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European Journal of Heart Failure 2001 3(2):183-187; doi:10.1016/S1388-9842(00)00133-1
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© 2001 European Society of Cardiology

Altered diaphragm position and function in patients with chronic heart failure

Lynn Caruanaa, Mark C. Petriea, John J. McMurraya and Niall G. MacFarlaneb,*

a Department of Cardiology, Western Infirmary Glasgow G11 6NT, UK
b Centre for Exercise Science and Medicine, Institute of Biomedical and Life Sciences, Glasgow University Glasgow G12 8QQ, UK

* Corresponding author. Tel.: +44-141-330-5965; fax: +44-141-330-4100. E-mail address: n.macfarlane{at}bio.gla.ac.uk (N.G. MacFarlane).


   Abstract
Top
 Abstract
1. Introduction
 2. Methods
 3. Results
 4. Discussion
 References
 
Background: Breathlessness is a common symptom experienced by patients with chronic heart failure (CHF) but its etiology remains controversial. Various molecular and histological adaptations have been reported for the diaphragm in CHF but their functional consequences are poorly described.

Aims: This study aims to determine the position and function of the diaphragm in CHF patients.

Methods: The diaphragm position was measured, relative to the renal pelvis, by ultrasound in 20 CHF patients and ninety controls matched for age and body mass. The extent and velocity of diaphragm movement was also measured during quiet breathing and sniffing.

Results: At the end of expiration, the diaphragm was significantly nearer to the renal pelvis in CHF patients (89.3 ± 16.8 vs. 96.3 ± 19.2 mm, P < 0.05) and also moved further during quiet breathing (18.2 ± 4.4 vs. 12.7 ± 4.6 mm, P < 0.001) and sniffing (23.9 ± 7.4 vs. 18.2 ± 5.7 mm, P < 0.005). Velocity of diaphragm movement was also increased in CHF patients during quiet breathing (26.5 ± 8.2 vs. 15.9 ± 6.1 mm s–1, P < 0.001).

Conclusions: These data demonstrate that the position and function of the diaphragm is altered in CHF.

Key Words: Heart failure • Breathlessness • Ultrasound imaging • Diaphragm

Received July 20, 2000; Revised August 14, 2000; Accepted October 12, 2000


   1. Introduction
Top
 Abstract
 1. Introduction
2. Methods
 3. Results
 4. Discussion
 References
 
Chronic heart failure (CHF) is a well recognised syndrome in which myocardial contractile dysfunction results in a constellation of secondary changes in other organ systems [1]. Exertional fatigue and breathlessness are perhaps the most common and debilitating symptoms experienced by CHF patients but their aetiology remains controversial [2–4].

The conventional explanation for orthopnoea, exertional dyspnoea and fatigue is that the neuroendocrine response to left ventricular dysfunction results in sodium and water retention, increasing left atrial pressure and maintaining cardiac output through the Starling mechanism [5]. This increase in left atrial pressure produces a parallel rise in pulmonary venous pressure and predisposes to pulmonary congestion and dyspnoea. Failure of the Starling mechanism to increase cardiac output and oxygen delivery to exercising muscle will result in premature fatigue [6]. It is apparent, however, that dyspnoea is not simply related to pulmonary venous congestion and that there are a number of contributing factors. Afferent neuronal activity arising from medullary and peripheral chemoreceptors, respiratory muscles and the lungs will all contribute to the perception of respiratory activity [7].

The diaphragm is regarded as the primary inspiratory muscle and accounts for approximately 70% of the tidal volume exchanged under normal conditions [8]. The diaphragm is similar to limb skeletal muscle in that its ability to generate force efficiently is related to the length of the muscle fibres and the stimulation frequency applied to the muscle [9]. Efficient respiratory muscle function is dependent upon accurate afferent information on its position and load, and although the intercostals compensate for loads with a rich supply of muscle spindles, the diaphragm contains few proprioceptive muscle spindles. It has been suggested that load changes on the diaphragm may be sensed via a phrenic to phrenic reflex or, in response to alterations in rib cage shape, an intercostal to phrenic reflex [10]. While the integration of afferent signals from different muscles is important for co-ordination of muscle contraction it has also been suggested that dyspneoa, the perception of difficult breathing, may be related to sensations of increased muscle tension conveyed by afferent mechanoreceptors [11].

A variety of molecular and histological adaptations have been described in the diaphragm during the development of CHF. An increase in the proportion of type I muscle fibres, reduced activity and protein levels for the sarcoplasmic reticulum calcium–ATPase and disproportionate atrophy of type II and type I muscle fibres have all been observed [12–14]. The functional consequences of these molecular and histological adaptations are poorly described but several studies suggest that the diaphragm is weak in both patients with CHF (using indirect methods of assessment) and animal models [15–19].

The purpose of the present study was, therefore, to determine if changes in diaphragm position and function occur in CHF patients using a recently developed non-invasive ultrasound technique. This study determines that the diaphragm is displaced downwards (both on inspiration and expiration) and moves further during normal quiet breathing and sniffing.


   2. Methods
Top
 Abstract
 1. Introduction
 2. Methods
3. Results
 4. Discussion
 References
 
2.1. Study population
Twenty patients with chronic (>3 months) heart failure due to left ventricular systolic dysfunction (left ventricular ejection fraction, LVEF, <0.40) were recruited from the outpatients clinics of the Department of Cardiology in the Western Infirmary, Glasgow, UK. Ninety controls matched for age and body mass were recruited from an open access echocardiography clinic and had normal left ventricular function (e.g. LVEF>0.40) and normal pulmonary function tests (FEV1, FVC, VC and TLC all >0.95 of predicted). Ethical approval was obtained from the local institutional committee for human research and informed consent was obtained from all subjects. Details of both subject groups are given in Table 1.


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  		Table 1 Patient characteristics and clinical featuresa

 
2.2. Echocardiography
Cardiac ultrasound examinations were performed using an Acuson 128 XP10c ultrasound imaging system, with the patients recumbent in the left lateral decubitis position. The same operator performed all examinations and a physician reported the studies. Assessment of left ventricular function was made quantitatively by calculating ejection fraction (%) from the relative change in ventricular volume between the end of diastole and systole (ventricular volumes were calculated from an apical four-chamber view using the disc summation method, i.e. Simpson's rule). Left ventricular mass was calculated using the Penn convention with end diastole taken at the onset of the QRS complex. All measurements were repeated six times and means calculated for statistical analysis.

2.3. Diaphragm ultrasonography
Ultrasound records of the diaphragm position and excursion were obtained using the same Acuson 128 XP10c ultrasound imaging system with a 4.0-MHz transducer. An intercostal probe position was chosen between the mid-axillary and anterior-axillary lines. The transducer was held in a fixed skin position during all phases of respiration. Scans of the right hemi-diaphragm were performed in a longitudinal plane that included the maximal renal bipolar length. Movement of the chest wall and abdomen was observed to exclude paradoxical movement of the diaphragm during respiration.

The position of the diaphragm was measured relative to the renal pelvis using the two-dimensional images obtained. Craniocaudal excursion was measured from the mid-point of the kidney to a point on the diaphragm at the same depth form the transducer on the ultrasound scan (see Fig. 1). The distance between these points was then measured on maximal inspiration (2Dinsp) and at the end of expiration (2Dexp).


Figure 1
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  		Fig. 1 Schematic showing the relative position of the ultrasound transducer to the right kidney and the diaphragm during the respiratory cycle. The position of the diaphragm is shown by a solid line at end-expiration and by a broken line on inspiration. The craniocaudal excursion from the midpoint of the kidney at the end of expiration (2Dexp) and on maximal inspiration (2Dinsp) are shown by * and **, respectively. The dotted line from the transducer represents the approximate position of the M-mode cursor during measurement of the posterior–anterior (PA) excursion of the right hemi-diaphragm during quiet breathing and sniffing.

 
As a separate measurement, the posterior–anterior (PA) excursion of the right hemi-diaphragm was measured from the M-mode image during quiet breathing. The M-mode cursor line was positioned at an angle of not less than 70o to the craniocaudal displacement line of the diaphragm (see Fig. 1). From the M-mode trace, the maximum PA displacement of that part of the diaphragm during each respiratory cycle was determined and at least six consecutive respiratory cycles were recorded during quiet breathing (Qex). The PA excursion was also measured during a voluntary sniff (Sex), a sniff being defined as a rapid inspiration through the nose with a similar volume to that in quiet breathing, i.e. it was not a deep breath in. In addition to measuring the magnitude of the diaphragmatic excursion, the velocity of diaphragm movement was also calculated during quiet breathing (Qv) and sniffing (Sv).

2.4. Variability and limitations of diaphragm ultrasonography
The intra-observer coefficients of variation (CV) for quiet breathing and sniffing were 12 and 7%, respectively. The measurements were made in the left lateral decubitis position and it is unknown whether the differences observed in this study also exist in the prone position, however, this position does limit any compensatory active expiration by the anterior abdominal wall [20].

2.5. Influence of body mass
Obesity or anorexia may have a significant influence on the position of the diaphragm and consequently on the measures recorded here. However, we found no correlation between body surface area and body mass index and the position of the diaphragm in two-dimensional images recorded during this study [e.g. BSA and 2Dexp gave the greatest correlation coefficient (r) at 0.095]. Nevertheless, patients were also matched for body surface area and body mass index in this study.

2.6. Statistical analysis
Comparison of the measures for diaphragm position and function were made using unpaired Student's t-tests. For all statistical relationships significance was taken at the 5% level and data are expressed as mean±S.D.


   3. Results
Top
 Abstract
 1. Introduction
 2. Methods
 3. Results
4. Discussion
 References
 
3.1. Characterisation of left ventricular function and morphology
Table 1 illustrates that all the patients in this study had a previous myocardial infarction and represent a homogenous group with ischaemic cardiomyopathy. Left ventricular systolic function was significantly depressed in the CHF population compared with controls (LVEF was calculated as 26.7±11.1 vs. 45.6±9.2%, P<0.001). Left ventricular mass and left ventricular mass index were significantly increased in the CHF population (325.0±21.1 vs. 202.1±11.3 g, P<0.001 and 186.3±15.3 vs. 104.1±6.7 g/m2 P<0.001).

3.2. Diaphragm displacement in CHF
The relative position of the diaphragm from the mid-point of the kidney in two-dimensional images obtained from CHF patients and controls are shown in Fig. 2. During normal breathing, at the end of expiration, the diaphragm in CHF patients was nearer to the renal pelvis than in controls matched for age and mass (i.e. 2Dexp was 89.3±16.8 vs. 96.3±19.2 mm, P<0.05). At maximal inspiration, however, there was no significant difference in the displacement of the diaphragm from the renal pelvis between CHF patients and controls (i.e. 2Dinsp was 80.5±17.0 vs. 86.6±18.8 mm, P=0.10).


Figure 2
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  		Fig. 2 Graph illustrating the relative position of the diaphragm in CHF patients (filled bars) and controls (open bars). 2Dinsp is the distance between the mid-point of the kidney and a point on the diaphragm at the same depth from the transducer measured on maximal inspiration; 2Dexp is a similar measurement made at the end of expiration. *P<0.05 between CHF patients and controls.

 
3.3. Diaphragm function in CHF
The velocity and extent of PA excursion by the right hemi-diaphragm during normal breathing and sniffing is shown in Fig. 3. During normal breathing, the CHF patients diaphragm's moved further than controls (i.e. Qex was 18.2±4.4 vs. 12.7±4.6 mm, P<0.001). The time of the inspiratory phase and respiratory rate was similar in both groups (i.e. 0.77±0.20 vs. 0.81±0.23 s, P=0.37; 19.6±2.3 vs. 20.4±2.2 breaths/min, P=0.42). This meant that the velocity of diaphragm excursion was increased in the CHF patients (i.e. Qv was 26.5±8.2 vs. 15.9±6.1 mm s–1, P<0.001).


Figure 3
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  		Fig. 3 Graph illustrating the extent of diaphragm movement (upper panel) during normal breathing and sniffing in CHF patients (filled bars) and controls (open bars). The velocity of the diaphragm movement during normal breathing is shown on the lower panel. Qex is the maximum PA displacement of the diaphragm during a respiratory cycle while breathing quietly; Sex is a similar measure during a maximum voluntary sniff. The velocity of diaphragm movement during quiet breathing is Qv **P<0.005 and ***P<0.001 between CHF patients and controls.

 
During a maximum voluntary sniff, however, both time of the inspiratory phase and velocity of diaphragm excursion were similar between groups (i.e. time for inspiration was 0.23±0.05 vs. 0.22±0.06 s, P=0.35; Sv was 103.6±29.5 vs. 91.7±54.6 mm s–1, P=0.18) but the diaphragm in CHF patients moved further than controls (i.e. Sex was 23.9±7.4 vs. 18.2±5.7 mm, P<0.005).

3.4. Relationship of diaphragm position and function to LV morphology and function in CHF
The position and function of the diaphragm in the CHF patients showed a moderate, but significant, correlation with left ventricular systolic function (e.g. 2Dexp gave the greatest correlation coefficient with LVEF at r=0.52, P<0.05). Changes in left ventricular morphology did, however, show a good correlation with the position and function of the diaphragm (e.g. r=0.90, P<0.001 for left ventricular end diastolic dimension, LVEDD, and craniocaudal excursion of the diaphragm; r=0.91, P<0.001 for left ventricular end diastolic dimension, LVEDD, and posterior-anterior excursion of the diaphragm).


   4. Discussion
Top
 Abstract
 1. Introduction
 2. Methods
 3. Results
 4. Discussion
References
 
The mechanics of breathing require a gradient of pressure in the airways to move air in and out of the lungs. An intrapleural pleural pressure gradient is developed by increasing thoracic volume during inspiration (predominantly by contraction and flattening of the diaphragm) and decreasing thoracic volume during expiration (normally a passive process at rest brought about by relaxation of the inspiratory muscles). Thus the position of the diaphragm is important not only in terms of the length-tension relationship for muscle contraction but also for the change in thoracic volume to generate an appropriate intrapleural pressure. Respiratory muscle length is normally dependent on lung volume, and the optimal length for diaphragm contraction occurs slightly below functional residual capacity.

In this study we observed a downward (craniocaudal) displacement of the diaphragm in CHF patients at the end of expiration that was strongly correlated with the changes of left ventricular morphology observed in the CHF patients. Thus the diaphragm displacement could represent and adaptive response to a change in the cardio-thoracic ratio (by direct mechanical displacement of the diaphragm due to an increase in heart size). The displacement of the diaphragm should, if resulting from a passive process, give rise to a decrease in muscle fibre length (in an analogous way to lung hyper-inflation). A reduction in muscle fibre length will compromise the ability of the diaphragm to produce force and decrease the velocity of shortening (e.g. lung reduction surgery in chronic obstructive pulmonary disease improves diaphragm contractility by reducing passive displacement). Our observations show, however, that the velocity of the diaphragm's excursion (equivalent to velocity of shortening) is actually increased in CHF patients.

A further consequence of any downward displacement diaphragm should be an increase in the total thoracic volume. Such an increase is likely to require that the diaphragm move further during inspiration to produce the same relative increase in thoracic volume that will be required to generate an appropriate airway pressure gradient. The data provided by this study also demonstrates that diaphragm excursion is greater in CHF patients during quiet breathing and is consistent with diaphragm displacement.

These observations force us to conclude that the diaphragm displacement we observe is the result of an ‘active’ process (i.e. the muscle is pre-contracted and has an increased level of intrinsic tension). In this situation, the altered diaphragm position will be associated with an increase in the load on the muscle and stimulate muscle mechanoreceptors that will contribute to the increased perception of breathlessness in CHF patients.


   References
Top
 Abstract
 1. Introduction
 2. Methods
 3. Results
 4. Discussion
 References
 

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