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(Radiology. 2000;215:574-583.)
© RSNA, 2000

Technical Developments

Diaphragm and Chest Wall: Assessment of the Inspiratory Pump with MR Imaging-Preliminary Observations1

Philippe Cluzel, MD, Thomas Similowski, MD, PhD, Carl Chartrand-Lefebvre, MD, Marc Zelter, MD, PhD, Jean-Philippe Derenne, MD and Philippe A. Grenier, MD

1 From the Departments of Diagnostic and Interventional Radiology (P.C., C.C.L., P.A.G.) and Respiratory and Intensive Care Medicine (T.S., J.P.D.) and the Pulmonary Function Test Laboratory (M.Z.), Hôpital Pitié-Salpêtrière, 43-87 boulevard de l'Hôpital, 75651 Paris 13, France; Unité Propre de Recherche de l'Enseignement Supérieur, Université Pierre et Marie Curie, Paris, France (T.S., M.Z., J.P.D.); and Institut National de la Santé et de la Recherche Médicale, Paris, France (P.A.G.). Received December 28, 1998; revision requested February 19, 1999; final revision received September 28; accepted October 12. Supported in part by grant PHRC 95009 from Assistance-Publique Hôpitaux de Paris and a grant from the Société Française de Radiologie. Address correspondence to P.C. (e-mail: philippe.cluzel@psl.ap-hop-paris.fr).


   Abstract
TOP
 Abstract
Introduction
 Materials and Methods
 Results
 Discussion
 Appendix
 References
 
Magnetic resonance (MR) imaging of the thorax with three-dimensional (3D) reconstruction and functional quantification was evaluated as a tool for structure-function evaluation of chest-wall mechanics. Good agreement was found between the corresponding spirometric and MR imaging values of lung volumes. Fast MR imaging of the thorax with 3D reconstruction should improve the ability to evaluate the inspiratory pump in clinical and research investigations.

Index terms: Diaphragm, 66.92, 795.92 • Diaphragm, MR, 66.121412, 66.12144, 75.12144 • Lung, function, 60.919 • Magnetic resonance (MR), motion studies, 66.12144, 75.12144 • Thorax, MR, 47.121412, 47.12144


   Introduction
TOP
 Abstract
 Introduction
Materials and Methods
 Results
 Discussion
 Appendix
 References
 
Imaging of the lung and its diseases has traditionally been the main focus of the chest radiologic literature, whereas imaging of the inspiratory pump has received little attention. Recently, Gierada et al (1) investigated the feasibility of imaging diaphragmatic motion with a fast gradient-recalled-echo magnetic resonance (MR) pulse sequence. However, for research on the mechanics of ventilation, there is still a need for a reliable, noninvasive, three-dimensional (3D) technique to assess the action of the muscles that form the inspiratory pump (ie, the diaphragm and the accessory inspiratory muscles). Their combined actions on the thoracic cage are the major determinants of changes in lung volume.

In the past, the inspiratory pump was investigated by using a number of radiologic and nonradiologic techniques (2–11). These provided only an indirect assessment of diaphragmatic shortening or volume displacement because of the complex 3D shape of the diaphragm. The complexity of the chest wall in terms of its 3D geometry and the mechanical interdependence of its constituent components makes the analysis of only one of these elements in one or two dimensions very difficult, thus emphasizing the necessity for a 3D analysis.

To our knowledge, Whitelaw (12) was the first to construct a 3D picture of the diaphragm from serial transverse sections obtained with a computed tomographic (CT) scanner. Later, Paiva et al (13) described a human diaphragmatic shape at functional residual capacity (FRC) with MR imaging. More recently, Gauthier et al (14) increased our understanding of diaphragmatic mechanics by establishing the shapes of the diaphragm at various lung volumes with MR imaging and provided the first set of values for diaphragmatic functional surface areas. Pettiaux et al (15), from the same laboratory, developed a technique of diaphragmatic imaging with spiral CT. However, characterization of the shape of the diaphragm, even with quantitative measurements of its various components, is not sufficient to understand its mechanical action. Additional information is needed about the concomitant changes in the volumes encompassed by both the rib cage and the diaphragmatic dome.

In this article, we describe the feasibility of simultaneous 3D reconstruction of both the rib cage and the diaphragm with MR imaging for (a) the shape of the rib cage and the diaphragm, (b) the respective volumes displaced by the rib cage and the diaphragm, and (c) the relationship between these volumes and the surface areas of the relevant diaphragmatic zones. All data were measured at different lung volumes from residual volume (RV) to total lung capacity (TLC).


   Materials and Methods
TOP
 Abstract
 Introduction
 Materials and Methods
Results
 Discussion
 Appendix
 References
 
Data Collection
Subjects.—Five healthy male volunteers (age range, 27–33 years; mean age, 29.8 years) participated in the study. They were informed of the purpose of the study and the methods used prior to giving their written consent. The study was conducted according to local ethical and legal regulations.

Spirometry.—Lung volume measurements were obtained in a pulmonary function laboratory with use of a spirometer (Pulmonet III; Gould, Cleveland, Ohio) and the helium dilution technique. Procedures and quality criteria of the European Respiratory Society (16) were used for these measurements. Because normal values for lung volumes are available in only the sitting position, spirometry was first performed with the subjects seated to ensure their data were actually normal in this respect. Then the spirometric data were gathered with the subjects in the supine position to allow the two sets of measurements of lung volume spirometry and MR imaging to be comparable (Table 1). Measurements were made before and two times after the MR imaging sessions. The purpose of repeated measurements was to verify that the subjects performed reproducible maneuvers when asked to maintain FRC or go to TLC or RV.


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  		TABLE 1. Physical Characteristics and Supine Lung Volumes of Five Healthy Subjects
 
Image acquisition.—Subjects underwent coronal and sagittal MR imaging at 1.5 T (Signa; GE Medical Systems, Milwaukee, Wis) in the supine position at three different pulmonary volumes: RV, TLC, and FRC. We used a body coil and a fast gradient-recalled-echo pulse sequence (repetition time msec/echo time msec = 6.7/2.2 with a 30° flip angle, receiver bandwith of 32 kHz, field of view of 48 cm, section thickness of 10 mm, intersection gap of 0 mm, 128 x 256 matrix, and one signal acquired). Subjects were instructed not to move between the acquisitions, and all the sagittal or coronal sections were acquired in the same series during the same session. Therefore, the coordinates of all voxels for each section were in the same frame of reference, those of MR imaging. For each pulmonary volume, 22–27 coronal sections and 30–33 sagittal sections were acquired in 22–33 seconds of apnea. One hundred sixty to 180 images were obtained for each subject. Only the set of sagittal sections was used for 3D reconstruction.

Control of lung volume and relaxation during acquisition.—These elements are crucial for the 3D reconstruction of the diaphragm to be reliable and representative; therefore, maximal care was taken to control them. During the acquisitions, the subjects used a bell spirometer. The corresponding trace was monitored online by an operator who checked the adequacy of lung volume before each acquisition and closed a buccal valve manually at each target volume. After the subjects were trained to relax against the buccal valve, acquisitions were performed during a breath hold with the glottis open. This allowed the series of coronal and sagittal sections to be acquired at exactly the same lung volume. In addition, esophageal pressure was monitored on an oscilloscope by using a balloon-catheter system: 80 cm of polyethylene tubing with an internal diameter of 1.7 mm and distal side holes and a low-compliance 10-cm-long rubber balloon filled with 1 mL of air (17) connected to a linear pressure transducer (MP15 [±50 cm H2O]; Validyne, Northridge, Calif). Only acquisitions performed under satisfactory relaxation conditions according to the esophageal pressure signal were retained for analysis.

Reproducibility.—The complete procedure was repeated twice in two subjects after an interval of several weeks.

Data Analysis
Diaphragmatic anatomy.—The diaphragm is attached to the inferior thoracic aperture as follows (18). The sternal part is attached to the back of the xyphoid process (Fig 1). The costal part is attached to the internal surfaces of the lower six costal cartilages and their adjoining ribs, interdigitating with fibers from the transverse muscle of the abdomen. The lumbar part is fixed to the aponeurotic medial and lateral arcuate ligaments and to some lumbar vertebrae by means of the crura. The lateral arcuate ligament arches across the lumbar quadrate muscle and attaches medially to the front of the first lumbar transverse process and laterally to the inferior edge of the 12th rib. The medial arcuate ligament is a tendinous arch in the fascia that covers the psoas major muscle. Medially, it blends with the lateral tendinous edge of the corresponding crus and is thus attached to the side of the first or second lumbar vertebral body. Laterally, it is attached to the front of the first lumbar transverse process. The crura arises from anterolateral aspects of the bodies and intervertebral discs of the upper three and two lumbar vertebrae on the right and left, respectively.



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  		Figure 1a. Sketches depict attachment of the diaphragm to the thoracic outlet. (a) On the inner anterior surface of the chest wall, the sternal part (1) is attached to the back of the xyphoid process. The costal part (2) is attached to the internal surfaces of the lower six costal cartilages and their adjoining ribs, interdigitating with fibers from the transverse muscle of the abdomen. (b) On the inner posterior surface of the chest wall, the lumbar part is fixed by the crura to the aponeurotic medial and lateral arcuate ligaments and to several lumbar vertebrae. The lateral arcuate ligament (3) arches across the lumbar quadrate muscle and attaches medially to the front of the first lumbar transverse process (5) and laterally to the inferior edge of the 12th rib (2). The medial arcuate ligament (4) is a tendinous arch in the fascia that covers the psoas major muscle. Medially, it blends with the lateral tendinous border of the corresponding crus and is thus attached to the side of the first or second lumbar vertebral body. Laterally, it is attached to the front of the first lumbar transverse process. The crura spring from anterolateral aspects of the bodies and intervertebral discs of the upper three and two lumbar vertebrae on the right and left, respectively. From this circumferential attachment, fibers converge into a central tendon of constant area (1).

 


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  		Figure 1b. Sketches depict attachment of the diaphragm to the thoracic outlet. (a) On the inner anterior surface of the chest wall, the sternal part (1) is attached to the back of the xyphoid process. The costal part (2) is attached to the internal surfaces of the lower six costal cartilages and their adjoining ribs, interdigitating with fibers from the transverse muscle of the abdomen. (b) On the inner posterior surface of the chest wall, the lumbar part is fixed by the crura to the aponeurotic medial and lateral arcuate ligaments and to several lumbar vertebrae. The lateral arcuate ligament (3) arches across the lumbar quadrate muscle and attaches medially to the front of the first lumbar transverse process (5) and laterally to the inferior edge of the 12th rib (2). The medial arcuate ligament (4) is a tendinous arch in the fascia that covers the psoas major muscle. Medially, it blends with the lateral tendinous border of the corresponding crus and is thus attached to the side of the first or second lumbar vertebral body. Laterally, it is attached to the front of the first lumbar transverse process. The crura spring from anterolateral aspects of the bodies and intervertebral discs of the upper three and two lumbar vertebrae on the right and left, respectively. From this circumferential attachment, fibers converge into a central tendon of constant area (1).

 
From this circumferential attachment, fibers converge to a central tendon of constant area (19). Thus, in our study, to precisely calculate the variation of the area of the muscle portion, the area of the central tendon was subtracted from the area of the whole diaphragm.

Three-dimensional reconstructions of the diaphragm and the chest wall.—Use of a large field of view and contiguous sections enabled sequential identification of anatomic structures such as vertebrae and ribs from section to section. Diaphragmatic points of origin were determined according to anatomic definitions of diaphragmatic attachments to the thoracic outlet. For practical reasons, these anatomic landmarks were determined once at TLC and were then readily recognized on the corresponding sections at FRC or RV. We paid close attention to the modifications due to lung-volume changes, particularly for the anteroposterior movement of the chest wall (Fig 2). Diaphragmatic silhouettes were manually segmented by one observer (P.C.) on a remote console by using a computer mouse; the contour was displayed as a series of dots. During tracing, the dots were displayed on-line by the computer, so that the observer could ensure the consistency of the tracing and the adequacy of sampling. The window and level settings were kept constant.



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  		Figure 2a. Fast gradient-recalled-echo images (6.7/2.2 with flip angle of 30°, section thickness of 10 mm, field of view of 48 cm, 128 x 256 matrix) of the diaphragm and rib cage used to determine diaphragmatic attachments to the thoracic outlet. (a-c) Sagittal images obtained at (a) TLC, (b) FRC, and (c) RV, 7 cm away from the midline. (a) On viewer's right, the first rib is no longer visible, but the subsequent ribs are (thin white arrows), and the large white arrow points to the 12th rib onto which the diaphragm is inserted. On viewer's left, black arrows indicate the lower part of the anterior chest wall, and the white arrow indicates the anterior insertion of the diaphragm onto the internal surfaces of the cartilage and adjoining ribs. Note that the apposition zone is close to zero at TLC. (b, c) Arrowheads indicate the upper limit of the apposition zone. Anatomic landmarks can be identified by paying close attention to the modifications caused by lung-volume variations. Other keys are as in a. (d-f) Coronal images obtained at (d) TLC, (e) FRC, and (f) RV. The 12th rib is no longer visible, and small white arrows indicate the remaining ribs. The large white arrow indicates the diaphragmatic insertion onto the inner surface of the 10th rib. In e and f, the star indicates the upper limit of the apposition zone.

 


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  		Figure 2b. Fast gradient-recalled-echo images (6.7/2.2 with flip angle of 30°, section thickness of 10 mm, field of view of 48 cm, 128 x 256 matrix) of the diaphragm and rib cage used to determine diaphragmatic attachments to the thoracic outlet. (a-c) Sagittal images obtained at (a) TLC, (b) FRC, and (c) RV, 7 cm away from the midline. (a) On viewer's right, the first rib is no longer visible, but the subsequent ribs are (thin white arrows), and the large white arrow points to the 12th rib onto which the diaphragm is inserted. On viewer's left, black arrows indicate the lower part of the anterior chest wall, and the white arrow indicates the anterior insertion of the diaphragm onto the internal surfaces of the cartilage and adjoining ribs. Note that the apposition zone is close to zero at TLC. (b, c) Arrowheads indicate the upper limit of the apposition zone. Anatomic landmarks can be identified by paying close attention to the modifications caused by lung-volume variations. Other keys are as in a. (d-f) Coronal images obtained at (d) TLC, (e) FRC, and (f) RV. The 12th rib is no longer visible, and small white arrows indicate the remaining ribs. The large white arrow indicates the diaphragmatic insertion onto the inner surface of the 10th rib. In e and f, the star indicates the upper limit of the apposition zone.

 


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  		Figure 2c. Fast gradient-recalled-echo images (6.7/2.2 with flip angle of 30°, section thickness of 10 mm, field of view of 48 cm, 128 x 256 matrix) of the diaphragm and rib cage used to determine diaphragmatic attachments to the thoracic outlet. (a-c) Sagittal images obtained at (a) TLC, (b) FRC, and (c) RV, 7 cm away from the midline. (a) On viewer's right, the first rib is no longer visible, but the subsequent ribs are (thin white arrows), and the large white arrow points to the 12th rib onto which the diaphragm is inserted. On viewer's left, black arrows indicate the lower part of the anterior chest wall, and the white arrow indicates the anterior insertion of the diaphragm onto the internal surfaces of the cartilage and adjoining ribs. Note that the apposition zone is close to zero at TLC. (b, c) Arrowheads indicate the upper limit of the apposition zone. Anatomic landmarks can be identified by paying close attention to the modifications caused by lung-volume variations. Other keys are as in a. (d-f) Coronal images obtained at (d) TLC, (e) FRC, and (f) RV. The 12th rib is no longer visible, and small white arrows indicate the remaining ribs. The large white arrow indicates the diaphragmatic insertion onto the inner surface of the 10th rib. In e and f, the star indicates the upper limit of the apposition zone.

 


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  		Figure 2d. Fast gradient-recalled-echo images (6.7/2.2 with flip angle of 30°, section thickness of 10 mm, field of view of 48 cm, 128 x 256 matrix) of the diaphragm and rib cage used to determine diaphragmatic attachments to the thoracic outlet. (a-c) Sagittal images obtained at (a) TLC, (b) FRC, and (c) RV, 7 cm away from the midline. (a) On viewer's right, the first rib is no longer visible, but the subsequent ribs are (thin white arrows), and the large white arrow points to the 12th rib onto which the diaphragm is inserted. On viewer's left, black arrows indicate the lower part of the anterior chest wall, and the white arrow indicates the anterior insertion of the diaphragm onto the internal surfaces of the cartilage and adjoining ribs. Note that the apposition zone is close to zero at TLC. (b, c) Arrowheads indicate the upper limit of the apposition zone. Anatomic landmarks can be identified by paying close attention to the modifications caused by lung-volume variations. Other keys are as in a. (d-f) Coronal images obtained at (d) TLC, (e) FRC, and (f) RV. The 12th rib is no longer visible, and small white arrows indicate the remaining ribs. The large white arrow indicates the diaphragmatic insertion onto the inner surface of the 10th rib. In e and f, the star indicates the upper limit of the apposition zone.

 


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  		Figure 2e. Fast gradient-recalled-echo images (6.7/2.2 with flip angle of 30°, section thickness of 10 mm, field of view of 48 cm, 128 x 256 matrix) of the diaphragm and rib cage used to determine diaphragmatic attachments to the thoracic outlet. (a-c) Sagittal images obtained at (a) TLC, (b) FRC, and (c) RV, 7 cm away from the midline. (a) On viewer's right, the first rib is no longer visible, but the subsequent ribs are (thin white arrows), and the large white arrow points to the 12th rib onto which the diaphragm is inserted. On viewer's left, black arrows indicate the lower part of the anterior chest wall, and the white arrow indicates the anterior insertion of the diaphragm onto the internal surfaces of the cartilage and adjoining ribs. Note that the apposition zone is close to zero at TLC. (b, c) Arrowheads indicate the upper limit of the apposition zone. Anatomic landmarks can be identified by paying close attention to the modifications caused by lung-volume variations. Other keys are as in a. (d-f) Coronal images obtained at (d) TLC, (e) FRC, and (f) RV. The 12th rib is no longer visible, and small white arrows indicate the remaining ribs. The large white arrow indicates the diaphragmatic insertion onto the inner surface of the 10th rib. In e and f, the star indicates the upper limit of the apposition zone.

 


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  		Figure 2f. Fast gradient-recalled-echo images (6.7/2.2 with flip angle of 30°, section thickness of 10 mm, field of view of 48 cm, 128 x 256 matrix) of the diaphragm and rib cage used to determine diaphragmatic attachments to the thoracic outlet. (a-c) Sagittal images obtained at (a) TLC, (b) FRC, and (c) RV, 7 cm away from the midline. (a) On viewer's right, the first rib is no longer visible, but the subsequent ribs are (thin white arrows), and the large white arrow points to the 12th rib onto which the diaphragm is inserted. On viewer's left, black arrows indicate the lower part of the anterior chest wall, and the white arrow indicates the anterior insertion of the diaphragm onto the internal surfaces of the cartilage and adjoining ribs. Note that the apposition zone is close to zero at TLC. (b, c) Arrowheads indicate the upper limit of the apposition zone. Anatomic landmarks can be identified by paying close attention to the modifications caused by lung-volume variations. Other keys are as in a. (d-f) Coronal images obtained at (d) TLC, (e) FRC, and (f) RV. The 12th rib is no longer visible, and small white arrows indicate the remaining ribs. The large white arrow indicates the diaphragmatic insertion onto the inner surface of the 10th rib. In e and f, the star indicates the upper limit of the apposition zone.

 
Diaphragmatic silhouettes were divided into two zones. The first zone, where the diaphragm is roughly horizontal and apposed to the lung above and the abdominal contents below, will hereafter be referred to as the "diaphragmatic dome." The second zone, where the diaphragm assumes a roughly vertical direction and through which the rib cage is apposed to the abdominal contents and thus exposed to abdominal pressure, will here after be referred to as the "apposition zone" (Appendix). The dots that corresponded to the upper limits of the apposition zone were determined at the time of digitization. Each set of images of the diaphragm enabled a set of 3D points to be established. Rib cage silhouettes were drawn similarly. Three-dimensional reconstructions were based on the Delaunay triangulation algorithm of object contours (20,21). This algorithm program was implemented by using a workstation (model RS/6000; IBM, Rochester, Minn). Briefly, each pair of dots in a plane is connected to its nearest-neighbor dot in an adjacent plane, thereby obtaining a triangulation. All these small triangles provide a 3D polygonal representation. We interfaced our customized software with a commercial visualization package (VISUALIZATION DATA EXPLORER version 3.1.2; IBM, Yorktown Heights, NY), which was used to render and manipulate the 3D volume.

Calculations.—Diaphragmatic lengths were calculated from digitized diaphragmatic silhouettes in three different planes, one coronal and two sagittal (right and left). These planes were chosen to correspond roughly to the orientations of diaphragmatic fibers, which radiate from the central tendon as observed at gross anatomic examination and described in anatomy textbooks (18,22) (Fig 1). The coronal plane was 10 mm in front of the diaphragmatic canal, and the sagittal planes were placed in the middle of the posterior costal ribs. Along these selected planes, we calculated total diaphragmatic length, length of the apposition zone, and length of the diaphragmatic dome. The length of the apposition zone included the anterior and posterior parts of the apposition zone in the sagittal sections and both the right and left parts of the apposition zone for coronal sections.

Diaphragmatic surface areas were the sum of all the appropriate small triangular surfaces. For each lung volume, we obtained estimates for the total diaphragmatic surface area (Adi), the area of the diaphragmatic dome, and the area of apposition. According to Arora and Rochester (19), central tendon surface area is 143 cm2 ± 25. By using this value, we calculated the muscle surface area (Am) of the diaphragm as follows: Am = Adi - 143.

To calculate the volume of the cavities delimited by the rib cage and the volume under the diaphragmatic dome, the rib cage and diaphragmatic silhouettes were closed by a plane that joined the anterior and posterior diaphragmatic attachments. Volumes were obtained by adding the volumes of tetrahedrons formed by connecting the surface points. The cavity volumes delimited by the rib cage and the volume under the diaphragmatic dome were then calculated for each lung volume (Fig 3). Intrathoracic volume was calculated by subtracting the volume under the diaphragmatic dome from the volume of the cavities delimited by the rib cage. The volume of the mediastinal structures was also calculated. The volume of both lungs was calculated by subtracting the volume of the mediastinal structures from the intrathoracic volume. The calculated volume of both lungs from each reconstruction was compared with the corresponding spirometrically determined lung volumes obtained with the subject in the supine position. The respective contributions of rib-cage and diaphragmatic volume displacements were also calculated from this comparison.



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  		Figure 3. Schematic of computed volumes. The volume of the cavity delimited by the rib cage (Vrc) and a plane that joins the anterior to the posterior diaphragmatic attachment (a-b segment) was calculated for each lung volume. The same process was used to determine the volume under the diaphragm (Vdi). Intrathoracic volume (Vth) was then calculated by subtracting the volume under the diaphragm from the volume of the cavities delimited by the rib cage. The segments a-a' and b-b' represent the apposition zone, which is close to zero at TLC. The red line represents the diaphragmatic dome.

 
Phantom Study
The accuracy of 3D reconstruction was assessed by using a spherical phantom with diameters roughly similar to those of an adult thorax. The acquisition parameters and 3D reconstruction method were the same as those used for in vivo studies. The diameter, length of the equator, surface, and volume of the sphere were calculated and compared with actual values.

Statistical Analyses
The spirometric measurements made before and those after the MR imaging sessions to check lung-volume reproducibility were compared by means of cross-correlation analysis. The effect of changes in lung volume on the various diaphragmatic parameters (lengths and surface areas) were assessed by means of one-way analysis of variance for repeated measures and a protected least square Fisher exact test. The comparison of lung volumes determined by means of MR imaging reconstructions by using our algorithm with the reference spirometric values was made with the graphic approach described by Bland and Altman (23). This method consists of plotting the differences between the measurements yielded with the reference technique—spirometry—and the technique used in this study—MR imaging—against the mean of these two values. From such a plot, it is possible to evaluate to what extent the measurements agree (rather than how they are correlated) and whether there is a relationhsip between the measurement error and the true value. This approach bypasses the numerous biases of regression analysis. The same approach was also used to assess the repeatability of MR imaging measurements (lengths, surface areas, and volumes) over time. Data were expressed as the mean plus or minus 1 SD. The level of significance of differences was set at .05.


   Results
TOP
 Abstract
 Introduction
 Materials and Methods
 Results
Discussion
 Appendix
 References
 
Phantoms
Volumes reconstructed with our 3D reconstruction algorithm agreed well with actual values. True values for the diameter, circumference, surface area, and volume of the sphere were 26.7 cm, 83.8 cm, 2,238 cm2, and 9,961 cm3, respectively, versus the calculated values of 26.2 cm, 83.0 cm, 2,247 cm2, and 9,875 cm3, respectively. This precision suggests that we were able to make the target measurements adequately in our subjects.

Volunteer Examples
Cross-correlation analysis showed that there was no significant difference between the FRC, RV, and TLC values measured in the five subjects on three separate occasions before and after the MR imaging acquisitions. In addition, the inspiratory capacities (TLC – FRC) and expiratory reserves (FRC – RV) monitored during the acquisition did not differ from the values obtained in the pulmonary function laboratory. Thus, the reproducibility of the lung volumes at which images were acquired can be considered satisfactory.

The algorithm visually reconstructed the 3D shape of the diaphragm and rib cage at the three lung volumes. Figure 4 gives examples of the reconstructed traces at TLC, FRC, and RV. Marked changes in the net curvature of the diaphragm with lung volume occur in both the sagittal and coronal planes.



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  		Figure 4a. Left anterolateral 3D reconstruction images of the diaphragm (in green) and rib cage (as dots) at (a) TLC, (b) FRC, and (c) RV. Note the marked changes in diaphragmatic shape that occur in both the sagittal and coronal planes and that the apposition zone is totally absent in a.

 


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  		Figure 4b. Left anterolateral 3D reconstruction images of the diaphragm (in green) and rib cage (as dots) at (a) TLC, (b) FRC, and (c) RV. Note the marked changes in diaphragmatic shape that occur in both the sagittal and coronal planes and that the apposition zone is totally absent in a.

 


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  		Figure 4c. Left anterolateral 3D reconstruction images of the diaphragm (in green) and rib cage (as dots) at (a) TLC, (b) FRC, and (c) RV. Note the marked changes in diaphragmatic shape that occur in both the sagittal and coronal planes and that the apposition zone is totally absent in a.

 
Diaphragmatic Lengths
Table 2 gives the length measurements estimated from selected MR imaging silhouettes. As the lung volume increased, the length of the diaphragm was reduced by 37% in the sagittal plane and by 28% in the coronal plane. At full lung inflation (TLC), the apposition zone disappeared (Fig 2).


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  		TABLE 2. Length Estimates from MR Imaging Silhouettes at Each Lung Volume
 
Diaphragmatic Areas
Changes in the different surface areas observed with vital capacity lung inflation are presented in Table 3. The total diaphragmatic surface area and area of apposition decreased over the vital capacity range by 48% and 100%, respectively, whereas the area of the diaphragmatic dome increased by 37%. The mean total diaphragmatic surface area and mean area of the apposition zone (Aaz) were maximal at RV and minimal at TLC, with TLC minus Aaz "close to zero." Owing to the relatively poor resolution of the technique, a few square millimeters of appositional surface area could not be rigorously eliminated, however irrelevant they might be from a physiologic point of view; therefore, we used the expression "close to zero." The area of the muscle portion decreased by 55% from RV to TLC.


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  		TABLE 3. Diaphragmatic Surface Area Estimates from 3D Reconstruction at Each Lung Volume
 
Rib Cage and Diaphragmatic Volumes
Table 4 reports volume measurements (ie, volume under the diaphragmatic dome, volume of the cavity delimited by the rib cage, intrathoracic volume, volume of the mediastinal structures, and volume of both lungs over the vital capacity range) calculated with our 3D reconstruction algorithm. The differences between lung volumes obtained with spirometric and MR imaging measurements are plotted in Figure 5. MR imaging tended to overestimate lung volume at RV and underestimate lung volume at TLC. Between RV and TLC, the mean volume under the diaphragmatic dome decreased by 66%, and the mean volume of the cavities delimited by the rib cage increased by 23%. The diaphragm contributed to 60% of the inspiratory capacity.


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  		TABLE 4. Diaphragmatic and Rib Cage Volume Estimates from 3D Reconstruction at Each Lung Volume
 


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  		Figure 5. Graph depicts agreement between lung volumes measured with MR imaging and reference technique, spirometry. Each point corresponds to one volume in one subject. The mean of the two measurements (spirometry and MR imaging) is reported on the x axis, and the difference between the two measurements is reported on the y axis. This plot magnifies any differences between the two measurements.

 
Reproducibility
Average lengths, surface areas, and volumes obtained with the first and second series of measurements and their respective differences are plotted in Figure 6a, 6b, and 6c, respectively. Repeatability appears sufficient for the practical purpose of follow-up.



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  		Figure 6a. Graphs depict repeatability of MR imaging measurements of diaphragmatic (a) lengths, (b) surface areas, and (c) volumes. Each data point corresponds to one measurement in one subject, with each measurement made at an interval of several weeks. The mean of the two measurements is reported on the x axis, and the difference between the two measurements is reported on the y axis. This plot magnifies any differences between the two measurements.

 


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  		Figure 6b. Graphs depict repeatability of MR imaging measurements of diaphragmatic (a) lengths, (b) surface areas, and (c) volumes. Each data point corresponds to one measurement in one subject, with each measurement made at an interval of several weeks. The mean of the two measurements is reported on the x axis, and the difference between the two measurements is reported on the y axis. This plot magnifies any differences between the two measurements.

 


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  		Figure 6c. Graphs depict repeatability of MR imaging measurements of diaphragmatic (a) lengths, (b) surface areas, and (c) volumes. Each data point corresponds to one measurement in one subject, with each measurement made at an interval of several weeks. The mean of the two measurements is reported on the x axis, and the difference between the two measurements is reported on the y axis. This plot magnifies any differences between the two measurements.

 

   Discussion
TOP
 Abstract
 Introduction
 Materials and Methods
 Results
 Discussion
Appendix
 References
 
Findings in this study demonstrated that the 3D reconstruction method was precise for determination of a known 3D object, accurate reconstruction of the rib cage and the diaphragm, adequate estimation of the respective volumes that they displaced, and measurement of diaphragmatic functional surfaces. This technique provides a noninvasive tool for simultaneous evaluation of the shape of both the rib-cage and diaphragmatic components of the inspiratory pump.

Comparison with Available Data
Shapes, lengths, and areas.—The diaphragmatic dome has a different shape when viewed from the side or the front. It flattens and tilts as the lung volume increases. We found few other studies that reported the shape of and provided quantitative data for the human diaphragm in vivo.

To our knowledge, Whitelaw (12) was the first to provide a 3D rendition of the diaphragm, which he constructed from serial transverse sections obtained with a CT scanner. Twelve sections were made at 0.5-cm intervals during 12 separatebreath holds. Sections were scanned at relaxed FRC and FRC plus 1 L. The configurations of the rib cage and abdomen were monitored by using magnetometers attached to the thorax and abdomen and were kept constant. Because the CT sections did not include the bottom of the rib cage, the muscle length between the lowest section and the insertion of the diaphragm was estimated on conventional radiographs obtained in the same subject, by assuming that the line of insertion ran from the transverse process of the first lumbar vertebra horizontally to the 12th rib and along the lower border of the rib cage 1 cm above the ends of the ribs. The calculated area of apposition in that study was 385 cm2 at FRC and 161 cm2 at FRC plus 1 L. The contracted diaphragm occupied a thoracic volume 680 mL lower than the relaxed one. No information was provided regarding total diaphragmatic surface areas, length of the diaphragm, or absolute volume under the diaphragm or the rib cage.

Paiva et al (13) studied four healthy men at FRC by using MR imaging. In the spin-echo mode, 11 apneas of 54 seconds (permitted by the administration of supplemental oxygen) allowed the acquisition of 36 sagittal and 30 coronal images. A flexible tube filled with a CuSO4 solution was fixed around the lower costal border of each subject to identify the loci of origin of the costal fibers of the diaphragm. The subsequent study by Gauthier et al (14) reported data on the diaphragm at three lung volumes (Tables 5, 6). Four healthy men were studied in the spin-echo mode with three sets of six sections (30-second data acquisition period each), one in the coronal plane and one in the sagittal plane for each hemidiaphragm. The loci of diaphragmatic insertions onto the rib cage were approximated in the same manner as in the previous study by Paiva et al (13). From the same laboratory, Pettiaux et al (15) developed a technique of diaphragmatic imaging by using spiral CT. They advocated that the long acquisition times of the previous methods were not adequate for the study of patients with chronic obstructive pulmonary disease. These authors studied the same four healthy subjects previously investigated with MR imaging (Table 6). Then, by using this same CT technique, Cassart et al (24) studied the effect of chronic hyperinflation on diaphragmatic length and surface area in patients with chronic obstructive pulmonary disease. Findings in a control group of 10 subjects were also investigated, and the results are summarized in Table 6.


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  		TABLE 5. Diaphragmatic Length Estimates Reported by Different Investigators
 

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  		TABLE 6. Diaphragmatic Surface Area Estimates Reported by Different Investigators
 
In the three previous studies (14,15,24), the shape of the diaphragm changed markedly along the sagittal plane with lung inflation, but there were no major changes in the coronal plane. Compared with findings in our study, this difference was mainly explained by the choice of loci of diaphragmatic insertions. In those studies, the choice of an external costal marker could have resulted in a systematic overestimation of total diaphragmatic length. By using anatomic landmarks, we found that the apposition zone was entirely eliminated at TLC (Fig 2). This finding is not unexpected (25) and agrees well with those in previous studies (12,25,26).

Lengths estimated with our MR imaging technique are in reasonable agreement with those reported in the literature (12–15,24,26–28) (Table 5). Our findings confirm that lung inflation to TLC is associated with an important length reduction of the human diaphragm. MR imaging acquisitions in our study were performed after muscle relaxation against the closed airways; thus, the results pertain to the relaxed muscle after the TLC maneuver contraction. Slight discrepancies could come from the different methods used to measure length. We tried to choose the most appropriate planes according to the directions of diaphragmatic fibers radiating from the central tendon, which are not necessarily correlated with the projected silhouette obtained from posteroanterior or right lateral radiographs of the chest. Our total diaphragmatic length measurements for equivalent planes and lung volumes were systematically smaller than those previously reported (14,15,24), but again the choice of loci of diaphragmatic insertions may explain the differences.

In our study, the average total diaphragmatic surface area value at FRC was 997 cm2 ± 93, which is close to 898 cm2 ± 146, a necropsy estimate reported by Arora and Rochester (19) for healthy humans. Our results also confirm the remarkable shortening of relaxed human diaphragmatic fibers (55% ± 11) over vital capac ity, consistent with the length-tension characteristics of diaphragmatic muscle fibers in vitro (29). Although our results are in reasonably good agreement with the available data (Table 6), the areas that we calculated were systematically smaller than those reported by others (13–15,24). The explanation for these differences is probably methodological. First, in our study, the images were acquired during a single apnea, which minimized errors due to displacements of the rib cage or diaphragm between acquisitions. Second, diaphragmatic attachments were determined by means of an anatomic analysis rather than by combining two different imaging modalities as in the study by Whitelaw (12) or by using an external landmark fixed around the lower costal border to identify the loci of origin of the costal fibers as in other studies (13–15,24). Third, our sections encompassed the entire thorax in one acquisition, which allowed acquisition of more spatial coordinates and increased precision. Therefore, we think our data might be more accurate and closer to reality than those previously published.

Estimation of volume and volume displacements.—The total volumes of the heart and large vessels were 586 mL ± 36, 702 mL ± 98, and 725 mL ± 93 at TLC, FRC, and RV, respectively, and are in agreement with data found in the literature for combined cardiac blood (18) and tissue volume of 680 mL (30). With lung inflation from RV to TLC, the total volume of the heart and large vessels decreased by 20%. This observation is in accordance with findings in the study by Hoffman and Ritman (31), which showed a total heart-volume reduction of 12% ± 0.5 when the lungs were inflated with a pressure of 15 cm H2O.

Investigators who used various indirect techniques to determine diaphragmatic displacement obtained conflicting results (Table 7). According to our method, the volume displaced by the diaphragm as it descends within the thorax (or diaphragmatic volume displacement) over the entire vital capacity represents 59.7% of the inspired volume. Because the volume under the diaphragm can be measured directly with MR imaging, we think that this method produces a more accurate measurement of diaphragmatic volume displacement than do indirect measurements.


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  		TABLE 7. Diaphragmatic Volume Displacement as a Percentage of Inspired Volume in Upright Healthy Subjects
 
Our estimates of lung volumes fit well with the spirometric values (Fig 5) but are not identical. We were careful to check the adequacy of lung volume before each acquisition and to determine lung volumes with spirometry in the supine position. Lung volume measurements obtained with MR imaging take into account the pulmonary blood volume and the lung tissue volume, which could be estimated at 500 mL (30,32) and 600 mL (33,34), respectively. By using these values, calculated values for RV and FRC were 1,745 cm3 ± 458 and 2,718 cm3 ± 964, which are slightly above (300–400 cm3) the expected values, respectively, 1,410 cm3 ± 310 and 2,290 cm3 ± 660 (Tables 1, 4). This discrepancy could be explained by the inclusion of a part of the dead space and pulmonary veins or arteries in the calculated volume. Conversely, calculated values for TLC, 6,036 cm3 ± 1,118, are slightly below the expected value of 6,780 cm3 ± 1,360. Potential explanations for this difference include consumption of oxygen during the period of apnea or the decrease in pulmonary blood volume between FRC and TLC. Also important could be compression of intrathoracic gas because of viscoelastic properties during relaxation against the buccal valve during the acquisition, which leads to a slight decrease in intrathoracic volume.

To our knowledge, few reports describe the use of MR imaging to calculate lung volumes (35,36). In a recent study based on an MR analysis of lung volume and thoracic dimensions in patients with emphysema before and after lung volume-reduction surgery, Gierada et al (37) found a significant correlation (r = 0.77, P < .001) between MR imaging and plethysmographic measurements of inspiratory lung volume, although the former measurements were consistently lower than the latter. No spirometric monitoring was performed during acquisition of images, however, and the lung volumes were determined with plethysmography with the subjects seated, different from their position for MR image acquisition.

Limitations and Perspectives
There are several potential limitations to our method, including the (a) resolution, (b) observer variability, (c) applicability to breathing while standing, (d) rate of image acquisition, and (e) time of reconstruction. As with all cross-sectional imaging techniques, MR imaging is affected by partial volume averaging, which may limit its accuracy for volume determinations. In comparison with previous studies on measurement of cardiac chamber volumes, however, this limitation is acceptable. Observer variability, which was not evaluated in this study, is also a potential cause of error and warrants further study. Difficulties in determining the diaphragmatic attachments and evaluating the contour location of the rib cage or diaphragm could be the two main sources of variability. We are currently working on a semiautomated image-segmentation process to decrease the latter, and a sound knowledge of anatomy should reduce the former. Manual segmentation required an average 21/2–3 hours per patient, but semiautomated image segmentation should reduce the entire process to about 30 minutes. Examination in the supine position is obviously a limitation for a physiologic study. However, open MR imaging should allow investigators to perform similar studies in the upright position, which is not possible with CT. Finally, an excessively long acquisition time (30–33 seconds in our study) may be a study limitation for patients with respiratory insufficiency. Although this breath-hold time remains within the range of capability of adults who are heavy smokers or who have chronic obstructive pulmonary disease (38), we have verified that it can be reduced to 18–20 seconds by using noncontiguous sections (unpublished data). This modification did not result in a relevant loss of accuracy. Use of faster acquisition modes should ensure maintenance of resolution and enable the study of more debilitated patients.

Despite these current limitations, findings in this study demonstrate the feasibility of 3D reconstruction of the inspiratory pump with MR imaging, which can provide accurate measurements of the diaphragmatic functional surfaces and the volumes displaced by the rib cage and the diaphragm. We think that this completely noninvasive technique has the potential to improve structure-function evaluations of chest-wall mechanics and has promising applications in clinical and fundamental research. Thus, a reliable method for measurement of lung volumes with MR imaging has become possible and offers the advantage of being less affected by variations in thoracic shape than are measurements made with conventional chest radiography (39).


   Appendix
TOP
 Abstract
 Introduction
 Materials and Methods
 Results
 Discussion
 Appendix
References
 
The apposition zone, defined as the roughly vertical portion of the diaphragm that separates the lower rib cage from the abdominal contents, is crucial to the inspiratory action of the diaphragm. In summary, when the diaphragm contracts, it shortens and descends, therefore pushing on the contents of the abdominal cavity, which are more or less incompressible in nature. This pushing results in a positive abdominal pressure that is transmitted to the lower part of the rib cage through the apposition zone. In response to this positive abdominal pressure and because of the anatomy of the costovertebral articulations, the ribs move outward and upward; hence, the transverse diameter of the lower thorax and the abdominal circumference increase, which are typical inspiratory phenomena. Simultaneously, a negative pressure is generated in the thorax. If the diaphragm contracts alone, as is the case during phrenic nerve stimulation, the upper rib cage actually deflates because of the negative pleural pressure. It is only because normal inspiration involves the coordinated contraction of upper rib-cage muscles and of the diaphragm that this upper rib-cage paradox is not usually observed.


   Acknowledgments
 
The authors thank the individuals who served as subjects in this study. Christian Straus and Noomen Kanoun helped gather pulmonary function data both during and between MR imaging acquisitions. The authors also thank Janet Jacobson for editing the manuscript for this article.


   Footnotes
 
Abbreviations: FRC = functional residual capacity RV = residual volume TLC = total lung capacity 3D = three-dimensional

Author contributions: Guarantor of integrity of entire study, P.C.; study concepts and design, P.C., T.S.; definition of intellectual content, P.C., T.S., C.C.L., P.A.G.; literature research, P.C., T.S., C.C.L.; clinical studies, all authors; data acquisition, all authors; data analysis, P.C., T.S., C.C.L.; statistical analysis, P.C., T.S.; manuscript preparation and review, P.C., T.S., C.C.L., P.A.G.; manuscript editing, P.C.


   References
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 Introduction
 Materials and Methods
 Results
 Discussion
 Appendix
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