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 ISI Web of Science (4)
Right arrow Citing Articles via Google Scholar
Google Scholar
Right arrow Articles by Olson, T. P.
Right arrow Articles by Johnson, B. D.
Right arrow Search for Related Content
PubMed
Right arrow PubMed Citation
Right arrow Articles by Olson, T. P.
Right arrow Articles by Johnson, B. D.
(Chest. 2006;130:164-171.)
© 2006 American College of Chest Physicians

Competition for Intrathoracic Space Reduces Lung Capacity in Patients With Chronic Heart Failure*

A Radiographic Study

Thomas P. Olson, PhD; Kenneth C. Beck, PhD; Jacob B. Johnson, BS and Bruce D. Johnson, PhD

* From the Division of Cardiovascular Diseases, Department of Internal Medicine, Mayo Clinic and Foundation, Rochester, MN.

Correspondence to: Bruce D. Johnson, PhD, Associate Professor of Medicine, Division of Cardiovascular Diseases, Gonda 5–369, Mayo Clinic, Rochester, MN 55905; e-mail: johnson.bruce{at}mayo.edu

Abstract

Background: The purpose of this study was to determine the influence of changes in cardiac size on total lung volume in patients with chronic heart failure compared to control subjects.

Methods: Forty-four patients and age-, gender-, and height-matched control participants were recruited. All participants underwent posteroanterior and lateral chest radiography for volumetric estimations of the total thoracic cavity (TTC), diaphragm, heart, and lungs. To assess the relationship between chronic heart failure severity and cardiac enlargement, patients with chronic heart failure were classified into groups based on New York Heart Association class, as follows: class I and II, n = 26 (group A); class III and IV, n = 18 (group B).

Results: There was no difference between the groups for TTC volume (TTCV) [p = 0.56]. Cardiac volumes were significantly different between all groups for both the absolute volumes (p < 0.001) were calculated as a percentage of TTCV (p < 0.001), with the largest cardiac volumes in group B (twice the volume of healthy control subjects). When expressed as a percentage of TTCV, there also was a clear reduction in lung volumes as a function of disease severity (p < 0.001).

Conclusions: The present study demonstrates a close relationship between the severity of heart failure and cardiac size. These changes in cardiac size within a closed thoracic cavity may pose significant constraints on the lungs, resulting in reductions in lung volumes that likely play a major role in the restrictive breathing patterns often reported in patients with chronic heart failure.

Key Words: cardiomegaly • lung volume • roentenography

Chronic heart failure is a progressive disease resulting in severe morbidity and mortality. Interestingly, certain resting measures of cardiac function (ie, ejection fraction [EF]) correlate poorly with exercise tolerance, and thus it is clear that chronic heart failure becomes a systemic disorder, influencing a number of organ systems that may contribute to activity intolerance.1 Because the pulmonary system lies in series with the heart, accepts nearly all of the cardiac output, and is exposed to similar intrathoracic pressure changes, it would be expected that changes in cardiac structure and function may have adverse consequences on the pulmonary system. Most studies2345 suggest mild-to-moderate changes in the pulmonary system with chronic heart failure, including both restrictive and obstructive changes as well as a reduction in lung diffusing capacity. Causes for changes in lung function remain unclear but have been thought to be related to respiratory muscle weakness, chronic pulmonary hypertension, and changes in lung fluid balance.67 Another possible contributor to the changes in pulmonary function relates to the progressive cardiac enlargement within a closed thoracic cavity. Such changes in cardiac volume would result in primarily restrictive lung changes manifested as reductions in total lung volume as well as vital capacity.89

Previous studies10 have reported marked changes in cardiac size as heart failure progresses. Such changes in cardiac size could clearly "steal" volume from the lungs, as the lungs are more compliant than the heart. Previously, we reduced lung volumes in healthy adults by 40% through chest wall strapping in order to increase the competition for intrathoracic space between the heart and lungs.11 Despite the marked reductions in lung volumes, there was relatively little impact on cardiac function. These findings are consistent with the much higher lung compliance as compared to the heart. To date, few studies121314 have closely examined the relationship between cardiac size and the alterations in lung volume within a closed thoracic cavity in the chronic heart failure population.

The purpose of this study was to examine the relationship between the radiographically determined thoracic, cardiac, and lung volumes in heart failure patients as compared to control participants without known cardiovascular disease. We hypothesized that the increased competition for intrathoracic space caused by changes in cardiac volume associated with chronic heart failure contributes significantly to the restrictive pulmonary changes observed in this population, and that these changes are associated with severity of chronic heart failure.

Materials and Methods

Population Characteristics
This retrospective analysis utilized data from 44 chronic heart failure patients from the database of the Mayo Clinic Heart Failure Service or the Cardiovascular Health Clinic (a preventive and rehabilitative center) from 2000 to 2004 (Table 1 ). Inclusion criteria included patients with a history of ischemic or dilated cardiomyopathy, stable heart failure symptoms (> 3 months), duration of heart failure symptoms > 1 year, left ventricular EF ≤ 35%, body mass index (BMI) < 35 kg/m2, and nonsmokers with a smoking history < 10 pack-years. Patients were treated with standard optimized medications for heart failure at the time of the study. An equal number of control participants were recruited via advertisement from the surrounding area and were matched with the heart failure group for age, gender, and height. Control participants had normal cardiac function (EF > 50%) and were without history of hypertension, lung disease, or coronary artery disease. All participants gave written informed consent after being provided a description of study requirements. The study protocol was approved by the Mayo Clinic Institutional Review Board; all procedures followed institutional and Health Insurance Portability and Accountability Act guidelines.


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

  		Table 1.. Differences in Participant Characteristics Between Study Groups*

 
Overview of Protocol
All participants underwent posteroanterior and lateral chest radiography. Patients with chronic heart failure were classified into two groups based on New York Heart Association (NYHA) class as follows: class I and II, n = 26 (group A), and class III and IV, n = 18 (group B).

Radiographic Volumetric Estimation
The posteroanterior and lateral radiographic views were used to make volumetric estimations of the total thoracic cavity (TTC), diaphragm, cardiac, and lungs based on the assumptions of a partial ellipsoid as initially described by Barnhard and colleagues15 and subsequently by others.16171819 This methodology has repeatedly been shown to be valid and reliable.1617 Briefly, volumetric measures were determined by manually tracing on a digitizing tablet (AccuGrid A43BL; Numonics Corporation; Montgomeryville, PA) the innermost edge of the intrathoracic cavity and the outermost edge of the cardiac silhouette on both radiographic views with data exported to a digitizing software program (Didger 3; Golden Software; Golden, CO) on a personal computer for off-line analysis. Coordinate data obtained from the digitizing software program were used to make linear measurements for the volumetric computation.

The TTC volume (TTCV) was determined as follows: (1) the posteroanterior and lateral view-digitized tracings were divided vertically into five sections, with the upper two sections equally divided into 2.75-cm segments, and the third and fourth sections equally divided between the most superior border of the diaphragm and lower border of the second section; (2) the fifth section included the region from the dome of the diaphragm to the insertion of the diaphragm with the rib cage; (3) and the volume of each elliptical cylindroid was calculated using the following formula:

Formula
where D1 is the width across the posteroanterior view, D2 is the depth from the lateral view, and D3 is the height of the posteroanterior view. Total thoracic volume was defined as the sum of each of the individual segment volumes (Fig 1 ).


Figure 1
View larger version (17K):
[in this window]
[in a new window]
[Download PPT slide]
  		Figure 1.. Representative digitized coordinate data plotted to demonstrate posteroanterior and lateral chest radiograph views with measurement sections as outlined in the "Materials and Methods" section.

 
Total cardiac volume was calculated using the following formula:

Formula
where D1 is the long diameter measured by establishing the longest line from the junction of the superior venous pedicle with the right atrium to the apex of the left ventricle from the posteroanterior view of the cardiac silhouette, D2 is the transverse diameter defined as the sum of two perpendicular lines extended from D1 to the furthest points of the left and right ventricular borders, and D3 is the depth of the cardiac silhouette defined as the longest diameter on the lateral view approximately perpendicular to D1 (Fig 1).

Total diaphragmatic volume was calculated using the following equation:

Formula
where D1 is the distance from the base of the of the posteroanterior view to the peak of the left diaphragm dome, D2 is the distance from the base of the posteroanterior view to the peak of the right diaphragm dome, and D3 is the width of the base of the lateral view (Fig 1).

Total pulmonary blood and parenchymal tissue volumes were estimated using a modified formula for body surface area,182021 as follows:

Formula
Total lung volume was calculated as the sum of the cardiac, diaphragmatic, pulmonary blood, and parenchymal tissue volumes subtracted from the TTCV, as follows:

Formula
As standard practice, participants were asked to maximally inspire immediately prior to obtaining the radiograph, and all radiographs were taken at a distance of 72 inches to ensure consistent target/film distances. To account for radiograph beam divergence, a correction factor (0.729) was applied to the final volumetric calculations.18

Statistical Analysis
Statistical analysis and graphic presentation were accomplished using statistical software (Prism version 4.0; Graphpad; San Diego, CA). One-way analysis of variance was used to test for differences in means among the groups, and unpaired t test was used to compare the means of the participant characteristics and radiographic variables between the control and chronic heart failure groups and between chronic heart failure groups. Pearson correlation coefficients were calculated between radiographic measures and measures of heart failure severity. Fisher Exact Test was used to examine the difference in medication usage and other categorical variables between groups. Statistical significance was set at p < 0.05 for all analyses. Data are presented as mean ± SD or number and percentage of the group, as appropriate.

Results

Population Characteristics
The clinical characteristics of each study group and the medications in use by the patients at the time of the study are reported in Tables 1, 2 , respectively. Notable differences between the groups include a significantly lower BMI for the control group compared to group A and group B (p < 0.05). These differences were due to a nonsignificant trend in the difference in body weight (p = 0.06) as opposed to differences in height. Also, the control group demonstrated significantly greater exercise habits as compared to either group A (p < 0.05) or group B (p < 0.05), with no significant differences between the chronic heart failure groups.


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

  		Table 2.. Heart Failure Patient Medications Separated by Group*

 
Radiographic Evaluation
The results of the radiographic volumetric measurements are reported in Table 3 . For absolute volumetric measurements, the groups differed significantly in diaphragmatic, cardiac, and blood and parenchymal tissue volumes (p < 0.05 for all) with a trend toward significance in lung volumes (p = 0.06) and no difference in total thoracic volume. Importantly, when examining these measurements as a percentage of the TTC, there were significant differences between the groups for all measurements (p < 0.05) except for the percent of the TTC volume that was blood and parenchymal tissue. The relationship between the NYHA class and absolute cardiac volume and percentage of the TTCV that is taken up by the heart is shown in Figure 2 , top, A, and bottom, B, respectively. The relationship between NYHA class and absolute lung volume and percentage of TTCV that is taken up by the lung is shown in Figure 3 , top, A, and bottom, B, respectively. These data suggest a clear relationship between increasing NYHA class and elevated cardiac volume and reduction in lung volume. Figure 4 demonstrates the close correlation (r = – 0.81, p < 0.001) between elevated cardiac size and reduction in lung volume within the entire population separated by groups.


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

  		Table 3.. Differences Between Groups in the Radiographic Volumetric Estimations*

 

Figure 2
View larger version (13K):
[in this window]
[in a new window]
[Download PPT slide]
  		Figure 2.. Top, A: Absolute cardiac volume measurement separated by groups. Bottom, B: Percentage of the total TTCV taken up by the heart separated by groups. *p < 0.05 vs control (CTL) group; {dagger}p < 0.05 vs group A.

 

Figure 3
View larger version (13K):
[in this window]
[in a new window]
[Download PPT slide]
  		Figure 3.. Top, A: Absolute lung volume measurement separated by groups. Bottom, B: Percentage of TTCV taken up by the lungs separated by groups. *p < 0.05 vs control group; {dagger}p < 0.05 vs group A. See Figure 2 legend for expansion of abbreviation.

 

Figure 4
View larger version (16K):
[in this window]
[in a new window]
[Download PPT slide]
  		Figure 4.. Correlation between the percentage of TTCV taken up by the heart and lungs for the study population divided by groups. {circ}, control; {blacksquare}, group A; {square}, group B.

 
Discussion

In this study, we found the following in patients with heart failure compared to control participants: (1) marked increases in cardiac size reaching twice that of healthy age- and gender-matched control participants; (2) a clear relationship between the severity of heart failure and increase in cardiac size; (3) and a negative correlation between the percentage of TTC occupied by lung and the percentage of TTC occupied by the heart. These findings demonstrate that a progressive increase in cardiac volume in chronic heart failure plays a significant role in the loss of lung volume and function that has been associated with this patient population.

A number of studies2142223 have examined pulmonary function before and after cardiac transplantation. Although there are a number of physiologic changes that may account for the improvements in lung function after transplantation (eg, reduced pulmonary hypertension and congestion), alteration of cardiac size in relation to other organs occupying the thoracic cavity (ie, the lungs) is a likely mechanism through which improvement in pulmonary function occur. For instance, Ravenscraft et al22 demonstrated that correction of severe congestive heart failure by cardiac transplantation results in normalization of FVC, FEV1, and total lung capacity (TLC). Similarly, Hosenpud and colleagues14 demonstrated that spirometrically assessed pulmonary function (ie, FVC and FEV1) in pretransplant heart failure patients were significantly improved 15 months after cardiac replacement; these authors suggest that the restrictive but not obstructive pulmonary limitations are at least in part directly related to the increased intrathoracic space occupied by the heart.

Only one study has attempted to examine the influence of cardiac size on lung function specifically in relation to the size of the thoracic cavity. Agostoni and colleagues13 demonstrated that heart failure patients with cardiomegaly defined by increased cardiothoracic index (the ratio between the maximal linear width measurement of the heart and thoracic cavity on the posteroanterior view of the chest radiograph) have significantly reduced FEV1 and vital capacity. These authors13 also suggest that, due to the increase in cardiac size, diffusion capacity of the lung suffers adversely, primarily as a consequence of a reduction in membrane diffusion as opposed to pulmonary capillary blood volume. Although moderate but significant correlations were observed between the cardiothoracic index and various components of pulmonary function, these findings may be underestimated for a number of reasons. For instance, these authors13 only examined these relationships based on a one-dimensional measure of the thorax and heart. Also, they did not report data on the pulmonary thoracic index or other radiographically determined lung measurements. Thus, it is difficult to extrapolate these findings to true cardiac or lung volumes in relation to the volume of the thoracic cavity.

The present investigation sought to expand this previous work and to gain a better understanding of the actual changes in cardiac volume in patients with stable chronic heart failure according to disease severity. In addition, we determined the impact that changes in cardiac volume have on lung volume using a three-dimensional volumetric analysis. Our results show a close association between the increase in cardiac volume and the loss of lung volume within a closed thoracic cavity, consistent with the restrictive pulmonary function pattern typically observed in heart failure patients.

Although not specifically examined in the present study, the increase in heart size and reduction in lung volumes likely contribute to the rapid and shallow breathing patterns often observed in this population, particularly during exercise.1124 This type of pattern may subsequently play a role in limiting exercise tolerance. Work by Nanas et al25 suggested that inspiratory capacity (IC) was the best predictor of functional capacity in patients with chronic heart failure. Therefore, restrictive lung changes would lead to a high elastic load to inspiration and likely result in a reduced IC. Our data do suggest that this reduction in IC could simply be related to the direct relationship between loss of lung volume secondary to increased heart size and disease severity.

Interestingly, absolute diaphragm volume was significantly elevated in both heart failure groups as compared to control subjects, although only a difference between the patients with more severe chronic heart failure and control subjects was demonstrated when diaphragm volume was examined as a percentage of TTCV. These differences may be attributed to type II muscle fiber atrophy or a change in the motor unit recruitment during contraction associated with the disease.26 This muscle fiber atrophy is associated with significant reductions in tissue force generation, thus limiting resting tonality and potentially contributing the upward crescent shape of the diaphragm.27 Another potential contributor to the increased diaphragm volume includes ascites. Mutoh and colleagues28 have shown, using a piglet model, a 40% reduction in TLC as a result of increased abdominal volume through a surgically implanted water-filled balloon. Although this relationship has yet to be fully examined in humans, the majority of the heart failure patients in the present study were clinically stable and did not have apparent ascites or otherwise significant abdominal distension.

Limitations
Importantly, a potential limitation to this study is the use of a single equation to estimate pulmonary blood and parenchymal tissue volumes in control subjects and patients with chronic heart failure. Understandably, the use of a single prediction equation may have a tendency to slightly underestimate actual volumes in this population. Until recently, pulmonary fluid accumulation was thought to be a chronic process occurring as a result of cardiac contractile insufficiency leading to elevated left atrial pressure, increased pulmonary venous pressure, and concomitant distension of the pulmonary vasculature, coupled with generalized central and peripheral fluid accumulation and retention.2930 However, data suggest that pulmonary edema may be an acute process of fluid redistribution, often developing more rapidly over a few hours.2931 Because the lung blood and parenchymal volumes were only a small fraction of the total volumes studied and each of the chronic heart failure patients in this study were receiving optimally managed medical therapy and were hemodynamically stable at the time of the radiograph measures, we feel this estimate provides sufficient information to draw relevant conclusions regarding cardiac and pulmonary measurements and does not detract from the relationships presented. It is also likely that if the pulmonary blood volume was slightly elevated in parallel to disease severity, we in fact may have slightly underestimated the cardiac effect on lung volume.

Another potential limitation to this study is the retrospective nature of the radiograph analysis. This retrospective portion of the study was conducted on data from patients who volunteered to participate in a prospective study examining the effects of cardiopulmonary interactions in heart failure patients. Although the analysis remains retrospective, all of the available participants who met the inclusion criteria were utilized in this analysis thus minimizing potential bias.

Clinical Implications
Posteroanterior and lateral chest radiographs are common clinical procedures for patients with heart failure. By using volumetric analysis of radiographs, estimates can be made of changes in cardiac, lung, diaphragm, and total thoracic volume. The changes observed in cardiac size within a closed thoracic cavity may pose significant constraints on the lung, resulting in significant reductions in lung volumes and resulting in the restrictive breathing pattern often reported in heart failure patients.24 In addition, the cardiomegaly associated changes in lung function may contribute to the inspiratory load, limit the encroachment on the inspiratory reserve volume during times of increased ventilatory demand, and contribute to symptoms of dyspnea.

Acknowledgements

The authors thank Kathy O’Malley and Minelle LaPolice for their help in data acquisition and management.

Footnotes

Abbreviations: BMI = body mass index; EF = ejection fraction; IC = inspiratory capacity; NYHA = New York Heart Association; TTC = total thoracic cavity; TTCV = total thoracic cavity volume

This work was supported in part by National Institutes of Health grants HL71478 and HL07111.

The authors of this manuscript do not have any conflicts of interest to disclose.

Received for publication October 18, 2005. Accepted for publication January 12, 2006.

References

  1. Braunwald, E, Zipes, DP, Libby, P (2000) Heart disease: a textbook of cardiovascular medicine 6th ed. W.B. Saunders. Philadelphia, PA:
  2. Dimopoulou, I, Daganou, M, Tsintzas, OK, et al Effects of severity of long-standing congestive heart failure on pulmonary function. Respir Med 1998;92,1321-1325[CrossRef][ISI][Medline]
  3. Kindman, LA, Vagelos, RH, Willson, K, et al Abnormalities of pulmonary function in patients with congestive heart failure and reversal with ipratropium bromide. Am J Cardiol 1994;73,258-262[CrossRef][ISI][Medline]
  4. Light, RW, George, RB Serial pulmonary function in patients with acute heart failure. Arch Intern Med 1983;143,429-433[Abstract]
  5. Wright, RS, Levine, MS, Bellamy, PE, et al Ventilatory and diffusion abnormalities in potential heart transplant recipients. Chest 1990;98,816-820[Abstract/Free Full Text]
  6. Daganou, M, Dimopoulou, I, Alivizatos, PA, et al Pulmonary function and respiratory muscle strength in chronic heart failure: comparison between ischaemic and idiopathic dilated cardiomyopathy. Heart 1999;81,618-620[Abstract/Free Full Text]
  7. Puri, S, Baker, BL, Oakley, CM, et al Increased alveolar/capillary membrane resistance to gas transfer in patients with chronic heart failure. Br Heart J 1994;72,140-144[Abstract/Free Full Text]
  8. Little, RW, George, RB Serial pulmonary function in patients with acute heart failure. Arch Intern Med 1983;143,429-433[Abstract]
  9. Faggiano, P, Lombardi, C, Sorgato, A, et al Pulmonary function tests in patients with congestive heart failure: effects of medical therapy. Cardiology 1993;83,30-35[CrossRef][ISI][Medline]
  10. Grossman, W, Jones, D, McLaurin, LP Wall stress and patterns of hypertrophy in the human left ventricle. J Clin Invest 1975;56,56-64[ISI][Medline]
  11. Miller, JD, Beck, KC, Joyner, MJ, et al Cardiorespiratory effects of inelastic chest wall restriction. J Appl Physiol 2002;92,2419[Abstract/Free Full Text]
  12. Enright, PL, Kronmal, RA, Smith, VE, et al Reduced vital capacity in elderly persons with hypertension, coronary heart disease, or left ventricular hypertrophy: the Cardiovascular Health Study. Chest 1995;107,28-35[Abstract/Free Full Text]
  13. Agostoni, P, Cattadori, G, Guazzi, M, et al Cardiomegaly as a possible cause of lung dysfunction in patients with heart failure. Am Heart J 2000;140,e24
  14. Hosenpud, JD, Stibolt, TA, Atwal, K, et al Abnormal pulmonary function specifically related to congestive heart failure: comparison of patients before and after cardiac transplantation. Am J Med 1990;88,493-496[CrossRef][ISI][Medline]
  15. Barnhard, HJ, Pierce, JA, Joyce, JW, et al Roentgenographic determination of total lung capacity. Am J Med 1960;28,51-60[CrossRef][ISI][Medline]
  16. Miller, RD, Offord, K Roenthenologic determination of total lung capacity. Mayo Clin Proc 1980;55,694-699[ISI][Medline]
  17. Glenn, WV, Greene, R Rapid computer-aided radiographic calculation of total lung capacity (TLC). Radiology 1975;117,269-273[Abstract]
  18. Rodgers, RPC, Tannen, R Rapid and accurate determination of total lung capacity (TLC) from routine chest radiograms using a programmable hand-held calculator. Comput Biol Med 1983;13,125-140[ISI][Medline]
  19. Keats, TE, Enge, IR Cardiac mensuration by the cardiac volume method. Radiology 1965;85,850-855[ISI][Medline]
  20. Yu, PN Pulmonary blood volume in health and disease. 1969 Lea and Febiger. Philadelphia, PA:
  21. DuBois, D, DuBois, EF A function to estimate the approximate surface area if height and weight be known. Arch Intern Med 1916;17,863-871[ISI]
  22. Ravenscraft, SA, Gross, CR, Kubo, SH, et al Pulmonary function after successful heart transplantation: one-year follow-up. Chest 1993;103,54-58
  23. Bussietes, LM, Pflugfelder, PW, Ahmad, D, et al Evolution of resting lung function in the first year after cardiac transplantation. Eur Respir J 1995;8,959-962[Abstract]
  24. Johnson, BD, Beck, KC, Olson, LJ, et al Ventilatory constraints during exercise in patients with chronic heart failure. Chest 2000;117,321-332[Abstract/Free Full Text]
  25. Nanas, S, Nanas, J, Papazachou, O, et al Resting lung function and hemodynamic parameters as predictors of exercise capacity in patients with chronic heart failure. Chest 2003;123,1386-1393[Abstract/Free Full Text]
  26. Howell, S, Maarek, JM, Fournier, M, et al Congestive heart failure: differential adaptation of the diaphragm and latissimus dorsi. J Appl Physiol 1995;79,389-397[Abstract/Free Full Text]
  27. Supinski, G, DiMarco, A, Dibner-Dunlap, M Alterations in diaphragm strength and fatiguability in congestive heart failure. J Appl Physiol 1994;76,2707-2713[Abstract/Free Full Text]
  28. Mutoh, T, Lamm, WJ, Embree, LJ, et al Abdominal distension alters regional pleural pressures and chest wall mechanics in pigs in vivo. J Appl Physiol 1991;70,2611-2618[Abstract/Free Full Text]
  29. Cotter, G, Kaluski, E, Moshkovitz, Y, et al Pulmonary edema: new insight on pathogenesis and treatment. Curr Opin Cardiol 2001;16,159-163[CrossRef][ISI][Medline]
  30. Gehlbach, BK, Geppert, E The pulmonary manifestations of left heart failure. Chest 2004;125,669-682[Abstract/Free Full Text]
  31. Northridge, D Furosemide or nitrates for acute heart failure. Lancet 1996;347,667-668[CrossRef][ISI][Medline]




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 ISI Web of Science (4)
Right arrow Citing Articles via Google Scholar
Google Scholar
Right arrow Articles by Olson, T. P.
Right arrow Articles by Johnson, B. D.
Right arrow Search for Related Content
PubMed
Right arrow PubMed Citation
Right arrow Articles by Olson, T. P.
Right arrow Articles by Johnson, B. D.

HOME HELP FEEDBACK SUBSCRIPTIONS ARCHIVE SEARCH TABLE OF CONTENTS