 Rebreathing Compared to Control Group*

 

   Discussion
TOP
 Abstract
 Introduction
 Materials and Methods
 Results
 Discussion
References
 
We have demonstrated that biofeedback relaxation feedback can significantly reduce parameters reflecting neural respiratory drive; this data supports previous findings that sleep or drowsy and meditative states decrease the ventilatory response to CO2 rebreathing8 9 17 18 19 20 when compared to a normal waking state.

The ventilatory CO2 response curves in Figure 4 and Table 2 are shifted to the right, and there is a flattening of the slope similar to those seen in previous studies.8 9 The 18% reduction in the mean value of I for the relaxation feedback (Table 3) is close to the reduction reported by Bulow8 for the drowsy state and to the reductions reported by Wolkove and coworkers9 for the meditative state. The control group showed no significant change in parameters reflecting NRD between baseline and no FB CO2 rebreathing. During relaxation feedback, there was a significant reduction in HR, self report of anxiety, and SOB compared to baseline (Table 4) which did not occur for the control group. The lack of a significant change in multiple parameters of NRD during CO2 rebreathing between eyes open and eyes closed in the subgroup study shows that the reduction in ventilatory response to CO2, reported by Asmussen10 does not appear to be due to merely closing the eyes.

One of the possible errors in this type of research is the reproducibility of repeated measurements of CO2 rebreathing. The data in Table 3 shows that there was no significant difference between baseline and no FB sessions in the control group, and there was no significant difference between the CO2 baselines of the biofeedback group and the control group (Table 1) . This shows the reproducibility of mean values during CO2 rebreathing.

Several studies have demonstrated decreased ventilator-weaning time in patients receiving biofeedback.7 21 22 23 Two breathing parameters whose reduction during biofeedback is associated with reduced ventilator-weaning time and reflects NRD are P100 and RR. Holliday and coworkers23 reported significant reductions in P100 and RR for high-drive ventilator patients between start of weaning and successful extubation using relaxation feedback. It was indicated above that several investigators1 2 3 reported that weaning was not successful when P100 was > 4 cm H2O. Yang and Tobin24 have found that RR is one of the best indicators of successful extubation. They have shown that if the ratio of RR/VT is < 100 there is a high likelihood of weaning, whereas a RR/VT > 100 indicates a poor chance of ventilator weaning. Table 3 shows that there are significant reductions in P100 and RR (without any significant reduction in VT) during CO2 rebreathing with relaxation feedback. Thus, the reduction in ventilator-weaning time with biofeedback training of ventilator patients appears to be related to the reduction of NRD. However, the present research study will have to be performed on ventilator patients before the statement can be made conclusively.

How does relaxation feedback reduce respiratory drive? In a review article, Shea25 presents the idea that there is a behavioral and an autonomic respiratory drive. Research in biofeedback has shown that what was thought to be purely autonomic phenomena could be controlled behaviorally if information about the phenomena to be controlled was fed back to the subject. Leitner and coworkers26 reported a reduction in VT, VT/TI, and peak airway pressure during loaded breathing with distraction using auditory tones. Gallego and Perruchet27 observed that humans exposed to eight pairings of sound and a brief hypoxic challenge altered their breath duration on subsequent trials with exposure to the sound alone. Since studies by Whitelaw and coworkers4 indicate that P100 is not consciously controlled, the significant reduction of P100 by biofeedback (Table 3) supports the contention that biofeedback can modify the autonomic drive.

Shea25 states that the reticular activating system (RAS) has significant effects on the brainstem respiratory complex. Activity in the RAS increases with arousal and can provide stimulatory effects on certain brainstem-related neurons. Shea25 points out that signs of increased arousal include an increase in sympathetic nervous system activity and EEG activation. Sensory stimulation is accompanied by increases in I, RR, slight increases in HR, BP, and EEG activation.28 In contrast, a reduction from an aroused state, such as relaxation, should have the opposite effect on the RAS, which is what the present research indicates. The study shows that during CO2 rebreathing relaxation feedback reduces ventilatory responses that reflect NRD. There are also significant reductions in HR and in feelings of anxiety and SOB for relaxation feedback CO2 rebreathing compared to baseline CO2 rebreathing (Table 4) which could result in reduced RAS activity. A great amount of research has been done to show that muscle fatigue is an important factor in ventilator-weaning failure. However, little attention has been paid to the influence of the brainstem and RAS on setting NRD. Biofeedback may reprogram the brainstem to reduce high NRD and facilitate weaning.

In summary, the above results show that relaxation feedback can reduce breathing parameters that reflect NRD. The reduction in NRD may be the underlying mechanism for biofeedback reducing ventilator-weaning time,7 but further studies on relaxation feedback and NRD on ventilator patients are required. The study suggests the existence of behavioral modulation of the hypercapnic ventilatory response that may be of practical utility in ventilator weaning.


   Acknowledgements
 
ACKNOWLEDGMENT: The writers thank the Critical Care staff of St. John's Mercy Medical Center for their cooperation during the study. A special thanks goes to Jackie O'Brien for assistance in performing the research and to Dr. Michael Lippman, Michael Range, and Kit Alter for editorial comments.


   Footnotes
 
Abbreviations: BK = background; DA = diaphragm; EMG = electromyogram; ETCO2 = end-tidal CO2; FB = feedback; HR = heart rate; NRD = neural respiratory drive; P100 = occlusion pressure 0.1 sec from onset of inspiration; RR = respiration rate; SOB = shortness of breath; T = threshold line; I = inspired minute ventilation; VT/TI = mean inspiration flow; VT = tidal volume; µV = microvolt

Received for publication April 6, 1998. Accepted for publication December 24, 1998.


   References
TOP
 Abstract
 Introduction
 Materials and Methods
 Results
 Discussion
 References
 

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J. E. Holliday and M. Lippmann
Reduction in Ventilatory Response to CO2 With Relaxation Feedback During CO2 Rebreathing for Ventilator Patients
Chest, October 1, 2003; 124(4): 1500 - 1511.
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