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(Chest. 2004;125:2069-2074.)
© 2004 American College of Chest Physicians

Influence of Immersion in Water on Muscle Function and Breathing Pattern in Patients With Severe Diaphragm Weakness*

Bernd Schoenhofer, MD, PhD, FCCP; Dieter Koehler, MD, PhD, FCCP and Michael I. Polkey, MD, PhD

* From Krankenhaus Kloster Grafschaft (Drs. Schoenhofer and Koehler), Zentrum für Pneumologie, Grafschaft, Germany; and Respiratory Muscle Laboratory (Dr. Polkey), Royal Brompton Hospital, London, UK.

Correspondence to: Bernd Schoenhofer, MD, PhD, FCCP, Division of Pulmonary and Critical Care Medicine, Klinikum Hannover–Oststadt, Podbielskistrasse 380, 30659 Hannover, Germany; e-mail: Bernd.Schoenhofer{at}t-online.de


   Abstract
TOP
 Abstract
Introduction
 Materials and Methods
 Results
 Discussion
 References
 
Study objective: Dyspnea is a common symptom in patients with diaphragm weakness or paralysis. In particular, dyspnea may be aggravated by immersion. We hypothesized that immersion to the neck in water would decrease vital capacity and consequently increase the demand/capacity ratio of the respiratory muscles.

Design: Case series study.

Subjects: Seven patients with profound diaphragm weakness or paralysis proven by phrenic nerve stimulation, and seven normal control subjects.

Intervention and measurements: We measured land-based and water-based spirometry, breathing pattern, and mouth occlusion pressures.

Results: We found that the patients could preserve minute ventilation despite a fall in vital capacity from a mean of 2.3 to 1.3 L, but this required an increased respiratory rate (RR) [21.4 to 26.7 breaths/min, p = 0.018]. We used mouth occlusion pressure 100 ms after the start of inspiration (P0.1) as an estimation of the drive to breath; P0.1 increased from 1.4 to 3.9 cm H2O (p = 0.018) without significant change in tidal volume.

Conclusions: Relative to control subjects, patients with diaphragm weakness have augmented drive to breathe in order to attempt to defend gas exchange. This conclusion is implied by the presevered minute ventilation with immersion, the augmented RR, and elevated P0.1 relative to maximum static inspiratory pressure.

Key Words: diaphragmatic weakness • immersion • lung function


   Introduction
TOP
 Abstract
 Introduction
Materials and Methods
 Results
 Discussion
 References
 
Diaphragm paralysis is a recognized cause of dyspnea; nevertheless, because the condition is relatively rare, diagnosis is frequently delayed. Breathlessness on immersion in water has previously been described as a clinical feature of diaphragm paralysis.123 The aim of this study was to investigate the influence of immersion in water on muscle function and breathing pattern in patients with severe weakness or paralysis of the diaphragm. We studied seven patients with severe bilateral diaphragm paralysis before and during immersion in water and compared the results to healthy control subjects.


   Materials and Methods
TOP
 Abstract
 Introduction
 Materials and Methods
Results
 Discussion
 References
 
Patients
Seven consecutive patients referred to the Krankenhaus Kloster Grafschaft for consideration of noninvasive ventilatory support were recruited for this study. The protocol was approved by our ethical review committee, and all subjects gave written informed consent to participate. Patients with bulbar paralysis and consequent weakness of the facial muscles were excluded. Clinical diagnoses are shown in Table 1 . Identical procedures were applied to seven healthy members of the local community of similar age, height, and weight who served as control subjects.


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  		Table 1.. Clinical, Anthropometric, and Spirometric Data of Patients Seated, and Anthropometric and Spirometric Data of Control Subjects Seated*

 
Land-Based Tests
Spirometry was measured using a portable spirometer (Vicatest; Hellige; Freiburg, Germany) in the seated erect posture according to the guidelines of the European Respiratory Society.4 Normal values are those of the European Respiratory Society.4

Inspiratory and expiratory flow were measured using a portable pneumotachograph (CP100, Bicore; Medilab; Estenfeld, Germany); integration of these data allowed measurement of tidal volume and respiratory rate (RR). With the same pneumotachograph, the ratio of inspiratory time to the total breathing cycle was measured. Mean values from a 5-min period are presented; the patients were allowed 15-min rest prior to this to acclimatize to their condition.

To determine registration of the mouth occlusion pressure 100 ms after the start of inspiration (P0.1),5 maximal static inspiratory pressure (PImax), and maximal static expiratory pressure (PEmax), both hardware and software were designed and constructed in-house using a piezoelectric pressure sensor. The device uses a flanged mouthpiece connected to a two-way nonrebreathing valve, and incorporates a small air leak as proposed by Ringqvist,6 but is without visual feedback for the patient. The inspiratory limb was occluded by the operator during expiration by an invisible and inaudible balloon without warning to the patient. The inspiratory valve was occluded for 0.2 to 0.3 s in intervals of 30 s for measuring the P0.1 value. The average value was calculated from five consecutive measurements.

PImax was determined at residual volume according to the method of Black and Hyatt.7 PEmax was determined at total lung capacity.

The twitch transdiaphragmatic pressure was measured in patients only. We used a pair of commercially available latex balloon catheters, 110 cm in length (P.K. Morgan; Rainham, Kent, UK), conventionally placed in the stomach and the esophagus. The position of the balloons was checked using the method of Baydur and coworkers.8 The catheters were connected to a differential pressure transducer (Validyne Engineering; Northridge, CA), carrier amplifiers (Model CD 23; CD 223; Validyne Engineering), a 12 bit analog-digital board (National Instruments Corporation; Austin, TX), and a personal computer running Labview software (in-house construction). Transdiaphragmatic pressure was obtained online by subtraction of esophageal pressure from gastric pressure.

Cervical magnetic stimulation (CMS)9 and unilateral magnetic stimulation (UMS)10 of the phrenic nerves were performed with the subjects seated wearing a noseclip with the abdomen unbound and the trouser belt undone. To minimize twitch potentiation, subjects were required to breathe quietly for 20 min before stimulation.11 For CMS, single stimuli were performed over the neck between the fifth and seventh cervical spines to find the best spot for stimulation.

Once this point was determined, a minimum of five stimulations at maximal stimulator output were given. Stimuli were given from a 90-mm circular coil powered by a Magstim 200 (Magstim; Whitland, Dyfed, UK). For UMS, single stimuli were performed over the surface landmarks of each phrenic nerve at the level of the cricoid cartilage to find the best spot for stimulation. Once this point was determined, a minimum of five stimulations at maximal stimulator output were given using a 45-mm figure-of-eight coil. When applying this technique in a healthy population in our laboratory, the average pressure for CMS was 33 cm H2O and for UMS was 16 cm H2O, which concords closely with those observed elsewhere.12

Water-Based Measurements
Patients were monitored in the water by a technician who was also a qualified lifeguard. Patients were supported in the water to the level of the neck in the erect position by the lifeguard and, if able, were permitted to grip the side-rail of the pool. In order not to hinder the rib cage displacement, the technician fixed only the patient’s pelvic ring with his hands.

In this position, patients repeated the spirometry, the assessment of the breathing pattern as detailed above, as well as the PImax and measurement of P0.1. Safety issues precluded the use of the magnetic stimulator at the poolside.

Statistics and Conventions
For both CMS and UMS, twitches were only accepted for the analysis if performed with the subject relaxed, as judged by esophageal pressure, and when baseline transdiaphragmatic pressure was similar to that seen at end-expiration during normal breathing, indicating relaxation of the respiratory muscles. Because the sample sizes were small, nonparametric tests were used. Therefore we compared differences between paralyzed patients and normal subjects using the Mann-Whitney test. For differences in the same subjects between being in and out of water, we used the Wilcoxon signed-rank test. Statistics were computed using Statview 4.02 (Abacus Concepts; Berkeley, CA), and a level of p < 0.05 was taken as significant.


   Results
TOP
 Abstract
 Introduction
 Materials and Methods
 Results
Discussion
 References
 
Anthropometric Data, Lung and Muscle Function
Diagnosis, spirometric, and clinical data are shown in Table 1. Respiratory muscle strength data of the patients are shown in Table 2 . All patients had severe bilateral diaphragm weakness (patients 1, 3, 4, and 6) or paresis (patients 2, 5, and 7), as judged by phrenic nerve stimulation and, in all but one patient (patient 2), expiratory muscle weakness. The control subjects were assumed to be free of neurologic and respiratory disease. Their mean PImax was 60.3 cm H2O, compared with 37 cm H2O in patients with diaphragm paralysis (p = 0.07).


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  		Table 2.. Respiratory Strength in Patients and Control Subjects Measured Land Based

 
Comparison Between Resting Dry to Immersion Data
Data from both patients and normal subjects, resting dry and immersed in water, are shown in Table 3 . As expected, the mean seated vital capacity (VC) was substantially less in patients than control subjects (2.3 ± 1.0 L vs 4.7 ± 1.1 L, p = 0.002). All patients had dyspnea on immersion in water.


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  		Table 3.. Land-Based and Water-Based Measurements in Patients and Control Subjects*

 
Significant differences were observed between patients and control subjects with respect to the effect of immersion on VC (Fig 1 ). Although tidal volume remained constant (Table 3), VC fell from a mean 2.3 to 1.3 L (a decrease of 34.4%, p = 0.03) in patients; this change was significantly greater than that observed in normal subjects (p = 0.026). Control subjects showed no significant change in VC; the mean decrease in VC was 100 mL (a 2.6% change).



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  		Figure 1.. VC seated and immersed in patients and control subjects.

 
In subjects with diaphragm weakness or paralysis, immersion caused a mean 25% increase in RR from 21.4 ± 6.4 to 26.7 ± 7.8 breaths/min (p < 0.02) [Fig 2 ]. Control subjects showed no significant change in RR.



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  		Figure 2.. RR seated and immersed in patients and control subjects.

 
The P0.1 was not different between patients and control subjects out of the water (Table 3). In the water, there was a significant increase in both normal subjects and patients (p < 0.03 for both); the magnitude of this increase was markedly greater in patients (mean, 190.7% vs 29.4%, p = 0.0006).

Finally, comparing the ratio of muscle load/capacity (P0.1/PImax), the mean seated value was 0.035 in normal subjects rising to 0.051 after immersion (increase of 30%) [Fig 3 ], whereas in patients the magnitude of increase (mean seated value was 0.045 rising to 0.166 after immersion [increase of 280.4%]) was greater (p = 0.004).



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  		Figure 3.. P0.1/PImax ratio seated and immersed in patients and control subjects.

 

   Discussion
TOP
 Abstract
 Introduction
 Materials and Methods
 Results
 Discussion
References
 
Although dyspnea in water is recognized as a symptom suggestive of diaphragm paralysis or weakness, no previous study has systematically investigated the underlying mechanisms. Moreover, in only one of the few cases so far described in the literature was diaphragm paralysis confirmed by phrenic nerve stimulation.2 Our data show that there was a substantial reduction in VC without significant reduction in tidal volume. Nevertheless, the patient’s complaint of dyspnea was consistent with the observation that RR rate and P0.1 increased sharply on immersion in water.

Inevitably, our study has some methodologic limitations. In particular, we acknowledge that the difference in PImax between patients and control subjects just failed to reach the 0.05 significance level. Nevertheless, based on clinical criteria, our control subjects were healthy and therefore, if anything, this serves to support our conclusion that the differences in PImax between the groups are due to respiratory muscle weakness.

Second, we acknowledge that minute ventilation is based on a frequency-tidal volume calculation without correction for anatomic dead space. Since no end-tidal CO2 measurements or arterial blood gas analyses are available, we cannot demonstrate that carbon dioxide was effectively cleared. Indeed, since minute ventilation was unchanged and breathing rate increased, alveolar ventilation may have dropped by virtue of an increased dead space/tidal volume ratio. Thus, had we measured it, CO2 might have risen and, if so, this would have contributed to dyspnea in this group.

In addition, P0.1 measurement is lung-volume dependent; therefore, there may be a theoretical risk that a part of the increase of P0.1 is caused by functional residual capacity (FRC) moving toward residual volume (RV). We acknowledge, however, that neither in patients nor in control subjects was FRC measured during immersion; therefore, the influence of lung volumes on P0.1 may be significant.

Immersion markedly increases the elastic work of breathing13 so that increased ventilatory drive is required to maintain alveolar ventilation. Similarly, a decreased chest wall compliance is caused by mass loading the respiratory system.14 The resulting increase in oxygen cost of breathing was not assessed in this study. Exposed to this combination some subjects may attempt to fight the load, while others will default to a tachypneic pattern to reduce the work of breathing.

Previous studies have examined the effect of immersion in water on VC in both normal subjects151617 and patients with COPD.18 In these studies, the fall in VC was ≤ 10%, as it was in the normal subjects in this study. By contrast, we found that patients with respiratory muscle weakness had a mean drop of 34% in VC on immersion. The fall in VC could, theoretically, be due to a reduction in total lung capacity (TLC) or a rise in RV. We acknowledge that in our study neither changes of TLC, FRC, and RV nor intraesophageal pressures were measured; therefore, the pressure-volume relationship of the lung and chest wall in water remains unclear.

Some of the changes following immersion would affect both patients with diaphragm weakness and normal subjects. For example, hydrostatic pressure is likely to force blood into the thorax.19 If this were so, it would be expected that this could also contribute to a fall in TLC and might also decrease lung compliance.

With regard specifically to the patients with diaphragm paralysis in the present study, we believe the bulk, if not all, of the fall in VC on immersion is due to a reduction in TLC. We argue this because even despite putative gas trapping, RV is observed to fall during immersion in normal subjects,19 and this is more likely in our patients who had expiratory muscle weakness also.

The combination of diminished inspiratory muscle strength and increased respiratory drive gives two additional sources of discomfort for patients with respiratory muscle weakness, and this is dramatically shown by examining the P0.1/PImax ratio. After immersion, in normal subjects this ratio increased by 30%, whereas an increase of 280% was observed in patients. One could also speculate that additional sources of respiratory muscle loading (for example, diseases causing reduced lung compliance) would give increase symptoms in a multiplicative rather than additive fashion, as would disease, such as COPD, where load is frequency dependent.

Relative to control subjects, patients with diaphragm weakness have augmented drive to breathe in order to attempt to defend gas exchange. This conclusion is implied by the preserved minute ventilation with immersion, the augmented RR, and elevated P0.1 relative to PImax.


   Acknowledgements
 
The authors thank Sven Wallstein and Patrick Appelhans for technical assistance with land-based and water-based measurements.


   Footnotes
 
Abbreviations: CMS = cervical magnetic stimulation of phrenic nerve; FRC = functional residual capacity; PEmax = maximal static expiratory pressure; PImax = maximal static inspiratory pressure; P0.1 = mouth occlusion pressure 100 ms after the start of inspiration; RR = respiratory rate; RV = residual volume; TLC = total lung capacity; UMS = unilateral magnetic stimulation of phrenic nerve; VC = vital capacity

Received for publication July 10, 2002. Accepted for publication September 16, 2003.


   References
TOP
 Abstract
 Introduction
 Materials and Methods
 Results
 Discussion
 References
 

  1. Mier, AK, Brophy, C, Green, M (1986) Out of depth, out of breath. BMJ 292,1495-1496[ISI][Medline]
  2. Davison, A, Mulvey, D Idiopathic diaphragmatic weakness. BMJ 1992;304,492-494[ISI][Medline]
  3. McCool, FD, Mead, J Dyspnea on immersion: mechanisms in patients with bilateral diaphragm paralysis. Am Rev Respir Dis 1989;139,275-276[ISI][Medline]
  4. Quanjer, PH, Tammeling, GJ, Cotes, JE, et al Lung volumes and forced ventilatory flows: Report Working Party Standardization of Lung Function Tests, European Community for Steel and Coal; Official Statement of the European Respiratory Society. Eur Respir J Suppl 1993;16,5-40[Medline]
  5. Whitelaw, WA, Derenne, JP, Milic-Emili, J Occlusion pressure as a measure of respiratory center output in conscious man. Respir Physiol 1975;23,181-199[CrossRef][ISI][Medline]
  6. Ringqvist, T The ventilatory capacity in healthy subjects: an analysis of causal factors with special reference to the respiratory forces. Scand J Clin Lab Invest 1966;18(Suppl 88),8-170
  7. Black, LF, Hyatt, RE Maximal respiratory pressures: normal values and relationships to age and sex. Am Rev Respir Dis 1969;99,696-702[ISI][Medline]
  8. Baydur, A, Behrakis, PK, Zin, WA, et al A simple method for assessing the validity of the esophageal balloon technique. Am Rev Respir Dis 1982;126,788-791[ISI][Medline]
  9. Similowski, T, Fleury, B, Launois, S, et al Cervical magnetic stimulation: a new painless method for bilateral phrenic nerve stimulation in conscious humans. J Appl Physiol 1989;67,1311-1318[Abstract/Free Full Text]
  10. Mills, GH, Kyroussis, D, Hamnegard, C-H, et al Unilateral magnetic stimulation of the phrenic nerve. Thorax 1995;50,1162-1172[Abstract]
  11. Wragg, SD, Hamnegard, C-H, Road, J, et al Potentiation of diaphragmatic twitch after voluntary contraction in normal subjects. Thorax 1994;49,1234-1237[Abstract]
  12. Polkey, MI, Harris, ML, Hughes, PD, et al The contractile properties of the elderly human diaphragm. Am J Respir Crit Care Med 1997;155,1560-1564[Abstract]
  13. Hong, SK, Cerretelli, P, Cruz, JC, et al Mechanics of respiration during submersion in water. J Appl Physiol 1969;27,535-538[Free Full Text]
  14. Sharp, J, Henry, JP, Sweany, SK, et al Effects of mass loading the respiratory system in man. J Appl Physiol 1964;19,959-966[Abstract/Free Full Text]
  15. Bondi, KR, Young, JM, Bennett, RM, et al Closing volume in man immersed to the neck in water. J Appl Physiol 1976;40,736-740[Abstract/Free Full Text]
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