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AJR 2000; 174:731-734
© American Roentgen Ray Society


Analysis of Diffusion Changes in Posttraumatic Bone Marrow Using Navigator-Corrected Diffusion Gradients

Robert Ward1, Shelton Caruthers1, Corrie Yablon1, Michael Blake1, Mathew DiMasi1 and Stephen Eustace1,2

1 Department of Radiology, Boston Medical Center, 88 E. Newton St., Boston, MA 02118.
2 Present address: Department of Radiology, Cappagh Orthopedic Hospital, Cappagh, Finglas, Co. Dublin, Ireland.

Received April 5, 1999; accepted after revision August 10, 1999.

 
Address correspondence to S. Eustace.


Abstract
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Abstract
Introduction
Materials and Methods
Results
Discussion
References
 
OBJECTIVE. This study was undertaken to analyze diffusion characteristics of normal and posttraumatic bone marrow.

MATERIALS AND METHODS. Fifty consecutive patients with knee pain underwent both conventional and diffusion-weighted MR imaging (b values, 0-980 sec/mm2). Diffusion maps derived from source data were analyzed on a workstation using region-of-interest techniques. Apparent diffusion values recorded in normal marrow were compared with values recorded in abnormal posttraumatic bone marrow (square centimeters per second).

RESULTS. Normal bone marrow identified in 35 patients showed minimal diffusion, with a mean value of 0.15 x 10-5 cm2/sec. Bone marrow in 15 patients sustaining direct traumatic injury (21 bone bruises) showed markedly increased diffusion, with a mean value of 0.8 x 10-5 cm2/sec (range, 0.4-1.3 cm2/sec).

CONCLUSION. Marrow injury after trauma with trabecular damage allows increased movement or diffusion of interstitial water relative to normal marrow. The magnitude of diffusion change appears to reflect the severity of marrow injury.


Introduction
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Abstract
Introduction
Materials and Methods
Results
Discussion
References
 
Local injury to the marrow with disruption of trabeculae resulting in local hemorrhage and edema after trauma, in the absence of cortical disruption, is termed a bone bruise [1,2,3]. These bruises are usually painful, reflecting traumatic injury to marrow cells, trabecular seams, and neurovascular structures. Similar to a fracture, the area of marrow injury or bone bruise generally heals over a 6-week to 3-month period [4, 5]. In most cases, immobilized by a solid intact cortical frame, bruises resolve despite continued weightbearing. Occasionally, bruises and pain persist, reflecting either initial severe injury, ischemia impairing the healing process (atrophic type of bruise), or repeated trauma and motion imposed by continued weightbearing (hypertrophic type) [1, 4,5,6].

Although bone bruises are readily identified on fat-suppressed images, attempts to gauge severity on the basis of size, shape, and signal intensity are subjective and therefore imprecise [1, 4,5,6]. This study was undertaken to analyze diffusion changes induced in marrow by trauma in an attempt to determine whether a recorded diffusion coefficient derived from the site of injury might provide an objective marker of the severity of injury.


Materials and Methods
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Abstract
Introduction
Materials and Methods
Results
Discussion
References
 
Fifty consecutive patients (40 men and 10 women; 26-68 years old; mean age, 42 years) referred with knee pain within 2 weeks of trauma (range, 12 hr to 2 weeks) were included for study.

Each patient underwent MR imaging of the knee using a dedicated quadrature coil on a 1.5-T (NT Gyroscan, Powertrack 1000; Philips Medical Systems, Shelton, CT).

Conventional imaging included the acquisition of a coronal fat-suppressed sequence (turbo short tau inversion recovery (STIR); TR/TE, 2000/20 msec; inversion time, 16 msec) followed in each case by the acquisition of a coronal T2-weighted (800/14), spin-echo diffusion image. The TR in each image was dictated by heart rate and was 800 msec at a heart rate of 75 beats per min. The recorded TE of 14 msec represents the sampling time after the application of diffusion gradients; in effect, the TE dictating contrast is equal to the sum of the time to apply diffusion gradients and the TE after their application; on average, 144 msec). In each case, images were acquired with a 14-cm field of view and a matrix of 128 x 256 after a single excitation. Diffusion images were acquired with navigator-corrected gradients, gated by a peripheral pulse monitor with b values ranging from 0 to 980 sec/mm2. Diffusion gradients were routinely oriented from superior to inferior when images were acquired in the coronal plane and from left to right in the axial plane (10 patients).

Source data were used to generate apparent diffusion coefficient maps that were subsequently analyzed at a workstation using 50-pixel regions of interest (derived from images with a 14-cm field of view, 256 x 256 matrix). In each case, the fat-suppressed image was analyzed by two experienced observers working by consensus to localize areas of normality or bone bruising before reviewing the diffusion maps.

In each of 35 patients with normal marrow, an average of three diffusion readings from epiphyseal yellow marrow and metaphyseal red marrow were recorded. In patients with heterogeneous metaphyseal red marrow, only regions of uniform red marrow were analyzed.

In a similar way, in the remaining 15 patients with recorded bone bruises, an average of three diffusion readings were recorded from the perceived epicenter of marrow hemorrhage and edema (bone bruising) identified on the fat-suppressed image. A total of 21 bruises were analyzed in the 15 patients.

In five patients with normal marrow and in five patients with detectable marrow hemorrhage and edema or bone bruising, additional diffusion imaging was performed in the axial plane.


Results
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Abstract
Introduction
Materials and Methods
Results
Discussion
References
 
Normal bone marrow identified in 35 patients showed minimal diffusion, with a mean value of 0.15 x 10-5 cm2/sec (range, 0.1-0.25 x 10-5 cm2/sec). Abnormal bone marrow in 15 patients with 21 bruises showed markedly increased diffusion, with a mean value of 0.8 x 10-5 cm2/sec (range, 0.4-1.3 x 10-5 cm2/sec).

In normal marrow, apparent diffusion was greater in red (mean, 0.2 x 10-5 cm2/sec) than yellow (mean, 0.1 x 10-5 cm2/sec) marrow; and in five patients in whom diffusion scans were acquired in two planes, the recorded diffusion coefficients were minimally increased in the coronal plane (anisotropic diffusion).

In 21 regions of marrow with detectable hemorrhage and edema (termed a bone bruise) on the fat-suppressed coronal image, the apparent diffusion was considerably greater than that recorded in normal marrow (0.1 versus 0.8 x 10-5 cm2/sec). In five patients in whom axial and coronal diffusion imaging was performed, the apparent diffusion was identical in both planes (bidirectional).

No correlation was observed between the size or signal intensity of the bone bruise on the fat-suppressed image and the observed magnitude of recorded diffusion (Fig. 1A,1B).



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Fig. 1A. —25-year-old man with rotational torque injury. Coronal short tau inversion recovery image (inversion time, 160; TR/TEeff, 2000/20) shows globular bone bruise (arrow) of lateral tibial plateau.

 


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Fig. 1B. —25-year-old man with rotational torque injury. Coronal apparent diffusion coefficient map shows minimal localized increase in diffusion (arrow) (apparent diffusion coefficient = 0.5 x 10-5 cm2/sec) at site corresponding to epicenter of bruise.

 

In each case, correlation was observed between the size and configuration of the bone bruise (itself dictated by mechanism of injury) and the area over which an alteration (not magnitude) in diffusion was recorded (Fig. 2A,2B).



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Fig. 2A. —28-year-old man with rotational torque injury and nondisplaced anterior cruciate ligament avulsion from intercondylar notch, Coronal short tau inversion recovery image (inversion time, 160; TR/TEeff, 2000/20) shows focal marrow edema (arrow) oriented perpendicular to axis of stress at site of avulsion.

 


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Fig. 2B. —28-year-old man with rotational torque injury and nondisplaced anterior cruciate ligament avulsion from intercondylar notch, Coronal apparent diffusion coefficient map shows marked localized increase (arrow) in diffusion (apparent diffusion coefficient = 1.2 x 10-5 cm2/sec) perpendicular to axis of stress at site of avulsion.

 

Markedly increased diffusion was recorded in two patients (apparent diffusion, 1.25 and 1.3 x 10-5 cm2/sec) in whom marrow injury was accompanied by disruption of cortex (fracture) and hence a gross alteration in morphology (Fig. 3A,3B,3C). These results are tabulated in Table 1.



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Fig. 3A. —42-year-old man after rotational torque injury with anterior cruciate ligament tear. Coronal short tau inversion recovery image (inversion time, 160; TR/TEeff, 2000/20) shows globular poorly marginated bone bruise of posterolateral tibial plateau with associated marginal depression fracture (arrow).

 


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Fig. 3B. —42-year-old man after rotational torque injury with anterior cruciate ligament tear. Sagittal fast spin-echo proton density-weighted image (2000/20) shows compression fracture of posterolateral tibial plateau (arrow). No contrecoup bruise or injury is identified in mid lateral femoral condyle because imposed forces are decompressed by fracture at posterolateral margin of tibial plateau.

 


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Fig. 3C. —42-year-old man after rotational torque injury with anterior cruciate ligament tear. Coronal apparent diffusion coefficient map shows diffuse markedly increased diffusion (apparent diffusion coefficient = 1.3 x 10-5 cm2/sec) at site of compression fracture and bruising (arrow and arrowheads).

 

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TABLE 1 Comparison of Apparent Diffusion Coefficient (ADC) and Direction of Diffusion in Bone Marrow and in Cerebral Spinal Fluid

 


Discussion
Top
Abstract
Introduction
Materials and Methods
Results
Discussion
References
 
Diffusion imaging is an MR imaging technique that allows noninvasive examination of tissue structure at a molecular level [7]. By applying equal and opposite gradients on either side of a refocusing lobe in a standard pulse sequence, diffusion sequences identify subtle interstitial movement of water (Fig. 1A,1B). In the absence of motion, tissue that is initially dephased becomes rephased by an applied equal and opposite gradient. In contrast, in the presence of motion, protons in tissue that is initially dephased do not become rephased by the equal and opposite gradient. The amount of recorded signal loss resulting from movement between the gradients is used as a marker of cellular diffusion or interstitial movement of water and allows indirect evaluation of tissue structure. Sensitivity of the sequence to movement is enhanced by increasing the time between the diffusion gradients, by increasing gradient strength, and by increasing the T2 weighting of the sequence at the expense of image signal.

Relying on the application of equal and opposite gradients, diffusion techniques are readily disturbed by macroscopic motion, a fact accounting for early application of the technique to evaluate stationary body parts such as the brain and spine [8, 9] and accounting for a few previously recorded reports of its use to examine the chest, abdomen, and extremities [10, 11].

The development of navigator-corrected, peripheral pulse-monitored diffusion gradients (NT Gyroscan; Philips Medical Systems) that compensate for or minimize the impact of macroscopic motion and pulsation now allow the application of diffusion techniques to the torso and extremities, even using standard gradients and imaging hardware, as in this study.

The results of this study suggest that, in health, minimal diffusion occurs in both red and yellow marrow, and that when diffusion is detected, it appears to be directional, oriented to the long axis of internal trabeculae.

After direct trauma to bone that results in injury to marrow cells, trabeculae, and neurovascular bundles [1,2,3], MR imaging routinely allows the detection of an increase in local fluid concentration, which is manifest as a signal alteration at the sites of injury [12,13,14,15]. It is therefore not surprising that diffusion-weighted scans of affected patients in this study revealed an increase in local motion of water in the regions of injury. Assuming that injury disrupts trabeculae, it is not surprising that recorded diffusion scans showed a local increase in water movement, not only in the coronal plane but also in the axial plane.

Because they reflect the mechanism of injury, impaction injuries produce extensive poorly marginated bone marrow edema with a globular configuration, shear injuries produce oblique linear edema resulting from local disruption to trabeculae, and distraction forces produce focal edema that is linear and perpendicular to the long axis of stress [1, 13, 15,16,17,18,19,20,21,22,23]. In a similar way, diffusion changes after impact injury tend to be diffuse, with a wide transition from increased diffusion at the epicenter of the injury to relatively normal values at the periphery of the documented bruise. Diffusion changes in shear injury tend to be oblique and localized to the axis of stress, whereas changes resulting from distraction forces tend to be focal, linear, and oriented perpendicular to the axis of stress.

Although marrow bruises are readily identified on fat-suppressed sequences [12,13,14,15], the results of this study in a small group of patients showed no correlation between the size of the bruise and the recorded local increase in apparent diffusion. In effect, in two patients, impact injury produced diffuse poorly marginated bruises, with relatively little apparent diffusion change. In contrast, avulsion injuries produced localized bone bruises with markedly increased local diffusion. Such a result emphasizes the need for an objective method to determine the severity of injury.

In this study, dramatically increased diffusion was identified in two patients in whom marrow injury was accompanied by cortical disruption and altered morphology. In both patients, the presence of a fracture appeared to reflect a more severe initial injury. In such a way, diffusion values appear to be a marker of the severity of the initial injury.

There are limitations to this study, which include the small study population, the lack of clinical correlation and follow-up, and, above all, the lack of histologic correlation. Accepting these limitations, this study clearly shows that increased diffusion occurs in areas of marrow after direct localized injury with trabecular disruption. The recorded pattern of diffusion change appears to mirror the mechanism and severity of the injury. Further study is required to determine whether recorded diffusion change might be used to predict ultimate temporal resolution of the bone marrow injury. Similarly, further study is required to explore whether a recorded diffusion value might be used to triage patients into those who should and those who should not be immobilized, and into those who should and those who should not undertake a non—weight-bearing regimen to promote healing.


References
Top
Abstract
Introduction
Materials and Methods
Results
Discussion
References
 

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