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Published online before print June 20, 2003, 10.1148/radiol.2282011554
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(Radiology 2003;228:389-394.)
© RSNA, 2003

Ultrasonography

Right Hemidiaphragmatic Mobility: Assessment with US Measurement of Craniocaudal Displacement of Left Branches of Portal Vein1

Nair S. G. Toledo, PT, Sérgio K. Kodaira, MD, PhD, Paulo C. B. Massarollo, MD, PhD, Osvaldo I. Pereira, MD, PhD and Sérgio Mies, MD, PhD

1 From the Liver Unit (N.S.G.T., P.C.B.M., O.I.P., S.M.) and Department of Radiology (S.K.K.), University of São Paulo Medical School, Brazil. Received September 19, 2001; revision requested November 26; final revision received November 25, 2002; accepted December 19. Supported by FAPESP grant 99/10418-3. Address correspondence to N.S.G.T., R. Luxemburgo, 113-CEP, 86046-410 Londrina, Brazil (e-mail: tolecosta@hotmail.com).


   ABSTRACT
TOP
 ABSTRACT
INTRODUCTION
 MATERIALS AND METHODS
 RESULTS
 DISCUSSION
 REFERENCES
 
PURPOSE: To evaluate the correlation and agreement between ultrasonographic (US) measurement of craniocaudal displacement of the left intrahepatic branches of the portal vein and radiographic measurement of right hemidiaphragmatic mobility.

MATERIALS AND METHODS: Fifty-one patients with indications for abdominal angiography or percutaneous cholangiography prospectively underwent radiographic evaluation of right hemidiaphragmatic mobility and B-mode US measurement of craniocaudal displacement of the left intrahepatic branches of the portal vein. US was performed by using a 3.5-MHz convex transducer in a right subcostal position with a longitudinal orientation. Statistical analyses were performed by using linear regression, paired Student t test, and Bland-Altman analyses.

RESULTS: The correlation between the US and radiographic measurements was found to be linear: hemidiaphragmatic mobility = (-1.562 + 1.032) x portal vein branch displacement (r = 0.651, P < .001). The mean craniocaudal displacement of the intrahepatic branches of the portal vein measured at US was 35.2 mm ± 10.7 (SD). The mean right hemidiaphragmatic mobility measured at radiography was 34.8 mm ± 17.0. The mean difference between the two measurements was not statistically significant (0.4 mm ± 12.9, P = .807).

CONCLUSION: US measurement of craniocaudal displacement of the left intrahepatic branches of the portal vein can be used for indirect assessment of right hemidiaphragmatic mobility.

© RSNA, 2003

Index terms: Diaphragm, 66.12989, 66.155, 66.91 • Hepatic veins, US, 957.12989 • Liver, US, 761.12989 • Ultrasound (US), physics, 761.12989, 957.12989


   INTRODUCTION
TOP
 ABSTRACT
 INTRODUCTION
MATERIALS AND METHODS
 RESULTS
 DISCUSSION
 REFERENCES
 
Ultrasonography (US) is commonly used to assess diaphragmatic mobility (1–3). US measurement is usually performed in the M mode or B mode. In both cases, the success of this examination depends on adequate visualization of the diaphragmatic dome. Some authors choose an intercostal US probe position below the costophrenic sinus (1,4,5). With use of this position, however, adequate visualization of the diaphragm becomes difficult during deep inspiration owing to lung interposition and the underlying movement of the ribs (5,6). To avoid these limitations, others place the transducer in a subcostal position on the abdomen (7,8). In this position the left hemidiaphragm often cannot be demonstrated because of gas in the intervening stomach or bowel (2,7–9). Evaluation of the right hemidiaphragm benefits from the interposition of the liver (8).

In the subcostal position, one can visualize the right dome by aiming the transducer in a cephalic direction underneath the inferior costal margin (8). Doing this causes the craniocaudal excursion of the muscle to be taken in a direction that is oblique to the angle of incidence of the ultrasound beam, and this impairs the precision of the mobility measurement. To overcome this limitation, we tried to develop an alternative method for assessing right hemidiaphragmatic mobility that involves the use of an angle of incidence of the ultrasound beam that is perpendicular to the craniocaudal axis.

The liver is easily visualized by using abdominal US. The mobility of the liver during breathing is similar to the mobility of the right hemidiaphragm (10–13). Because the viscus is parenchymatous and there is little alteration in its shape during breathing (13), an equal displacement of all intrahepatic structures is expected. Thus, theoretically, the mobility of biliary branches and intrahepatic vessels could be used for the indirect evaluation of right hemidiaphragmatic mobility to overcome the limitations of direct US assessment.

The aim of this study was to evaluate the correlation and agreement between US measurement of craniocaudal displacement of the left intrahepatic branches of the portal vein and radiographic measurement of right hemidiaphragmatic mobility.


   MATERIALS AND METHODS
TOP
 ABSTRACT
 INTRODUCTION
 MATERIALS AND METHODS
RESULTS
 DISCUSSION
 REFERENCES
 
The study protocol was approved by the ethics committee of our institution, and written informed consent was obtained from each patient. Fifty-one patients (28 male patients, 23 female patients; mean age, 46.8 years ± 12.6 [SD]; age range, 15–71 years) with indications for abdominal angiography or percutaneous cholangiography were examined prospectively. The diagnoses received by the patients are listed in Table 1. The 51 radiologic examinations performed in the 51 patients were hepatic arteriography (n = 13), hepatic venography (n = 1), and cholangiography (n = 37). The indications for these examinations are presented in Table 2.


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  		TABLE 1. Diagnoses in 51 Patients

 

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  		TABLE 2. Examinations Performed in 51 Patients

 
US and Radiographic Measurements
Immediately before undergoing the radiologic examinations just described, the patients were evaluated for the craniocaudal excursion of the intrahepatic branches of the portal vein with B-mode US. All US examinations (performed with several different units) were performed with the patient in the supine position and by the same physician (S.K.K.). A 3.5-MHz convex transducer was placed in a right subcostal position with a longitudinal orientation. The transducer was held so as to direct the ultrasound beam perpendicularly to the craniocaudal axis during all phases of respiration.

US examinations of the liver were performed in the sagittal plane, which included the retrohepatic portion of the inferior vena cava (Fig 1). Initially, a branch of the portal vein was identified in the field of view. The left branch was identified in all but two patients; in these two cases the base of the right portal vein branch was evaluated. The position of the portal vein branch was marked with a cursor during forced expiration and forced inspiration, and the craniocaudal displacement of these points (in millimeters) was recorded (Fig 2). Three measurements were recorded for each patient, and the highest value was used for analysis.



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  		Figure 1. Drawings of the scanning plane used for B-mode US measurement of craniocaudal displacement of the left intrahepatic branch of the portal vein (LBPV). The transducer was placed in a right subcostal position with longitudinal orientation. Vertical arrows show the direction of the ultrasound beam. A, Lateral view. The ultrasound beam was directed perpendicularly to the craniocaudal axis during all phases of respiration. B, Transverse view. The liver was scanned in a sagittal plane, which included the retrohepatic portion of the inferior vena cava (IVC). With this angle of incidence, the left branch of the portal vein usually was identified in the field of view.

 


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  		Figure 2. B-mode US measurement of craniocaudal displacement of the left intrahepatic portal vein branch (arrow). The liver was scanned in a sagittal plane, which included the retrohepatic portion of the inferior vena cava. The P cursor marks the initial position of this vessel during forced expiration, and another cursor marks the position of the vessel during forced inspiration. The craniocaudal displacement of these points, measured from cursor to cursor, was recorded in millimeters.

 
Next, the patients were transferred to the interventional radiology unit and placed in a supine position on a radiographic table. A graduated radiographic ruler was placed longitudinally under the right hemithorax, close to the thoracoabdominal transition. The patient was asked to hold his or her breath twice in a forced inspiration. During these breath holds, two radiographs of the center of the right hemithorax were recorded on the same film. The same procedure was used to obtain two radiographs during forced expiration. All radiographic examinations were conducted by a second radiologist (O.I.P.), who was unaware of the results of US.

Radiographs depicting large inspiratory and expiratory diaphragmatic excursions were selected. The two radiographs were carefully overlaid by using the graduation ruler depicted on them. The highest point of the right hemidiaphragmatic dome was identified on the deep-expiration image, and a longitudinal line was traced from this point. The intersection of this line with the diaphragmatic dome was used to define the measurement point on the forced-inspiration image. The diaphragmatic displacement between inspiration and expiration was measured by using a pachymeter (Mitutoyo, Nakatsugawa, Japan) with 0.02-mm precision. The graduation of the ruler between inspiration and expiration, as depicted on the radiograph, was used as a reference to correct the magnification that resulted from the divergence of the x rays. The distance between the two graduation points (on the radiograph depicting the ruler) that corresponded to 10 mm was measured. The corrected value of hemidiaphragmatic mobility was obtained by using the following formula: AM = (MM x 10)/GD, where AM is the actual mobility (in millimeters); MM, the measured mobility (in millimeters); and GD, the ruler graduation distance (in millimeters).

Statistical Analyses
Statistical analyses were performed by using linear regression analysis, the paired Student t test, and the Bland-Altman method for assessment of agreement between two measurement methods (14,15). Sample size was calculated by using a computer program (Sample Power, version 1.0; SPSS, Chicago, Ill) to detect a mean difference of at least 8 mm between the US and radiographic measurements, with an SD of 16 mm (2) and type I and II errors limited to within 5% (ie, {alpha} = ß = .05). Results are expressed as means ± SDs and as 95% confidence limits.


   RESULTS
TOP
 ABSTRACT
 INTRODUCTION
 MATERIALS AND METHODS
 RESULTS
DISCUSSION
 REFERENCES
 
The linear regression curve between the craniocaudal displacement of intrahepatic branches of the portal vein measured with US and the right hemidiaphragmatic mobility measured with radiography is shown in Figure 3. There was a positive linear correlation between the two measurements: hemidiaphragmatic mobility = (-1.562 + 1.032) x portal vein branch displacement (r = 0.651, P < .001). Mean craniocaudal displacement of the portal vein branches was 35.2 mm ± 10.7. Mean right hemidiaphragmatic mobility was 34.8 mm ± 17.0. The mean difference between the two measurements was not statistically significant (0.4 mm ± 12.9, P = .807). The 95% confidence limits for this difference were -3.2 and 3.6 mm.



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  		Figure 3. Linear regression curve between US measurement of craniocaudal displacement of the intrahepatic portal vein branches and radiographic measurement of right hemidiaphragmatic mobility. There was a positive linear correlation between the two measurements: hemidiaphragmatic mobility = (-1.562 + 1.032) x portal vein branch displacement (r = 0.651, P < .001).

 
Differences between the US and radiographic measurements in each patient are plotted against the means in Figure 4. The mean difference between the paired initial and final values of right hemidiaphragmatic mobility was 0.6 mm ± 9.0. Differences between the paired initial and final values of radiographic measurements are plotted against the means in Figure 5. The mean difference between the paired initial and final values of displacement of the intrahepatic branches of the portal vein was 0.6 mm ± 4.8. Differences between the paired initial and final values of US measurements are plotted against the means in Figure 6. The repeatability coefficients for the radiographic and US measurements were 18.1 and 9.6 mm, respectively.



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  		Figure 4. Differences between US and radiographic measurements in each patient plotted against means. The limits of agreement correspond to the top and bottom lines and were calculated by adding and subtracting 2 SDs from the mean difference. These extreme values define the range within which 95% of the differences between the two measurement methods are expected to lie.

 


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  		Figure 5. Differences between repeated radiographic measurements of right hemidiaphragmatic mobility plotted against means. If the initial and final measurements in each case were the same, all points would lie on the line corresponding to the mean difference. However, the points show considerable variation in repeated measurements performed in the same subjects, and this variation indicates poor repeatability.

 


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  		Figure 6. Differences between repeated US measurements of craniocaudal displacement of the intrahepatic portal vein branches plotted against means. The points are closer to the mean difference line compared with the points in Figure 5 and thus indicate better repeatability with the US method.

 

   DISCUSSION
TOP
 ABSTRACT
 INTRODUCTION
 MATERIALS AND METHODS
 RESULTS
 DISCUSSION
REFERENCES
 
US has several advantages over fluoroscopy in the evaluation of diaphragmatic kinetics, including lack of risk from ionizing radiation, equipment portability, and direct quantitative information (4,5). Nevertheless, the precision of US measurements of diaphragmatic craniocaudal movement may be limited owing to difficulty in obtaining an adequate angle of visualization of the diaphragmatic dome.

In the B mode, the craniocaudal movement of the right diaphragmatic dome is observed on longitudinal sections, and, ideally, the transducer should be positioned at an angle of incidence perpendicular to the direction of movement to avoid imprecision. This can be achieved by placing the transducer in an intercostal space below the costophrenic sinus (1,4,5). With use of this angle of incidence, visualization of the right hemidiaphragm is jeopardized during deep inspiration owing to lung interposition and the underlying movement of the ribs (5,6).

There have been several studies (1,4,5) to evaluate the craniocaudal excursion of the posterior part of the diaphragmatic dome instead of the mobility of the central area. Use of this artifice may result in an overestimated measurement because the movement of the posterior part of the dome is up to 40% greater than the movement of the anterior portions (16). To overcome these limitations, the transducer can be placed in the subcostal position on the abdomen and aimed in a cephalic direction underneath the inferior costal margin (8,17). Doing this, however, causes the craniocaudal excursion of the muscle to be taken in a direction oblique to the angle of incidence of the ultrasound beam.

In the M mode, the diaphragm is visualized as an echogenic line that traces a curve corresponding to the amplitude of diaphragmatic displacement in the direction of the angle of incidence of the ultrasound beam. Thus, direct measurement of the craniocaudal excursion of the right diaphragmatic dome in the M mode should be performed by positioning the transducer in this same direction. Because this position is not technically feasible, the US probe is generally placed in a subcostal or intercostal position so that the transducer is aimed in a cephalic direction (1,4,8). In these positions, the measurement corresponds to the anteroposterior movement of the muscle (1,3,18). The correlation between this measurement and the craniocaudal mobility changes as a function of the angle formed by the ultrasound beam and the movement direction (3,18).

Houston et al (1), studying diaphragmatic mobility at M-mode US by using an intercostal transducer position, observed intra- and interobserver variabilities of 24% and 19%, respectively. These authors suggested that this variability may be related to anatomic variations in the curvature of the posterior part of the diaphragm and concluded that the lack of reproducibility limits the application of the method.

Ayoub et al (3) stated that these limitations can be avoided by using a 90° angle of vision with the diaphragm, which can be formed by placing the transducer in a subcostal position. These authors, examining six patients, did not find significant differences between the US measurements obtained with this angle of incidence and the craniocaudal displacement measured with fluoroscopy. Because of the small patient sample size, however, caution in interpreting the results of their study is warranted owing to the probability of a type II error.

To overcome these limitations, we tried to design an alternative method of right hemidiaphragmatic mobility assessment that involves the use of B-mode US with an angle of incidence of the ultrasound beam that was perpendicular to the craniocaudal axis during the entire respiratory cycle, including deep inspiration. Because these conditions are inadequate for visualization of the hemidiaphragmatic dome, we tried to identify another anatomic structure that would satisfy two requirements: being observable at the angle considered ideal and demonstrating movement similar to that of the right hemidiaphragm. The liver was chosen owing to these and some other particular characteristics.

The shape, volume, and location of the liver permit easy observation with abdominal US, even at an angle of incidence perpendicular to the craniocaudal axis. The shape of the liver changes very little during breathing, and this organ is permeated by several vessels and biliary ducts that ramify into segments. These structures have been used as anatomic references for the determination of hepatic mobility with computed tomography (12).

To confirm the assumption that the mobility of biliary-vascular elements can be used for indirect assessment of right hemidiaphragmatic mobility, we decided to compare this method with an established direct measurement technique (14). We did this by evaluating the correlation and agreement between the US measurement of craniocaudal displacement of left intrahepatic branches and the radiographic measurement of right hemidiaphragmatic mobility.

Simple linear regression analysis is a popular approach for comparing measurement methods (19). By using this analysis, we found a significant positive linear correlation between the US and radiographic measurements (r = 0.651, P < .001). The estimated linear regression line was almost perfectly superimposed on the line of equality despite some dispersion of the observed points.

The aim of agreement assessment is to investigate the presence of significant biases between two methods. The presence of a constant bias indicates that the method being tested facilitates measurements that are consistently higher or lower than the reference method measurements (19). In the present study, paired Student t test results did not indicate a significant constant bias.

Even when two methods agree closely on average, as was the case in the present study, the individual differences between the two methods exhibit a variation that may be estimated by adding and subtracting 2 SDs from the mean difference (14,15). These extreme values are called limits of agreement and reflect how much smaller or larger the measurement obtained by using the method being tested can be compared with the measurement obtained by using the standard method in each individual (14,15).

The interpretation of limits of agreement depends on the degree of repeatability of each method. A lack of repeatability, in the sense that there is considerable variation in repeated measurements performed in the same subject, limits the amount of agreement that is possible (14,15). The poor repeatability of one method leads to poor agreement between methods for individuals. When the old (ie, reference) method is more variable, the new (ie, tested) method will not agree with it, even if the new method has better repeatability (14,15). This situation was observed in the present study. The coefficient of repeatability for radiographic measurement was 18.1 mm, which corresponds to twice the SD of the mean difference between the initial and final measurements for each case (14,15). Thus, the difference between two repeated radiographic measurements could have been up to 18.1 mm, which is almost twice the difference observed between two repeated US measurements of portal vein branch mobility (9.6 mm). In essence, it is very likely that this poor repeatability could have caused an "artificial" lack of agreement between the two methods. For this reason, the limits of agreement were not quantified.

We evaluated the craniocaudal displacement of the left branches of the portal vein in most of the US examinations. The left branch of the portal vein is more medial and generally coincides with the mamillary line, and, thus, it is easily visualized in the subcostal area. Despite these advantages, the assessment of this vessel was inadequate in two cases. In one case, visualization of the portal vein branch was precluded by the reduced dimension of the left liver lobe. In the other case, the portal vein branch was observed in the caudal limit of the section plane and extended beyond the field of view during deep inspiration. In both cases, the transducer was moved sidelong and the lower surface of the right portal vein branch was analyzed.

Although the present study was intended for assessment of right hemidiaphragmatic mobility, theoretically one could adapt the described US measurement method for use in the evaluation of the left hemidiaphragm by measuring the displacement of intrasplenic vessels. This alternative approach may be especially interesting because of the greater difficulty in visualizing the left hemidiaphragmatic dome due to intervening gas in the splenic flexure, stomach, and bowel (2,7–9).

Results of the present study lead us to conclude that US measurement of craniocaudal displacement of the left intrahepatic branches of the portal vein can be used for indirect evaluation of right hemidiaphragmatic mobility.


   FOOTNOTES
 
Author contributions: Guarantors of integrity of entire study, N.S.G.T., P.C.B.M.; study concepts and design, all authors; literature research, N.S.G.T., P.C.B.M.; clinical studies, all authors; data acquisition, N.S.G.T., S.K.K., O.I.P.; data analysis/interpretation, all authors; statistical analysis, P.C.B.M.; manuscript preparation and definition of intellectual content, all authors; manuscript editing, N.S.G.T., P.C.B.M.; manuscript revision/review and final version approval, all authors


   REFERENCES
TOP
 ABSTRACT
 INTRODUCTION
 MATERIALS AND METHODS
 RESULTS
 DISCUSSION
 REFERENCES
 

  1. Houston JG, Morris AD, Howie CA, Reid JL, McMillan N. Technical report: quantitative assessment of diaphragmatic movement—a reproducible method using ultrasound. Clin Radiol 1992; 46:405-407.[CrossRef][Medline]
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