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Michael R. Baria, MD; Andrea J. Boon, MBChB; Kaiser G. Lim, MD, FCCP
Author and Funding Information

From the Department of Physical Medicine and Rehabilitation (Drs Baria and Boon), the Division of Clinical Neurophysiology (Dr Boon), Department of Neurology, and the Department of Pulmonary and Critical Care Medicine (Dr Lim), Mayo Clinic and Foundation.

CORRESPONDENCE TO: Michael R. Baria, MD, Mayo Clinic and Foundation, PM&R, 200 First St SW, Rochester, MN 55905; e-mail: baria.michael@mayo.edu


FINANCIAL/NONFINANCIAL DISCLOSURES: The authors have reported to CHEST that no potential conflicts of interest exist with any companies/organizations whose products or services may be discussed in this article.

Reproduction of this article is prohibited without written permission from the American College of Chest Physicians. See online for more details.


Chest. 2014;146(4):e146-e148. doi:10.1378/chest.14-1228
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To the Editor:

We thank Drs Kumar and Chandra for their interest in our work1 and the opportunity to discuss the use of ultrasound imaging of the diaphragm in the clinical context. Regarding our hypothesis that the diaphragm might show hypertrophy in COPD, this was based on the assumption that the diaphragm may be more active in patients with COPD during quiet breathing than in healthy subjects with normal lung function. This would be consistent with the increased firing rate of diaphragm motor unit potentials reported by Ottenheijm et al2 during tidal breathing in patients with COPD. However, our study did not show any such compensatory hypertrophy, and although it is theoretically possible that accelerated protein degradation and associated atrophy could offset any compensatory hypertrophy, Ottenheijm et al2 actually did not find a reduction in cross-sectional area of diaphragm fibers in patients with mild to moderate COPD. Although they established a reduction in myosin content (which affects maximum force generation), this did not correlate with a change in cross-sectional area, and the atrophy they refer to appears to be at the molecular level, without affecting the gross anatomic structure. As they pointed out, changes in diaphragm structure and function in COPD are still poorly understood, and there is likely a complex interplay of multiple factors involved, but our goal was to establish normal thickness and thickening ratio in patients with COPD such that we could use these measures to diagnose superimposed phrenic neuropathy or other neuromuscular disease.

Regarding the second point, we concur that diaphragm thickness does not change consistently with lung volume and increases significantly above 50% of vital capacity, but we respectfully disagree with their statement that there is a large increase in thickness between relaxation and 10% of the inspiratory effort.3,4 We studied a group of 150 healthy subjects and found that the degree of diaphragm thickening during tidal breathing was highly variable from one individual to another, and > 30% of diaphragms did not thicken at all during quiet inspiration. Cohn et al3 also found a nonlinear relationship between diaphragm thickness and lung volume, with lower levels of thickening occurring earlier in inspiration and higher levels seen with lung volumes > 50%. Because of the different technique used by Wait et al5 (M mode ultrasound in the axial plane, as opposed to B mode ultrasound in the sagittal oblique plane used in our study and several others), direct comparisons cannot be made; however, we would like to point out that Wait et al5 only evaluated diaphragm thickening at lung volumes < 50% because of their methodology using M mode, in a small group of 10 normal men, and only reported the relationship of diaphragm thickening fraction to lung volume and not diaphragm thickness to lung volume.5 Given that the thickening fraction is derived directly from diaphragm thickness, there should be a similar relationship for both thickness and thickening fraction.

We agree with Gottesman and McCool6 that diaphragm thickness alone cannot always differentiate an atrophic paralyzed diaphragm from a normal diaphragm, hence the importance of evaluating the function of the diaphragm by looking at thickening ratio or thickening fraction.6 Regarding the comparison between thickening ratio and thickening fraction, both describe the same phenomenon but present the data in slightly different ways. Both methods have been used to evaluate diaphragm function with B mode ultrasound (Boon et al,7 De Bruin et al,8 and Ueki et al9 report thickening ratio, whereas Wait et al,5 Gottesman and McCool,6 McCool and Tzelepis,10 and Summerhill et al11 chose to report thickening fraction). If at any point in the inspiratory cycle there were a linear relationship between thickening ratio and lung volume, this should also be seen with thickening ratio.

We concur that looking at diaphragm thickening vs change in diaphragm length may be of interest, although we caution against using indirect measures of shortening,3,5,10,12 given the frequency of regional differences in diaphragm thickening and motion and the very wide range of normal thickening (20%-400%) in healthy control subjects.4,7,13

References

Baria MR, Shahgholi L, Sorenson EJ, et al. B-mode ultrasound assessment of diaphragm structure and function in patients with COPD. Chest. 2014;146(3):680-685. [CrossRef] [PubMed]
 
Ottenheijm CA, Heunks LM, Dekhuijzen PN. Diaphragm muscle fiber dysfunction in chronic obstructive pulmonary disease: toward a pathophysiological concept. Am J Respir Crit Care Med. 2007;175(12):1233-1240. [CrossRef] [PubMed]
 
Cohn D, Benditt JO, Eveloff S, McCool FD. Diaphragm thickening during inspiration. J Appl Physiol (1985). 1997;83(1):291-296. [PubMed]
 
Harper CJ, Shahgholi L, Cieslak K, Hellyer NJ, Strommen JA, Boon AJ. Variability in diaphragm motion during normal breathing, assessed with B-mode ultrasound. J Orthop Sports Phys Ther. 2013;43(12):927-931. [CrossRef] [PubMed]
 
Wait JL, Nahormek PA, Yost WT, Rochester DP. Diaphragmatic thickness-lung volume relationship in vivo. J Appl Physiol (1985). 1989;67(4):1560-1568. [PubMed]
 
Gottesman E, McCool FD. Ultrasfound evaluation of the paralyzed diaphragm. Am J Respir Crit Care Med. 1997;155(5):1570-1574. [CrossRef] [PubMed]
 
Boon AJ, Harper CJ, Ghahfarokhi LS, Strommen JA, Watson JC, Sorenson EJ. Two-dimensional ultrasound imaging of the diaphragm: quantitative values in normal subjects. Muscle Nerve. 2013;47(6):884-889. [CrossRef] [PubMed]
 
De Bruin PF, Ueki J, Bush A, Khan Y, Watson A, Pride NB. Diaphragm thickness and inspiratory strength in patients with Duchenne muscular dystrophy. Thorax. 1997;52(5):472-475. [CrossRef] [PubMed]
 
Ueki J, De Bruin PF, Pride NB. In vivo assessment of diaphragm contraction by ultrasound in normal subjects. Thorax. 1995;50(11):1157-1161. [CrossRef] [PubMed]
 
McCool FD, Tzelepis GE. Dysfunction of the diaphragm. N Engl J Med. 2012;366(10):932-942. [CrossRef] [PubMed]
 
Summerhill EM, El-Sameed YA, Glidden TJ, McCool FD. Monitoring recovery from diaphragm paralysis with ultrasound. Chest. 2008;133(3):737-743. [CrossRef] [PubMed]
 
McKenzie DK, Gandevia SC, Gorman RB, Southon FC. Dynamic changes in the zone of apposition and diaphragm length during maximal respiratory efforts. Thorax. 1994;49(7):634-638. [CrossRef] [PubMed]
 
Harris RS, Giovannetti M, Kim BK. Normal ventilatory movement of the right hemidiaphragm studied by ultrasonography and pneumotachography. Radiology. 1983;146(1):141-144. [CrossRef] [PubMed]
 

Figures

Tables

References

Baria MR, Shahgholi L, Sorenson EJ, et al. B-mode ultrasound assessment of diaphragm structure and function in patients with COPD. Chest. 2014;146(3):680-685. [CrossRef] [PubMed]
 
Ottenheijm CA, Heunks LM, Dekhuijzen PN. Diaphragm muscle fiber dysfunction in chronic obstructive pulmonary disease: toward a pathophysiological concept. Am J Respir Crit Care Med. 2007;175(12):1233-1240. [CrossRef] [PubMed]
 
Cohn D, Benditt JO, Eveloff S, McCool FD. Diaphragm thickening during inspiration. J Appl Physiol (1985). 1997;83(1):291-296. [PubMed]
 
Harper CJ, Shahgholi L, Cieslak K, Hellyer NJ, Strommen JA, Boon AJ. Variability in diaphragm motion during normal breathing, assessed with B-mode ultrasound. J Orthop Sports Phys Ther. 2013;43(12):927-931. [CrossRef] [PubMed]
 
Wait JL, Nahormek PA, Yost WT, Rochester DP. Diaphragmatic thickness-lung volume relationship in vivo. J Appl Physiol (1985). 1989;67(4):1560-1568. [PubMed]
 
Gottesman E, McCool FD. Ultrasfound evaluation of the paralyzed diaphragm. Am J Respir Crit Care Med. 1997;155(5):1570-1574. [CrossRef] [PubMed]
 
Boon AJ, Harper CJ, Ghahfarokhi LS, Strommen JA, Watson JC, Sorenson EJ. Two-dimensional ultrasound imaging of the diaphragm: quantitative values in normal subjects. Muscle Nerve. 2013;47(6):884-889. [CrossRef] [PubMed]
 
De Bruin PF, Ueki J, Bush A, Khan Y, Watson A, Pride NB. Diaphragm thickness and inspiratory strength in patients with Duchenne muscular dystrophy. Thorax. 1997;52(5):472-475. [CrossRef] [PubMed]
 
Ueki J, De Bruin PF, Pride NB. In vivo assessment of diaphragm contraction by ultrasound in normal subjects. Thorax. 1995;50(11):1157-1161. [CrossRef] [PubMed]
 
McCool FD, Tzelepis GE. Dysfunction of the diaphragm. N Engl J Med. 2012;366(10):932-942. [CrossRef] [PubMed]
 
Summerhill EM, El-Sameed YA, Glidden TJ, McCool FD. Monitoring recovery from diaphragm paralysis with ultrasound. Chest. 2008;133(3):737-743. [CrossRef] [PubMed]
 
McKenzie DK, Gandevia SC, Gorman RB, Southon FC. Dynamic changes in the zone of apposition and diaphragm length during maximal respiratory efforts. Thorax. 1994;49(7):634-638. [CrossRef] [PubMed]
 
Harris RS, Giovannetti M, Kim BK. Normal ventilatory movement of the right hemidiaphragm studied by ultrasonography and pneumotachography. Radiology. 1983;146(1):141-144. [CrossRef] [PubMed]
 
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