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1 Department of Radiology, Children's Hospital, 300 Longwood Ave., Boston, MA
02115.
2 Department of Radiology, Massachusetts General Hospital and Harvard Medical
School, Boston, MA 02114.
Received September 13, 2002;
accepted after revision November 11, 2002.
Address correspondence to G. A. Taylor.
Abstract
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MATERIALS AND METHODS. Proximal femoral perfusion was evaluated in 18 studies of 10 piglet hips with unenhanced power Doppler sonography, enhanced power Doppler sonography with IV contrast agent, and digital angiography, in neutral position, hyperabduction, and after release to neutral position. Enhancement ratios between pixel intensities of power Doppler sonography and enhanced power Doppler images in each position were calculated. Angiograms were analyzed for differences in flow with changes in hip position.
RESULTS. With the piglet in neutral position, power Doppler sonography revealed few vessels in the femoral head. Contrast administration resulted in a temporary marked increase in the visualization of vessels in the femoral head. Quantitative enhanced power Doppler sonography revealed a marked decrease in pixel intensity with abduction (p < 0.001) that was not apparent on unenhanced studies (p = 0.28). The enhancement ratio decreased from 0.45 (mean ± SD, ± 0.26) in neutral position to 0.10 (± 0.21) after abduction; it returned to 0.41 (± 0.14) after release of abduction (p < 0.001 for each comparison). Angiographic studies in hyperabduction revealed a variable level of ischemia.
CONCLUSION. Enhanced power Doppler sonography can be used to visualize the vascular supply to the cartilaginous femoral head in piglets and can detect reversible ischemia induced by hip hyperabduction. These differences correlate with digital angiographic evidence of ischemia.
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MR imaging has been proposed as a modality to evaluate femoral head perfusion [6] and to detect early changes of abduction-related ischemia at a reversible stage [7, 8]. MR imaging may be useful in infants immobilized in spica casts when there is no sonographic window and the risk of avascular necrosis is high, ranging from 20% to 47% [9]. Most infants with developmental dysplasia of the hip however are treated by immobilization with a Pavlik harness when sonographic evaluation is feasible. Although safer, abduction in a Pavlik harness has been associated with avascular necrosis with reported incidences of 2.4%, 5%, 9%, and even 11% [10, 11, 12, 13]. Power Doppler sonography has been advocated to evaluate abduction-related changes of the hip in infants [14].
Unfortunately, visualization of femoral head vascularity with power Doppler sonography is inconsistent and may not provide the detailed information about perfusion necessary to diagnose focal areas of ischemia. Other significant limitations of this technique are that femoral head vascularity is sparse and patient motion often requires diminution in gain and sensitivity to minimize motion artifact.
Enhanced power Doppler sonography has been shown to significantly increase the visualization of blood flow in vascular beds such as the neonatal brain, kidney, and testicle [15]. We have undertaken a study in piglets to explore the feasibility of visualizing cartilaginous femoral head perfusion using enhanced power Doppler sonography, to determine if enhanced power Doppler sonography can detect early reversible ischemia of the capital femoral epiphysis and physis induced by hip hyperabduction in piglets, and to determine whether any detected changes correlate with conventional angiography.
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This study was approved by our institution's animal care and use committee.
Sonographic Evaluation
The contrast agent Imagent (formulation AF0150, Alliance Pharmaceutical,
San Diego, CA) was reconstituted according to the manufacturer's directions. A
dispersion of surfactant-coated perfluorohexane-nitrogen–containing
microbubbles with a median diameter of approximately 5 µm was formed after
reconstitution. Elimination from the blood was accomplished by evaporation
through the lungs [16].
Contrast material was administered at a dose of 0.2 mL/kg. Each dose was
injected IV over a 1- to 2-sec interval. The dose range was determined from
previous experiments with this agent
[15]. At least 15 min elapsed
between injections, and the catheter and stopcock were flushed with saline
using three times the volume of the catheter dead space after each dose to
clear any residual contrast agent from the delivery system.
In five piglets, serial power Doppler images of each femoral head were obtained in the axial and coronal orientations before and after contrast injection using a 7-MHz linear transducer (128 XP10, Acuson, Mountain View, CA). The piglets were examined in neutral position, then during extreme abduction, and after release to neutral position in a manner similar to that of positioning for angiography. Each position required a separate injection of IV contrast material. As a result, each piglet underwent a total of six contrast injections (three for each hip joint examined).
Imaging parameters were set to standardize the dynamic range of the image using the lowest temporal averaging settings. Doppler power settings were set at their highest level (< 500 mW estimated in situ spatial peak temporal average). Nonlinear image pre- and postprocessing (input–output conversion) curves were not used. Color gain was optimized using the method of Rubin et al. [17] to maximize vascular signal and reduce tissue-motion artifacts. All imaging parameters were set and left unchanged throughout the experiment.
Angiography
Direct arteriography of both common iliac arteries, both superficial and
profunda femoris arteries, and their branches was performed using rapid hand
injections of nonionic contrast material (Optiray 320, E. M. Parker,
Wilmington, MA) with the catheter tip at the bifurcation of the aorta.
Anteroposterior images of each hip were obtained in neutral position, during
forced hyperabduction, and after release to neutral position in every piglet
using a 2-cm field of view on a high-resolution digital fluoroscopy unit (XRE,
Littleton, MA). Each piglet underwent six sets of IV contrast injections,
three for each hip joint examined.
The imaging sequence was the same in each animal. Each hip was examined by unenhanced power Doppler sonography in three positions and followed by contrast-enhanced power Doppler sonography in the same three positions. Digital arteriography was always performed after power Doppler sonography and in a similar sequence of positions.
Image Analysis
Sonographic images were electronically captured using a digital image
processing unit (Aegis QV200, Acuson) and saved in an 8-bit TIFF (tagged image
file format) format. Images were then transferred onto a Power Macintosh
computer (Apple, Cupertino, CA) and analyzed using Adobe Photoshop 4.0 (Adobe
Systems, Mountain View, CA). Serial images obtained in each hip position were
saved as separate layers within a Photoshop file. Regions of interest were
drawn over each femoral head. Each region of interest was identified on
unenhanced images and electronically superimposed on subsequent anatomically
registered enhanced images. Thus, the same region of interest size was used
for determining mean pixel intensity in each femoral head so that differences
in intensity reflected changes in mean pixel value and not variations in the
size of the area measured. Number of pixels and mean pixel value for each
region of interest were calculated using the program's histogram function.
Enhancement ratios (ER) over each femoral head were calculated using the
following formula based on the ratio of mean pixel intensities (MPI):
ER = enhanced MPI – unenhanced MPI.
Unenhanced Mean Pixel Intensity
Digital arteriograms for each hip were graded for presence and degree of
vascular obstruction (occlusion or attenuation) of the profunda femoris and
circumflex arteries during forced abduction and again for reconstitution of
flow after release of the hip back to neutral position. Vascular occlusion was
defined as a sharp cutoff of the profunda femoris artery and nonvisualization
of the circumflex arteries. Vascular attenuation was defined as a narrowed
caliber of the profunda femoris and circumflex arteries with diminished
contrast opacification of the circumflex arteries. Image grading was performed
by consensus of three radiologists, who were not blinded to the results of the
power Doppler examinations.
Statistical Analysis
Differences between enhanced and unenhanced mean pixel intensities, and
differences in enhancement ratio with changes in hip position were analyzed
using analysis of variance.
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The differences in mean pixel intensities are shown in bar graph form in Figures 2A, 2B. On unenhanced images, mean pixel intensities were similar in neutral position (mean ± SD, 69.92 ± 21), abduction (72.58 ± 25) and release (71.54 ± 23, p = 0.28). In comparison, mean pixel intensities on enhanced images during forced abduction were significantly lower than those in neutral position (78.96 ± 5 vs 99.49 ± 15, respectively, p < 0.001). The enhancement ratio decreased from 0.45 (± 0.26) in neutral position to 0.10 (± 0.21) after abduction; it returned to 0.41 (± 0.14) after release to neutral position. The difference between enhancement ratios in neutral position and abduction is statistically significant (p < 0.001), as is the difference between enhancement ratios in abduction and release back to neutral position (p < 0.001).
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The apparent decrease in blood flow to the capital femoral epiphysis with forced hyperabduction was also visualized on digital angiography. A variable level of ischemia was seen, ranging from occlusion of the profunda femoris artery (seven hips, Figs. 3A, 3B) to attenuation of flow in the branches of the medial circumflex artery (four hips).
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It would be optimal to have the ability to show preservation of femoral head vascularization and femoral head position while the hip was in an immobilization device. Gray-scale sonography has long been used to show femoral head position in infants wearing the Pavlik harness, and power Doppler sonography has shown some promise as a method to show changes in femoral head vascularity with abduction [14]. However, practical limitations to power Doppler sonography of the infant hip include the inherently sparse femoral head vascularity and the resultant inconsistency of vascular visualization. This limitation is accentuated by infant motion.
Although our study is limited by a small number of experimental animals and the need for repeated IV injections of the sonographic contrast agent, it suggests that enhanced power Doppler sonography allows visualization of more vessels in the cartilaginous femoral head so that changes induced by hip position become more conspicuous. Our data suggest that abduction-induced changes in femoral head vascularity seen with power Doppler sonography were appreciable only with the addition of contrast material. Enhanced power Doppler sonography may be useful in the monitoring of therapy in infants with developmental dysplasia of the hip, specifically in ensuring the presence of flow within the cartilaginous femoral head in hopes of avoiding the late complication of hip avascular necrosis. Additional clinical studies are needed to determine the utility of this technique in infants.
In summary, enhanced power Doppler sonography allows conspicuous visualization of vessels in the cartilaginous femoral head in piglets and can detect reversible ischemia induced by hip hyperabduction. These differences correlate with digital angiographic depiction of attenuation in hip vascularity.
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