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  • 8/14/2019 Optimized Noninvasive Monitoring of Thermal Changes on Digital B-Mode Renal Sonography During Revasculariza

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    Optimized Noninvasive Monitoring ofThermal Changes on Digital B-ModeRenal Sonography DuringRevascularization Therapy

    Objective. Noninvasive real-time thermal change monitoring of human internal organs can play a crit-

    ical role in diagnosis and treatment of many disorders, including reperfusion of renal arteries during

    anticoagulation therapy. Methods. This article focuses on tissue temperature detection using ultra-

    sound velocity changes in different structures and their related speckle shift from their primary loca-

    tions on high-quality B-mode digital sonography. We evaluated different speckle-tracking techniques

    and optimized them using appropriate motion estimation methods to determine the best algorithm

    and parameters. Results. Performing thermal detection methods on simulated phantoms showed a

    good correlation between speckle shifts and the ground truth temperature. For the simulated images,

    average thermal error was 0.5C with an SD of 0.5C, where lower errors can be obtained in noiseless

    (motionless) data. The proposed technique was evaluated on real in vivo cases during surgical occlu-

    sion and reopening of the renal segmental artery and showed the potential of the algorithm for obser-

    vation of internal organ changes using only digital ultrasound systems for diagnosis and therapy.

    Conclusions. The adaptive Rood pattern search proved to be the best block-matching technique,

    whereas the multiresolution Horn-Schunck technique was the best gradient optical flow method. The

    extracted thermal change during in vivo revascularization therapy is promising. In addition, we present

    an evaluation of several block-matching and optical flow motion estimation techniques. Key words:

    block matching; optical flow; reperfusion therapy; speckle tracking; ultrasound thermometry.

    Received February 4, 2009, from the Department ofBiomedical Engineering, Tehran University ofMedical Sciences, Tehran, Iran (M.D.A.); Departmentof Electrical and Computer Engineering, Universityof Louisville, Louisville, Kentucky USA (V.T.); andScience and Research Branch, Islamic AzadUniversity, Tehran, Iran (N.S.). Revision requested

    March 16, 2009. Revised manuscript accepted forpublication April 21, 2009.

    We thank Ali Najafian and Hossein Jandaghi forassistance with animal surgery and sonographicimage acquisition and Ehsan Mohammadi for

    preparing agar gel phantoms. This work was sup-ported in part by the Research Center for Scienceand Technology in Medicine, Tehran University ofMedical Sciences.

    Address correspondence to Vahid Tavakoli, MD,MS, Department of Electrical and ComputerEngineering, University of Louisville, Medical ImageComputing Laboratory, Lutz Hall, Room 308,Louisville, KY 40292 USA.

    E-mail: [email protected]

    AbbreviationsARPS, adaptive Rood pattern search; ES, exhaustive search;4SS, 4-step search; MAD, mean absolute difference; MSE,mean square error; PSF, point spread function; ROI, regionof interest; 3SS, 3-step search; 2D, 2-dimensional

    Tissue Temperature Detection

    Thermal changes in different parts of the human body

    are directly related to the physiologic characteristics and

    functions of the organs. The main supplier of the heat for

    any organ is blood flow, and any disturbance in tissue

    perfusion can be shown as a temperature gradient. Also,

    many nonvascular disorders such as inflammations and

    abscess formation are related to the changes in tempera-

    ture. Therefore, superficial or mucosal thermal detection

    (ordinary thermometer) is a major part of any physicalexamination in any clinic.1 However, for a deeper tem-

    perature measurement, there is a lack of a standard tech-

    nique. Moreover, ordinary electronic sensors (infrared

    detectors and thermistors) are restricted to local use in

    specific parts, are implanted, and are also invasive. In this

    article, we introduce a novel method for assessing ther-

    mal changes using speckle shifts on high-quality B-mode

    sonography. This technique is not only noninvasive but

    also real time and easily performable on an entire organ

    even in 3-dimensional views.2

    2009 by the American Institute of Ultrasound in Medicine J Ultrasound Med 2009; 28:15351547 0278-4297/09/$3.50

    Technical Advance

    Author: Please give degrees for names mentioned in acknowledgments.

    Mohammad D. Abolhassani, PhD, Vahid Tavakoli, MD, MS, Nima Sahba, MS

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    The proposed technique is used to observe the

    thermal changes during renal revascularization

    therapy because revascularization (opening an

    occluded artery) redirects the blood flow to the

    tissue and elevates the temperature.

    Thermal Detection Using Sonography

    Use of laser and radio frequency knives, which

    are based on thermal-controlling applications,

    requires accurate thermal detection. Treatment

    monitoring consists of real-time tissue damage

    monitoring and real-time temperature estima-

    tion.3,4Regarding ultrasound thermometry, different

    methods have been proposed so far, such as analysis

    of the frequency-dependent attenuation,5 speed

    of sound, thermal expansion,69 and back-scattered

    power.10 One novel technique is ultrasound-simulated acoustic emission, which was shown

    to be temperature dependent.11 Konofagou et al12

    used ultrasound-simulated acoustic emission in

    detection and monitoring of thermal lesion for-

    mation and thermal therapy.13,14

    For many materials, the ultrasound velocity is

    dependent on the temperature. The estimations

    of the temperature variations are obtained by

    calculating the axial displacement of the scatter-

    ers due to tissue warm-up. The displacements

    are caused primarily by the changes of the speed

    of sound in the tissue when the temperature

    changes. The second reason for the changes of

    the signals is the thermal expansion of tissue. The

    dependency of the speed of sound on the tem-

    perature introduces apparent or virtual shifts in

    the scatterer positions, and the thermal expan-

    sion of the medium introduces physical shifts in

    the scatterer positions. The variation of the speed

    of sound with respect to the temperature is for-

    mulated as Equation 1:

    (1)

    Where c is the ultrasound velocity; T is the

    temperature at distance x; c0

    (x) = c(x, T0); and

    is the coefficient of speed change

    with regard to temperature. Moreover,

    (2)

    where is a medium-dependent

    parameter; is linear coefficient of thermal

    expansion; and dis the displacement.

    Details of the formulation have been describedpreviously. In a novel method, Abolhassani et al2

    proved the correlation between the temperature

    estimation and the thermal speckle shifts on

    high-quality B-mode digital sonography in tissue-

    mimicking phantoms through which a heater

    electrode and an array of thermistors were

    inserted. The average error of their study was

    0.2C; the maximum error was 0.53C; and the SD

    was 0.53C.

    Speckle-Tracking Methods

    To date, there have been many methods ofspeckle tracking between 2 ultrasound images.

    Block matching is one of them, which focuses on

    the gray scale similarity between 2 sliding blocks

    of an image. There are many methods of observ-

    ing the similarity between 2 blocks; for instance,

    the mean absolute difference (MAD), mean

    square error (MSE), maximum likelihood, and

    entropy maximization. Moreover, there are sev-

    eral approaches to using these block-matching

    techniques. An old and famous one is exhaustive

    block matching, but its time consumption has

    led to newer methods with comparable results,

    such as the 3-step search (3SS), 4-step search

    (4SS), cross-diamond search, adaptive Rood pat-

    tern search (ARPS), and simple and efficient

    algorithms. These techniques have been dis-

    cussed in detail previously.1523

    Another group of motion estimation methods,

    introduced in 1981, was the gradient optical flow

    methods such as Lucas-Kanade (which pre-

    sumes intensity constancy between the consec-

    utive frames) and Horn-Schunck (a velocity

    constancy assumption is added to the previousmethod). Many other optimizations have been

    performed on these techniques, such as phase

    matching, discrete cosine transform preprocess-

    ing, uniform or gaussian prefiltering, invariant

    moment implementation, histogram equaliza-

    tion, a multiresolution approach (Suhling-Unser

    strategy), and new iterations or warping flow

    charts.2325

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    Moment Implementation and Multiresolution

    Strategy

    During motion, pixels of an image not only

    translate but also shear and rotate. Based on this

    fact, many motion estimation methods makeuse of moments (Zernike or spline) to achieve a

    high degree of invariance and robustness to

    shear and noise.2628

    On the other hand, moment implementation is

    not the whole story. In each frame, pixels have

    different motion vectors in each region; ie, each

    region of an image translates, rotates, or shears

    into different sizes. To overcome this problem, we

    proposed a multiresolution strategy inspired by

    the Suhling-Unser multiresolution method.29,30

    In the Suhling-Unser technique, coarse kernels

    are obtained on the whole image, and then finerkernels are implemented until a certain amount

    of error is satisfied. It means that areas of large

    motion are computed using coarser windows,

    and areas of fine motions are computed using

    small moments. Using this technique, we can

    capture smaller regions of motion that would be

    invisible to a large-kernel method.

    From Speckle Tracking to Thermal Change

    Detection

    Equations 1 and 2 relate the speckle displace-

    ment to the thermal change. Each speckle shift

    shows its own thermal shift in addition to the

    thermal shift of the proximal speckles (with

    respect to the probe). Therefore, there is an accu-

    mulation effect in the thermal speckle shift on

    B-mode ultrasound images.

    To recover the thermal change of each speckle,

    it has been proven that vertical displacement

    derivation is necessary. The derivation step can

    enhance the noise, and it is crucial to preserve

    the robustness of the proposed method. Some

    articles have discussed the noise sensitivity ofthe thermal change detection during the vertical

    derivation and showed that an order statistics fil-

    ter can extract the thermal changes from the

    speckle displacements.31

    Handling Motion Artifacts in the z-Axis

    Several studies have shown that the optical

    flowbased methods can handle large motion arti-

    facts in the z-axis. Several studies extracted motion

    vectors on 2-dimensional (2D) B-mode echocar-

    diographic images from the 3-dimensional heart

    motion.3234As will be discussed later, this error is

    called an out-of-plane error and can be overcome

    using temporal windowing and confidence mea-

    surement.

    Materials and Methods

    In this section, we present different motion esti-

    mation techniques that were used in this project.

    Several methods were implemented and opti-

    mized using different parameters. The algo-

    rithms were evaluated on the simulated thermal

    change in the simulated tissue to evaluate their

    effectiveness and performances.

    Motion Estimation Methods for Speckle TrackingThere are many different methods for extracting

    motion between different images, such as block-

    matching techniques, gradient-based methods

    (optical flow), and feature correlation. Figure 1

    illustrates different types of motion estimation

    methods.

    The block-matching methods try to find a sim-

    ilar block in 2 frames. Optical flow is inspired by

    the block-matching method, whereas both of

    them assume intensity constancy in a region or

    between several pixels. Nevertheless, optical flow

    algorithms use advanced variational calculus

    techniques that make them very fast. The feature

    matching and correlation techniques extract 2

    similar features in 2 frames. These techniques

    suffer from loss of features, finding good features

    to track, and providing dense motion fields.

    However, the optical flow techniques are very

    fast, but their sensitivities to noise can induce

    inaccurate results.

    The best approach to find an efficient motion

    estimation technique is the implementation of

    different methods on simulated or real images.The simulated images provide us with accurate

    measurements, whereas it is usually very difficult

    to obtain accurate and dense results from the

    real sequences.

    To find out an optimal technique for ultra-

    sound thermal detection, we implemented dif-

    ferent algorithms on the simulated ultrasound

    images and then validated the results on the real

    ones. Figure 1 shows different types of motion

    estimation techniques.

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    Abolhassani et al

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    There are several major differences between

    echocardiographic series and camera sequences.

    Camera movies primarily suffer from occlusion

    and aperture and transparency problems. On the

    other hand, echocardiographic series mainly sufferfrom an out-of-plane error, a low signal to noise ratio,

    and violation of the Nyquist theorem in the spa-

    tiotemporal dimension. Echocardiographic motion

    estimation is especially dependent on spatiotem-

    poral aliasing and an out-of-plane error; there-

    fore, higher frame rates can dramatically increases

    the accuracy.

    Block-Matching Algorithms

    The main idea toward this type of motion esti-

    mation is the fact that each block of a frame

    moves toward a similar block in another frame ifthe time interval is small enough. The general

    strategy is to move a microblock over the other

    blocks and compute the most similar blocks. To

    find the best block matching, it is necessary to

    have a similarity-matching function called the

    cost function, through which similarity between

    consecutive images is extracted. There are sever-

    al famous block-matching algorithms including

    the MAD and MSE:

    (3)

    (4)

    whereNis the size of the macroblock, and Cand

    R define pixel shifting.

    Exhaustive Search Method (Full Search Method)

    This method computes the cost function of any

    block of the macroblock (area in which we arelooking for a smaller block). This is a very time-

    consuming but an exact method.

    Another variation is the cross-correlation

    method. In this algorithm, 1 block of the image

    slides over the next image, and the most corre-

    lated block to the primary block is considered

    a matched block with which motion can be

    estimated:

    (5)

    The maximum peak of c(m, n) indicates the

    speckle displacement, where SP1

    and SP2

    are the

    sliding microblock and macroblock, respectively.

    The usual correlation methods are computation-

    ally expensive, and this problem has led to manyoptimizations in this area, such as gradient

    descent-based approaches.

    Other Variations of Block Matching

    To cope with the computational expense of the

    exhaustive search (ES), several searching strategies

    are proposed, such as the 3SS, 4SS, simple and effi-

    cient search, new 3SS, diamond search, and ARPS.

    Gradient-Based (Optical Flow) Methods

    Horn-SchunckThe general differential formulation of the opti-

    cal flow computation assumes that the intensity

    of a particular point in a moving pattern does not

    change with time.6 This constant intensity

    assumption is written as

    (6)

    where E is the pixel intensity with the gradient

    toward the spatial and temporal dimension, and

    is a weighting parameter.23

    Locally Constant Motion (Lucas-Kanade)

    As an alternative to the brightness constancy

    model in Equation 6, the Lucas-Kanade method

    (Equation 7) proposed to solve the problem on

    small local windows where the motion vector is

    assumed to be constant. We ought to minimize

    this equation:

    (7)

    where Eis the pixel intensity, and Wis a weight-

    ed vector.

    Results will be

    ATW2AV = ATW2b ,

    where W = diagonal [W(x1),...,W(x

    n)]; b = (E

    t

    (x1),...,(Et (xn)); and u and vare our motion vec-

    tors inxandydirections.25

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    Multiresolution Approach

    Primarily coarse kernels are obtained on the

    whole image, and then finer kernels are imple-

    mented until a certain amount of error is satis-

    fied. Therefore, large motions are computedusing coarse windows, and fine motions are com-

    puted using small moments. Multiresolution

    moment implementation for ultrasound images

    has been discussed in detail previously.2630

    Motion Extraction in Simulated Data

    Renal tissue movement consists of 2 major sub-

    group motions: (1) motion artifacts due to respi-

    ration and patient displacement and (2) thermal

    speckle shift. The steps resulting to the thermal

    estimation are shown in Figures 2 and 3.

    It is obvious that for accurate motion estima-tion, we ought to remove the first group, which

    is more prominent and destructive. B-mode

    sonography has a periodic nature because of res-

    piratory motion; therefore, noise removal is cru-

    cial for obtaining a motionless frame. The

    following steps are implemented to extract the

    thermal change motion:

    1. Region of interest (ROI) where renal tissue is

    extracted. The pixels in this area define the renal

    tissue, but those outside the ROI pertain to

    abdominal organs.

    2. Region of interest neighborhood motion esti-

    mation. The motion vectors around the ROI area

    are extracted, and on the basis of these vectors,

    the interpolation is performed in the ROI using a

    cubic B-spline to approximate the pure ROI

    motion artifact vectors.

    3. Warping strategy. The fact that there are

    always some degrees of motion in the proximity

    of renal tissue, even in carefully fixed frames,

    necessitates ROI adjustment. Note that we have

    a combination of the motion artifact and the

    thermal speckle shift inside the renal tissue.A motion interpolation step using cubic B-spline

    interpolation (called Ispline) was implemented

    in the previous step with the neighboring renal

    pixels (ROI) to extract the motion artifact in the

    ROI. After that, the motion artifact vectors adjust

    the primary image pixel shifting after a simple

    subtraction.

    4. After the ROI adjustment, the motion estima-

    tion is performed in the ROI. Many speckle-

    tracking techniques were implemented on

    images to evaluate their efficacy and time con-

    sumption in favor of the novel optimized tech-

    nique. Shifts in B-mode frames show thermal

    velocity changes if motion artifacts are desirably

    removed. We implemented block-matchingmethods (3SS, 4SS, cross-diamond search, sim-

    ple and efficient search, and ES using the MSE

    and MAD) and gradient-based optical flow

    methods (Lucas-Kanade, Horn-Schunck, and

    iterative Lucas-Kanade with different numbers

    of iteration). These methods were performed

    using Zernike and spline moments to observe

    the accuracy of different sizes, orders, and types.

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    Abolhassani et al

    Figure 1. Different types of motion estimation techniques.

    Figure 2. Schema of thermal extraction steps.

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    Transformation From the Speckle Shift to the

    Thermal Change

    According to Equation 2, knowing k, the medium

    dependent parameter, which can be obtained

    experimentally for different tissues, and the pixel

    displacement, we can estimate the local temper-

    ature change.

    Renal B-Mode Sonographic Simulation

    We simulated abdominal sonography in the renal

    tissue region regarding the gaussian speckle archi-

    tecture and randomness. Also, we added respira-

    tory motion with respect to the diaphragmatic

    motion, modeled as a sinusoidal expansion and

    contraction of the abdomen with varying frequen-

    cies from 14 to 22 per minute, as in the normal

    human body. A small part of these images had

    very small changes to simulate thermal speckle

    shifts, and the amounts of their speckle shifts were

    proportional to k, the renal pixel displacement

    coefficient, and other equations and coefficients

    that were analyzed in the previous sections. The

    amounts of the speckle shifts were tuned from 0

    to 15 pixels, which were in correlation to the

    amounts of thermal changes during the vascular

    occlusion and revascularization (from 0C to

    20C). The model presumes that the system form-

    ing the image has a linear and space invariant

    point spread function (PSF). If the biological tissue

    is modeled by a continuous distribution of pointscatterers, whose impulse response is T(x,y), then

    the radio frequency image I(x,y) can be obtained

    by spatial convolution of them:

    (8) I(x, y) = PSF(x, y) T(x, y).

    By performing a spatial Hilbert transformation,

    the final image was obtained as the envelope of

    the radio frequency image I(x, y). In particular,

    the PSF has been defined in terms of the acoustic

    wavelength, , and the axial and lateral resolu-

    tion of the imaging system by

    (9)

    We inserted a transducer frequency of 4 MHz,

    sound velocity of 1540 m/s, wavelength of

    0.385 mm, spatial frequency of sound of 5.195

    cycles/mm, SD along the x- and y-axes of

    0.426 mm, SD along the z-axis of 0.213 mm, x-

    and y-axis range of 5 to 5 mm, and z-axis range

    0 to 5 mm. The pattern was added to a mobile cir-

    cular or multichamber cardiac model. A detailed

    description of the B-mode ultrasound modeling

    was published previously.24

    Thermoacoustic Lens Effect

    The ultrasound beam traversing the heated

    region deviates as the thermal change alters its

    velocity. The steep temperature gradient can

    worsen this effect, which is usually negligible.

    This phenomenon results in a regional ripple dis-

    tal to the heated region. There are software and

    hardware methods to reduce it; the former,

    which is in our interest, is 2D spatial filtering. A

    time-varying 2D gaussian filter as described

    below will be used for postprocessing the ther-

    mal change data:

    (10)

    where k= K/C, and n is the order of the filter.8

    Converting Speckle Displacements to Thermal

    Changes

    Because the motion of each speckle is an accu-

    mulated motion, the vertical motion vector is

    derived once. Moreover, because derivationmakes the algorithm noise sensitive, we imple-

    mented an order statistic filter of size 20, as

    described previously.31,32According to Equations

    1 and 2, displacements are converted to a thermal

    shift. Finally, a gaussian kernel size of 10 pixels

    and variance of 0.5 can smooth the result.

    Motion Artifacts in the z-Axis

    As we have discussed previously, optical flow has

    been able to recover exact motion fields in the 2D

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    Figure 3. Different motions of renal tissue and their extraction.

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    images even in the presence of large motion arti-

    facts in the z-axis (such as cardiac motion detec-

    tion in B-mode echocardiographic series).

    The motion in the z direction is called an out-

    of-plane error. There are 2 techniques to cope with the out-of-plane error: (1) temporal win-

    dowing (spatiotemporal windowing) and (2)

    confidence measurement.

    1. Temporal windowing (spatiotemporal win-

    dowing). This technique applies a gaussian kernel

    among the consecutive frames (using a weighted

    summation of the consecutive frames). This strat-

    egy reduces the effect of the out-of-plane error,

    especially when the temporal kernel is large.

    Moreover, temporal windowing dramatically

    decreases the power of noise and increases the sig-

    nal to noise ratio, which is a helpful phenomenonin noise-sensitive optical flow techniques.

    2. Confidence measurement. The robustness

    and sensitivity of the optical flow methods are

    not the same among different regions of an

    image. Considering a confidence measurement

    for the motion estimation increases the accura-

    cy, especially for the out-of-plane error regions.

    A detailed discussion of confidence measure-

    ment was published previously.30

    Clinical Evaluation

    Any medical system should be implemented on

    real tissue before practical application. We selected

    3 healthy sheep and then occluded a renal seg-

    mental artery in each to observe the heat changes

    in that special lobule (each lobule is supplied by

    a segmental artery). Theoretically, we should have

    had a decrease in the renal lobular temperature

    after occluding the segmental artery. The occlusion

    was done surgically, and a gradual reopening of the

    segmental arterial branch was performed in nearly

    2 hours to model anticoagulation reperfusion med-

    ications ideally. The animals were anesthetizedwith midazolam and morphine. The incision was

    done as a great midline incision. The whole surgery

    lasted 1 hour and was finalized with a bolus of

    potassium chloride injected intravenously.

    Results

    B-Mode Sonographic Simulation

    The coefficients described in Renal B-Mode

    Sonographic Simulation above were used in the

    sonographic simulation. Finally a 20-frame

    sonographic sequence was obtained, in which 1

    point was considered the hot point. The temper-

    ature of the hot point varied from 0C to 50C.

    The appropriate thermal coefficient and motionartifacts were assigned to the simulation.

    Different motion estimation techniques were

    implemented and optimized using different

    parameters. In this study, the evaluation was per-

    formed on simulated images to find out the best

    algorithm and optimized coefficients.

    Evaluation of Motion Estimation Methods on

    the Simulated Data (Finding the Optimized

    Method)

    According to the algorithm, which was discussed pre-

    viously, we synthesized the computerized B-modesonographic movies. The speckle-tracking tech-

    niques were evaluated on these simulated images.

    All sequences were prefiltered using a gaussian

    kernel of size 20 pixels and variance 0.5. For the

    Lucas-Kanade method, we experimentally found

    that a local window of size of 5 pixels was the best

    one. All other parameters were set as described

    by Barron et al.35 For the Horn-Schunck method,

    an iteration number equal to 300 was found to

    be the best. The number was optimized

    between 0 to 1000, and 600 was found to be the

    best. Gaussian spatial and temporal windows

    were considered 15 pixels and 10 frames, respec-

    tively. All the applications were performed in

    MATLAB 7.1 (The MathWorks, Natick, MA) with a

    3-GHz processor (Intel Corporation, Santa Clara,

    CA), and 1028 MHz of RAM.

    It is a very popular evaluation to implement the

    motion estimation techniques on the simulated

    sequences.35 Errors were computed with the

    widely used amplitude (Equation 11) and angu-

    lar errors (Equation 12):

    (11)

    (12)

    where V, Vdefine the real and estimated vectors.33

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    Figures 47 show the results of the implementa-

    tion of different motion estimation techniques on

    the simulated images with respect to the average

    amplitude and angular error. The gradient-based

    optical flow methods show better results than theblock-matching methods except the ES method.

    According to the images, newer block-matching

    techniques have better performance because of

    their adaptive behavior with respect to the previ-

    ous frame and their better searching strategy in

    the diamond search and 3SS. The performance of

    older block-matching techniques such as the 3SS

    is lower than that of the newer ones. The exhaus-

    tive and correlation-based methods are accurate

    but more computationally expensive. The corre-

    lation algorithm is the most time-consuming

    technique, and implementing the gradientdescent cannot dramatically remove this prob-

    lem. There was no significant difference between

    the MAD and MSE, but the MSE takes more time.

    Among the optical flow techniques, the moment-

    based approaches act better because of their

    invariant hypergeometry. Horn-Schunck outper-

    forms the popular Lucas-Kanade due to its higher

    robustness to the out-of-plane error. The imple-mentation of the phase matching has a small

    effect on increasing the accuracy. Increasing the

    optical flow iterations can increase the accuracy

    but also increases the time consumption.

    Table 1 shows the results of implementation of

    the optimized optical flow (multiresolution Horn-

    Schunck) and optimized block-matching (ARPS)

    techniques for thermal detection. To determine

    the thermal changes, motion vectors are derived

    once with respect to the vertical axis. Therefore,

    the robustness to noise and achieving smooth

    results will be very important. Theoretically, theHorn-Schunck energy function has a smoothing

    term that achieves smooth and visually attrac-

    tive results. Therefore, thermal detection is more

    accurate based on the Horn-Schunck algorithm.

    Moreover, the multiresolution moment imple-

    mentation of the Horn-Schunck technique has

    the ability to achieve invariant features and

    reduce noise (contrary to their high-pass nature).

    Figure 8 shows 2 frames of the synthetic

    sequence before and after the thermal shift. Figure

    9 is the result of the implementation of the most

    accurate algorithm (Horn-Schunck) using the

    optimized coefficients on the mentioned frames.

    The thermal motion is extracted after subtracting

    the interpolated motion from the total motion.

    The left image is the total motion vector and is pre-

    dominantly made up from the motion artifact.

    The right image shows the net thermal shift after

    motion artifact removal using the proposed

    method.

    Figure 10 is the color-coded result of the ther-

    mal change in the same frames. The top image

    shows the real thermal change (ground truth), which was used in the model, and the bottom

    images show the result of the optimized method

    in the presence of a motion artifact (left image)

    and without a motion artifact (right image).

    In Vivo Results Based on the Optimized Method

    So far, it has been shown that the multiresolu-

    tion Horn-Schunck method is the optimized

    technique for simulated ultrasound images.

    We implemented this algorithm on the real data

    1542 J Ultrasound Med 2009; 28:15351547

    Monitoring of Thermal Changes During Revascularization Therapy

    Figure 4. Comparison of different block-matching speckle-tracking methods usedon the simulated data.

    Figure 5. Comparison of different block-matching speckle-tracking methods usedon the simulated data.

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    during occlusion and reopening of the renal

    artery, only the optimized motion estimation

    technique, ie, multiresolution Horn-Schunck,

    was applied to the sequences, and the coeffi-

    cients were set the same as for the simulatedsequence validation. It is very difficult to quan-

    titatively analyze the thermal change on real

    animal frames, and we validated the in vivo

    results on the basis of the clinical knowledge of

    physicians.

    The real sequences were obtained using a

    probe frequency of 7 MHz and a temporal reso-

    lution of 25 frames per second. Three sheep were

    anesthetized successfully using midazolam and

    morphine. All of the subjects remained alive dur-

    ing the whole surgery, and no significant operat-

    ing room side effect happened.Figure 11 shows 2 frames of the sequence,

    which were taken 0 and 10 minutes after the

    reopening. The occluded artery in not visible

    in the ultrasound images, but the thermal

    change results of the arterial occlusion can be

    detected.

    1. In the first step, the total motion is extracted

    (combined motion artifact and thermal change)

    for the ROI and ROI neighborhood using the

    optimized method. The ROI (a 200 200 box) is

    defined manually for the first frame. The ROI

    neighborhood pixels are defined as 100 pixels

    around the primary ROI. Figure 12 shows imple-

    mentation of the optimized algorithm (mul-

    tiresolution Horn-Schunck) on the real

    ultrasound images in the ROI and ROI neighbor-

    hood pixels for the mentioned frames.

    2. In the next step, the interpolated motion vec-

    tors of the ROI are computed on the basis of the

    motion vectors of the ROI neighborhood pixels.

    We implemented cubic Ispline interpolation in

    2D followed by mild gaussian smoothing (vari-

    ance, 0.1; size, 5 5). Figure 13, left image, showsthe total motion vector for the mentioned frames.

    3. To extract the pure thermal change, we sub-

    tracted the total ROI motion vectors (Figure 13, left

    image) from ROI motion artifact (Figure 13, cen-

    ter image). Figure 13, right image, shows the total

    motion vector in the ROI region.

    4. The vertical thermal motion vectors are

    derived with respect to the vertical axis to deter-

    mine the net thermal change. Figure 14 shows

    the thermal elevation in the ROI.

    As proved, the lower renal lobe temperature

    increases. It is evident that there is a warm-up

    gradient in the temperature in the bottom of the

    renal tissue, which correlates well with the

    anatomy of the lower renal lobe perfusion. With

    respect to the fact that the lower renal segment

    was being occluded and reopened in that case,

    the lower renal part warm-up is noteworthy after

    the reperfusion.

    Figure 15 shows the thermal change between 0

    and 5, 0 and 10, 0 and 15, and finally 0 and 20minutes in the sonographic series. In the last 2

    J Ultrasound Med 2009; 28:15351547 1543

    Abolhassani et al

    Figure 6. Results of implementation of optical flow techniques on the simulateddata.

    Figure 7. Comparison of different block-matching speckle-tracking methods usedon the simulated data.

    Table 1. Thermal Detection Results of the Best Motion EstimationMethod of Each Category

    Thermal Change Average Variance of ThermalMethod Error, C Change Error, C

    ARPS 1.2 2.4Horn-Schunck 1.02 1.9Multiresolution Horn-Schunck 0.50 0.502

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    color images, even branching of the central lobar

    artery is substantial (although sonography can-

    not even show the main artery). Note that ther-

    mal change estimation cannot extract the

    primary temperature but only the thermal

    change between 2 frames.

    We averaged the temperature change of the ROI

    of each frame. Figure 16 shows that the averagedtemperature in the ROI increases after reopening

    of the arterial segment (warming section). The

    results of the real data were validated by clinical

    experts. The plots in Figures 15 and 16 are well

    related to the clinical knowledge of the lower seg-

    mental renal artery.

    Discussion

    We have proposed a novel real-time and nonin-

    vasive method for thermal detection based on

    ultrasound velocity changes in tissue matter.

    This technique was used to follow revasculariza-

    tion therapy in renal tissue after renal arterial

    occlusion. The motion artifacts were carefully

    removed. Implementation of the algorithm on

    the real and the simulated data showed a good

    correlation among them.

    1544 J Ultrasound Med 2009; 28:15351547

    Monitoring of Thermal Changes During Revascularization Therapy

    Figure 8. Simulated thermal change in renal tissue. The boxesshow the thermal detection ROI.

    Figure 11. Two frames of the renal sonographic series immedi-ately and 10 minutes after reopening. Note that the renal lower

    lobe artery cannot be seen. The boxes show the ROI, and the

    line indicates a slight vertical shift.

    Figure 9. Left image, Motion vectors of the abdominal sono-graphic model in the ROI of the aforementioned frames. Right

    image, Thermal change vectors after subtracting the motion arti-

    fact using the optimized method (multiresolution Horn-Schunck).

    Figure 10. Top image, Thermal change in the renal tissue.Bottom, right image, Result of implementation of the multireso-

    lution Horn-Schunck technique (the most accurate method)

    using the optimized coefficients in the presence of a motion arti-

    fact. Bottom, left image, Same implementation without a motion

    artifact. Obviously, the motion artifact decreases accuracy.

    Figure 12. Motion vectors of the ROI and ROI neighborhood pixels,which are a summation of thermal changes and a motion artifact.

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    Among all of the motion estimation techniques

    analyzed, the ARPS was the best block-matching

    method, whereas the moment-based multireso-

    lution Horn-Schunck technique was the best

    gradient-based method. However, the latter out-

    performed the former; therefore, we used the

    multiresolution Horn-Schunck technique for the

    thermal change extraction.The ARPS was the best block-matching method

    because of its adaptive strategy, which adjusts

    the next motion vectors according to the previ-

    ous vectors. The multiresolution approaches

    were able to extract different values of thermal

    change, overcome the local minima problem,

    and achieve more reliable outputs. Fine motions

    were preserved using finer moments, and large

    and coarse motions were preserved. For the sim-

    ulated images, the average thermal error was

    0.5C with an SD of 0.5C, although much lower

    errors can be obtained in noiseless (motionless)

    data. This method can be an efficient technique

    for revascularization therapy evaluation and

    follow-up based on digital B-mode sonographic

    methods. This study was also a good evaluation

    of several motion estimation techniques for

    speckle tracking.

    We are currently working on multigrid meth-

    ods to achieve faster techniques. Moreover, we

    are interested in implementing this algorithm in

    other clinical problems. Many vital changes in

    the human body also change the tissue temper-

    ature; therefore, thermal detection can be a ref-

    erence standard for tracking them. The most

    attractive but complex one is detecting the

    myocardial temperature during streptokinase-

    based coronary revascularization, which is very

    difficult because of the great myocardial contrac-

    tion and relaxation.

    J Ultrasound Med 2009; 28:15351547 1545

    Abolhassani et al

    Figure 13. Left image, Total motion vectors of the ROI. Centerimage, Interpolated ROI motion vectors using ROI neighborhood

    pixels. Right image, Subtraction of the left image from the cen-

    ter images, which is the thermal change.

    Figure 15. Renal B-mode sonograms and their extracted thermal changes afterarterial reopening in the ROI. The first image (a) was taken 10 minutes after the

    revascularization therapy, whereas the others were taken 20 (b), 30 (c), and 40 (d)minutes after the revascularization therapy respectively. There is a gradual ROIwarm-up when the artery is opened, and even branching of the vessel is evident

    in the last frame. e, Close-up of the thermal change in d.

    Figure 14. Thermal change after derivation of accumulatedthermal displacements in Figure 13, right image. The color bar

    shows the thermal change in degrees Celsius.

    Figure 16. Renal lower segment thermal elevation after reperfusion.The x-axis is the time in minutes, and the y-axis is the temperature

    of the tissue. Notice the close correlation with the clinical situation.

    Author: In Figure 14 legend, please verify Figure 13, right

    image, as changed from Figure 9c.

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