Original Research

Study of Laser Ablation in the In Vivo Rabbit BrainWith MR Thermometry

Lili Chen, PhD,1 Janaka P. Wansapura, PhD,1 Gary Heit, PhD,2 and Kim Butts, PhD1*

Purpose: To investigate the peak temperature and thermaldose (T43) as tissue damage indicators for thermal therapy.

Materials and Methods: The proton resonant frequency(PRF) shift thermal coefficient was calibrated on six in vivorabbit brains during interstitial laser ablation. The peaktemperature and T43 were correlated with the lesion bound-ary observed on T2-weighted spin-echo (SE) MRI at 4 hourspost-heating in seven thermal lesions using direct MR mea-surement and analysis based on a binary discriminatemodel.

Results: The peak temperature and T43 were 48.3 � 1.7°Cand 191 � 219 minutes, respectively, from the direct MRmeasurement. The values derived by the binary discrimi-nate analysis were 47.8 � 2.2°C and 28 � 41 minutes,respectively.

Conclusion: Our results suggest that tissue damage inrabbit brain 4 hours after thermal ablation can be predictedreliably from a threshold temperature of approximately48°C.

Key Words: laser ablation; interventional MRI; thermaldose; thermometry; in vivo rabbit brain

J. Magn. Reson. Imaging 2002;16:147–152.© 2002 Wiley-Liss, Inc.

IMAGE-GUIDED THERMAL THERAPY is very promis-ing for the minimally invasive and noninvasive treat-ment of benign and malignant tumors. Image guidancecan be used to monitor the procedure to ensure thesafety and efficacy of the treatment. MRI is particularlypromising as a guidance modality because of its excel-lent soft-tissue contrast, sensitivity to temperature,and ability to evaluate tissue damage after therapy.

Many studies have shown that thermal lesions can beclearly visualized on MR images (1–16). In our previous

studies (15,16) we demonstrated that T2-weighted MRIcorrelated within 0.5 mm with the cell death zone usingcell viability staining with triphenyl tetrazolium chlo-ride (TTC) in rabbit brain 4 hours after focused ultra-sound ablation. Although T2-weighted MRI accuratelydepicts thermal lesions post-treatment, it cannot beused for real-time monitoring in the brain due to a timedelay of more than 15 minutes before the lesion ap-pears (15). Real-time MR thermal mapping can providean indication of tissue damage if a measure of tissuedamage is known. Several studies have elucidated spe-cific values of peak temperature, thermal dose, and atemperature-time product for thermal indicators of tis-sue damage in various tissue types, such as in the thighmuscle and the prostate (17,18). However, much workneeds to be done before values for thermal indicatorscan be determined for all tissue types and cancers. Thisis especially true since initial studies on different tis-sues have resulted in different values for these param-eters (17,18). For example, the threshold temperatureof 51°C and the T43 of 200 minutes in the in vivo canineprostate were reported by Peters et al (18), while 47°Cand T43 of 4.7 minutes in the in vivo rabbit muscle werereported by McDannold et al (17).

The purposes of this work were to investigate thethreshold temperature and thermal dose, T43 (19), asindicators of tissue damage in the in vivo rabbit brain,and to determine a practical approach for in vivo ther-mal monitoring on an interventional MRI scanner.

MATERIALS AND METHODS

Laser System and MR Scanner

Custom-made, conical-tipped laser fibers (30 feet long)manufactured by Surgical Laser Technologies (Mont-gomeryville, PA) were used. The fibers were 0.6 mm indiameter, with a 5-mm-long tip and 0.2-mm diameter(laser diffusion region). The wavelength was 1064 nm.The laser power source was located outside the scanroom. All the MR images were performed using a stan-dard 0.5 T Signa SP open MRI system (GE MedicalSystems, Milwaukee, WI).

PRF Thermal Coefficient Calibration

Six New Zealand white rabbits (3.5–4.0 kg) were used.The animal experiments were approved by the Admin-

1Department of Radiology, Stanford University, Stanford, California.2Department of Neurosurgery, Stanford University, Stanford, Califor-nia.Contract grant sponsor: Whitaker Foundation; Contract grant sponsor:NIH; Contract grant numbers: R21 CA 79931; RR 09784.*Address reprint requests to: K.B., Department of Radiology, StanfordUniversity, 1201 Welch Rd., Stanford, CA 94305-5488.E-mail: Kim@s-word.stanford.eduReceived August 21, 2001; Accepted March 29, 2002.DOI 10.1002/jmri.10152Published online in Wiley InterScience (www.interscience.wiley.com).

JOURNAL OF MAGNETIC RESONANCE IMAGING 16:147–152 (2002)

© 2002 Wiley-Liss, Inc. 147

istrative Panel on Laboratory Animal Care (APLAC) atStanford University. Each rabbit was anesthetized withketamine (35 mg/kg) and xylazine (5 mg/kg) adminis-tered subcutaneously. After induction, the rabbit wasintubated and anesthesia was maintained with isoflu-rane (2% to 3%) and oxygen (1%). Prior to laser ablation,a piece of skull (approximately 25 � 20 mm) was sur-gically removed. The dura mater was carefully rupturedwithout injury to the brain. The rabbit was placed in thebore of the 0.5 T MR scanner in a prone position. Anextremity coil was placed above the brain. A warm plas-tic blanket was placed between the scanner table andthe rabbit to aid in thermoregulation. A laser fiber wasinserted 8 mm into the brain and was placed betweentwo Luxtron fiberoptic temperature sensors (LuxtronCorporation, Santa Clara, CA). The Luxtron sensorswere 8 mm apart and 8 mm into the brain. All threefibers were placed in one hemisphere in a sagittal MRIplane, approximately 3 mm away from the longitudinalfissure. T1-weighted fast spin-echo (FSE) images (TR/TE � 500/17 msec, FOV � 16 � 16 cm, matrix � 256 �128, slice thickness � 3.0 mm) were performed to checkthe registration between the MRI scan plane and thetwo Luxtron temperature sensors. Gradient-echo (GE)MR phase images with three TE settings in separateexperiments (TR/TE � 77.2/38.9, 21.5, 13.3 msec;FOV � 16 � 16 cm; matrix � 256 � 128; slice thick-ness � 3.0 mm; flip angle � 30°; image time � 10seconds) were continuously obtained before, during,and after heating. A reference phantom, separated fromthe animal by 2 cm, was used for correction of anyscalar phase drift during imaging. After heating, theprocedure was repeated for the other hemisphere. Thebrains were heated with 2 W laser power. The heatingtime ranged from 1 to 8 minutes. The maximum tem-peratures measured by the Luxtron temperature sen-sors ranged from 45°C to 83°C (�T � 10–47°C). Allanimals were euthanized with intravenous injection ofeuthanasia solution at 1 mL/4.5 kg immediately afterheating.

Thermal Ablation Techniques

Seven rabbits were used to study the correlation be-tween maximum (threshold) temperature, thermaldose, and lesion boundary on T2 SE-weighted MRI.Each animal was anesthetized and prepared as de-scribed above. The rabbit was placed in the bore of the0.5 T Signa SP MR scanner in a prone position. A laserfiber was inserted approximately 8 mm into the brainand 3 mm lateral to the longitudinal fissure. Two ricenoodles (approximate 1 mm in diameter) were insertedapproximately 8 mm into the brain, on both sides of thelaser fiber, as fiducial markers. The laser fiber and thetwo rice noodles were located within a sagittal MR scanplane. A Luxtron temperature sensor was inserted 8mm into the brain and approximately 4 mm lateral tothe laser fiber, and baseline temperature was mea-sured. A reference phantom separated from the animalby 2 cm above the animal was used for correction ofphase drift during imaging. T1-weighted FSE (TR/TE �500/17 msec, FOV � 16 � 16 cm, matrix � 256 � 128,slice thickness � 3.0 mm) images were used to check

the registration between the MR scan plane and thefiducial markers. The brains were heated with 2 W laserpower. The heating time ranged from 30 to 581 seconds(Table 1). To ensure that a thermal lesion was created ineach experiment, heating was applied until a tempera-ture of at least 55°C was measured by Luxtron temper-ature sensor. GE MR phase images were continuouslyacquired (TR/TE � 77.2/38.9 msec; FOV � 16 � 16cm; matrix � 256 � 128; slice thickness � 3.0 mm; flipangle � 30°; image time � 10 seconds) before, during,and after heating. One pixel resolution was 0.6 � 1.2 �3.0 mm. Based on our previous studies, in which thethermal lesion on MRI correlated well with the celldeath zone at 4 hours post-treatment (16), the animalswere kept in the magnet under general anesthesia for 4hours. A set of T2-weighted SE MR images were thenacquired (TR/TE � 4000 msec; matrix � 512 � 256;FOV � 16 � 16 cm; slice thickness � 2 mm; number ofexcitations � 4). One pixel resolution was 0.3 � 0.6 �2.0 mm. The animals were then euthanized.

Data Analysis

Image Processing

MR temperature maps were processed in near real timeto provide immediate assessment of the heating. Base-line phase maps acquired before heating were sub-tracted from the remaining phase maps. This was doneby multiplying each image by the complex conjugate ofthe baseline image on a pixel-by-pixel basis. In addi-tion, the phase measured in the separate phantom wassimilarly subtracted from the phase maps. This wasdone to correct for any scalar phase drift during thecourse of the heating. This processing was repeatedretrospectively at the time of image analysis.

PRF Thermal Coefficient Calibration

A region of interest (ROI) for MR temperature measure-ment was taken at the tip of the thermal sensor (2 � 2pixels). Paired data (MR, Luxtron) were obtained from1140 time-points. Lines were fitted to the phase shift(��) vs. temperature elevation (�T) for each TE, and to��/�T vs. TE, respectively. The thermal coefficient wasfound from the fitted line. The data analysis indicatedan interaction between the laser beam and the Luxtrontemperature sensors. As a result, our calibrations only

Table 1Heating Parameters Used to Make Seven Lesions in SevenAnimals for Temperature and T43 Measurements

Lesion no.Laserpower

(W)

Baselinetemperature

(°C)

Heatingduration

(s)

Lesiondiameter

(mm)

1 2 37.2 200 7.82 2 33.5 187 5.63 2 33.8 30 6.94 2 35.0 120 8.85 2 36.0 330 9.46 2 37.5 250 8.87 2 34.6 581 10.3

148 Chen et al.

used the data points that were taken when the laserwas turned off.

Measurement of Peak Temperature and T43 on theLesion Boundary Using Direct MR Measurement

Seven lesions were used for data analysis. The fiducialand anatomical markers were used for registration be-tween T2 and GE-MRI. The exterior margin of the brightring on T2-weighted SE-MRI was defined as the thermallesion boundary (Fig. 1). T2-weighted images were mag-nified 4 times (2048 � 1024) using a bilinear interpo-lation in order to trace the boundary accurately. Thelesion boundaries were then manually traced, as werethe fiducial markers and the outline of the brain. Thefiducial markers and outline of the brain were regis-tered to the GE images used for the temperature map-ping. The manually traced lesion boundary was thensuperimposed on MR temperature maps. For each pixelin the lesion boundary, the maximum temperaturereached through the entire heating was measured. Thepeak temperatures from the lesion boundary were thenaveraged, yielding a single average value for each le-sion.

For each lesion, the cumulative thermal dose (T43)was calculated on each pixel over the lesion boundarybased on the Arrhenius-damage integral (19). The ther-mal doses from each pixel on the lesion boundary wereaveraged, yielding a single average value of T43 for eachlesion. The uncertainty of the T43 for each lesion was thedifference between the maximum and minimum valueson the lesion boundary.

Determination of Critical (Maximum) and T43 Using theBinary Discrimination Model

The values of critical temperature and T43 that discrim-inate the pixels just inside the lesion boundary fromthese just outside the boundary were determined usingreceiver operating characteristic (ROC) curves (5). TwoROIs were chosen: one at the location of one pixel insidethe lesion boundary, and the other at the location of onepixel outside the lesion boundary. The peak value ofeach pixel during the course of the heating was used forthe analysis. The threshold temperature/T43 is given bythe point geometrically nearest to the upper left cornerof the ROC curve, which corresponds to the thresholdvalue that maximizes the fraction of pixels just insidethe boundary exceeding the threshold, and minimizesthe fraction of pixels just outside the boundary that aremisclassified by exceeding the threshold.

RESULTS

Calibration of Thermal Coefficient

In this study we found the phase change, ��/�T (indegrees/°C), as a function of TE by

��/�T � � 0.0098� Bo TE � 0.48 (1)

where � is the gyromagnetic ratio, Bo the magneticfield strength, and 0.48 a phase offset (see Discus-sion).

Figure 1. T2-weighted MRI 4 hours after laser ablation, showing the thermal lesion boundary and two fiducial markers.

MR Thermometry for Thermal Therapy 149

Direct Measurement of Critical Temperature andT43 on the Lesion Boundary in MRI

Table 2 shows averaged values of threshold tempera-ture and T43 on the lesion boundary for seven lesions.The averaged value over all seven lesions is 48.3 � 1.7°C, and the averaged T43 is 191 � 219 minutes. Therange of the T43 value is 7.0–546 minutes.

Measurement of Critical Temperature and T43

Using a Discrimination Model

Figure 2a is a typical graph showing the number ofpixels in percent above a temperature threshold on theinside ROI vs. the number of pixels above that thresh-old on the outside ROI from lesion 1. A point on thecurve is chosen which is geometrically closest to the

upper left corner. This point corresponds to a thresholdtemperature of 48°C. At this temperature, 66% of pixelson the inside ROI were above the threshold value, whileonly 27% of pixels on the outside ROI were above thisthreshold temperature. These ROI data are again plot-ted in Figure 2b as the number of pixels above thethreshold temperature vs. threshold temperature. Thethreshold temperature of 48°C is plotted as a verticalbar, nicely differentiating the two ROIs. Table 3 sum-marized the threshold temperature derived from thediscriminate model over all seven lesions. On average,the threshold temperature is 47.8 � 2.2°C. At this tem-perature, 73% of pixels on the inside ROI were abovethe threshold temperature while only 30% of pixels onthe outside ROI were above this threshold.

Table 2Direct Measurement of Maximum Temperature and T43

on Lesion Boundary

Lesion no. Maximum T (°C)a T43 (minutes)b

1 47.8 � 2.7 20 (0.3–385)2 46.8 � 4.4 50 (0.1–601)3 47.4 � 3.4 546 (0.01–28200)4 51.1 � 3.3 330 (2.2–3681)5 48.4 � 1.9 18 (0.5–92)6 46.6 � 1.8 7.0 (0.1–77)7 50.2 � 3.2 366 (2.0–6174)

Average 48.3 � 1.7 191 � 219 (7.0–546)aThe error is the standard deviation.bThese values in brackets are the variations from pixel to pixel.

Figure 2. a: Plot of the number of pixels in percent above a threshold temperature on the inside ROI vs. the number of pixelsabove that threshold on the outside ROI from lesion 1. The point on the curve geometrically closest to the upper left cornercorresponds to a critical temperature of 48°C. At this temperature, 66% of pixels in the inside ROI were above the thresholdvalue, while only 27% of pixels in the outside ROI were above this threshold temperature. b: Plot of the number pixels above thethreshold temperature vs. threshold temperature. The critical temperature of 48°C is indicated as a vertical line, nicelydifferentiating the two ROIs.

Table 3Threshold Temperature on Lesion Boundary Measured FromDiscriminate Model

Lesion no.Threshold T

(°C)

% pixels insideboundary

�threshold T

% pixels outsideboundary

�threshold T

1 48.0 66 272 45.3 66 343 46.7 91 314 51.4 61 305 48.7 62 346 45.2 91 127 49.2 71 43

Average 47.8 � 2.2 73 � 13 30 � 9

The error is the standard deviation.

150 Chen et al.

Similarly, the threshold T43 from lesion 1 was alsoplotted in Figure 3. The threshold T43 was found to be13 minutes. Figure 3a shows that 52% of pixels on theinside ROI were above the threshold while only 14% ofpixels on the outside ROI were above this threshold.These ROI data are again plotted in Figure 3b as thenumber of pixels above the threshold T43 vs. thresholdT43. The threshold T43 of 13 minutes was also plotted asa vertical bar, differentiating the two ROIs. Table 4shows the values of threshold T43 over all seven lesions.On average, the threshold T43 was 28 � 41min. At thisT43, 67% of pixels on the inside ROI were above thethreshold T43 while only 25% of pixels on the outsideROI were above the threshold. From Figures 2 and 3, wecan see that the threshold temperature and T43 models

provide similar discrimination values, although there isa large variation in T43.

DISCUSSION

The thermal coefficient of –0.0098 � 0.0005 ppm/°Cobtained from this study in rabbit brain in vivo is ingood agreement with that of –0.0098 � 0.0002 ppm/°Cin pig brain ex vivo reported by Harth et al (20). Peterset al (21) reported that the thermal coefficient is inde-pendent of tissue type ex vivo. The value of the thermalcoefficient obtained from this study is consistent withthe findings of Harth et al (20) in ex vivo brain, as wellas with our own previous study on ex vivo bovine liver(22).

A phase offset of 0.48 degrees/°C was found in ourcalibration study (see Eq. [1]). In an electrically conduc-tive media, B1 (t) experiences a phase lag dependent onthe temperature-sensitive electrical conductivity of themedia. This phase lag does not subtract away withsubtraction of baseline images and does not depend onthe TE. In our experiments, the phase offset was sub-stantial and not completely explained by the offset de-scribed by Peters and Henkelman (23). The exact rea-son for the apparent phase offset in our experimentsremains to be investigated.

It is evident from Eq. [1] that the effect of the phaseoffset on ��/�T will be smaller with longer TE. Forexample, with a shorter TE of 13 msec, there will be a48% error in ��/�T if the phase offset is not taken intoaccount. With a longer TE of 38 msec, there will be onlya 17% error in ��/�T if the offset is not taken into

Figure 3. a: Plot of the number of pixels in percent above a threshold T43 on the inside ROI vs. the number of pixels above thatthreshold on the outside ROI from lesion 1. The point on the curve geometrically closest to the upper left corner corresponds toa critical T43 of 13 minutes. At this T43, 52% of pixels in the inside ROI were above the threshold value, while only 14% pixels inthe outside ROI were above this threshold T43. b: Plot of the number pixels above the threshold T43 vs. threshold T43. The criticalT43 of 13 minutes is indicated as a vertical line, nicely differentiating the two ROIs.

Table 4Threshold T43 on Lesion Boundary MeasuredFrom Discriminate Model

Lesion no.T43

(minutes)

% pixels insideboundary

�threshold T43

% pixels outsideboundary

�threshold T43

1 13.2 52 142 0.6 68 393 4.7 84 244 104 53 235 6.8 71 406 1.6 91 107 70.8 53 24

Average 28 � 41 67 � 15 24 � 11

The error is the standard deviation.

MR Thermometry for Thermal Therapy 151

account. Therefore, we recommend the use of longer TEto reduce the effect of the phase offset if it will not beexplicitly measured. Alternatively, a two-echo sequencecan be used to obtain an initial phase at an early TE forsubtraction of the phase offset.

Detailed data analysis showed that on the tempera-ture vs. time curve, the maximum temperature for in-dividual pixels could be reached at different times (orimages) during heating. In this study, the peak temper-ature for each pixel on the lesion boundary was selectedover the entire heating time. In this way we ensuredthat the maximum temperature reached from eachpixel was measured as accurately as possible.

The results of our data suggest that in vivo calcula-tions of T43 are quite variable, more so than the calcu-lations of the critical temperature. This variability maybe in part due to the fact that our temporal resolutionwas relatively low at 10 seconds per image. Even anerror of a few seconds in measurement of the time at thepeak temperature can result in large variations in thecalculated T43. However, temporal resolution can onlybe gained at the expense of the signal-to-noise ratio(SNR) and/or spatial resolution. Graham et al (5) alsofound large variations in calculations of T43 ex vivo. Wewould agree with their assessment that from a practicalstandpoint it may be better and simpler to state thetime required at a particular temperature to achieve thedesired effect (5).

The results of this study are of significance to theclinical application of MRI guidance for thermal ther-apy. However, the parameters (critical temperature andT43) derived from this study are different from those incanine prostate reported by Peters et al (18) and inrabbit muscle reported by McDannold et al (17). It ap-pears that different organs may have different thresh-olds of temperature and T43 for tissue damage. It is notclear whether different cancers have different thresh-olds for tissue damage. Therefore, measurements invarious tissues and species are required before clinicalapplication of this technique.

In summary, we have validated thermal coefficientsin MRI in the in vivo normal rabbit brain using the PRFshift method. The threshold temperature and T43 as athermal dose from the thermal lesion boundary in MRIwere measured, yielding a value of 48°C for the thresh-old temperature. The value for T43 was highly inconsis-tent, which led us to conclude that in practice thisparameter would be difficult to use to monitor thermalablations that are similar to our experimental setup.

ACKNOWLEDGMENTS

We thank Dr. Karl Vigen for comments on the manu-script. We are grateful to Diane Howard and WendyBaumgardner for their expert technical assistance.

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