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British Journal of Radiology (2006) 79, 308-314
© 2006 British Institute of Radiology
doi: 10.1259/bjr/23046051
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Full Paper

Influence of post-treatment delay on the evaluation of the response to focused ultrasound surgery of breast cancer by dynamic contrast enhanced MRI

A Khiat, PhD, D Gianfelice, MD, M Amara, MSc and Y Boulanger, PhD

Département de Radiologie, Hôpital Saint-Luc du CHUM, 1058 St-Denis, Montreal, Quebec, H2X 3J4 Canada

Correspondence: Dr Y BoulangerPhD, Département de Radiologie, Hôpital Saint-Luc du CHUM, 1058 St-Denis, Montréal, Québec, H2X 3J4 Canada.


   Abstract
Top
 Abstract
Introduction
 Patients and methods
 Results
 Discussion
 References
 
The assessment of the effectiveness of MRI-guided focused ultrasound surgery (MRIgFUS) of breast carcinomas can be performed by dynamic contrast-enhanced magnetic resonance imaging (DCE-MRI) parameters which monitor the presence of residual tumour. The aim of this study was to evaluate the effect of the post-treatment delay on this assessment. DCE-MRI data were acquired immediately and 3–14 days after MRIgFUS treatment of 26 tumours (<7 days, n = 6; =>ge;7 days, n = 20). The percentage of residual tumour was determined histologically on the resected mass and correlated with two DCE-MRI parameters: increase in signal intensity (ISI) and positive enhancement integral (PEI). No correlation could be found between DCE-MRI data acquired immediately after treatment and the percentage of residual tumour. Good correlation coefficients were found for data acquired several days after treatment (ISI, r = 0.749; PEI, r = 0.778). However, they were higher when the post-treatment time interval was 7 days or more (ISI, r = 0.962; PEI, r = 0.934). These results suggest that a post-treatment delay of 7 days is necessary for the accurate assessment of the presence of residual tumour by DCE-MRI parameters.


   Introduction
Top
 Abstract
 Introduction
Patients and methods
 Results
 Discussion
 References
 
Magnetic resonance imaging-guided focused ultrasound surgery (MRIgFUS) is a non-invasive thermotherapeutic method allowing the elimination of different types of lesions without incision, thus reducing the risk of infection and scarring as well as diminishing the pain considerably [1]. MRIgFUS studies have been reported for patients with breast fibroadenomas [2], breast carcinomas [3–6] and uterine fibroids [7, 8]. The ultrasound radiation produced by a transducer elevates the temperature at a focal point and destroys the tissue by protein denaturation and tissue necrosis. The repeated application of the procedure leads to the ablation of multiple points covering the entire lesion or the desired part of the lesion. As the exact location of the focal points may vary depending on the tissue composition through which the focused ultrasound beam passes, monitoring the effects of the focused ultrasound is done using a non-invasive method such as MRI.

Once the MRIgFUS is performed, early detection of residual disease is of crucial importance to evaluate the response. Indeed, clinical examination is compounded by necrosis and fibrosis which are often intermixed with residual tumour, breast oedema, or inflammation. Dynamic contrast-enhanced magnetic resonance imaging (DCE-MRI) allows the monitoring of the presence of tumour by demonstrating changes in the enhancement curves following the injection of contrast agent [9, 10]. In the breast, this technique has been applied to detect the presence of tumours [11–13], to assess their grade [14, 15] and to monitor the results of different types of treatment [16–18]. Enhancing lesions on post-treatment DCE-MR images are normally indicative of the presence of significant residual tumour, but growing evidence suggests that the situation may be more complicated due to the fact that some benign processes such as oedema, fibrosis, necrosis and inflammation can mimic malignant contrast [19, 20]. Hence, the presence of contrast enhancement alone is not exclusively specific to residual cancer. An enhancing lesion indicates abnormal tissue, but the shape of the enhancement curve must be considered to identify the nature of this tissue. Indeed, inspection of the lesion morphology and enhancement profile shows that most malignancies have an irregular border and display very rapid enhancement and a distinct early washout phase in DCE-MRI. This pattern can be used to distinguish malignant masses from benign lesions or normal tissue which enhance and washout slowly [21]. Since benign phenomena due to the therapy such as necrosis, fibrosis, oedema and inflammation can often occur and be responsible for abnormal enhancement, the time interval between treatment and post-treatment must be taken into account when analysing DCE-MRI data to minimize the contribution of these processes. In the case of conventional treatments such as lumpectomy and conventional surgery, time intervals ranging from 4 weeks to 12 months have been reported to be necessary for a reliable assessment of residual tumour by DCE-MRI [19, 20, 22, 23].

In our efforts to assess the value of the MRIgFUS technique for the treatment of breast carcinomas, DCE-MRI data were collected immediately and several days after treatment, and then compared with the percentage of residual tumour determined by histopathology of the excised treated mass. In our previous report, data acquired several days after treatment were presented for 17 patients which demonstrated a strong correlation between DCE-MRI parameters and the percentage of residual tumour [5]. However, for a few patients the correlation was inexplicably poor. In the present study, DCE-MRI data acquired both immediately and several days after treatment were analysed for 25 patients (26 tumours) to determine the effect of the time interval between MRIgFUS and post-treatment MRI data acquisition.


   Patients and methods
Top
 Abstract
 Introduction
 Patients and methods
Results
 Discussion
 References
 
Patients
25 women aged between 45 years and 87 years (mean age±SD, 61.3 years±11.0) fulfilling the inclusion/exclusion criteria completed the protocol between March 2000 and June 2004. Each patient was diagnosed by core breast biopsy with an invasive breast carcinoma of less than 3.5 cm in diameter (Grade 1). The tumour volumes determined by MRI ranged between 0.11 cm3 and 11.2 cm3 (Table 1Go). All tumour types were invasive ductal carcinomas except for one. In one patient (patient 7), two tumours were treated. All patients signed an informed consent form approved by the Scientific and Ethics Committees of our institution prior to any exam or MRIgFUS.


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  		Table 1. Lesion and exam parameters for breast tumours treated by MRI-guided focused ultrasound surgery (MRIgFUS)

 
Inclusion criteria were a life expectancy of at least 5 years and the possibility of receiving hormone replacement or Tamoxifen therapy. Major exclusion criteria were pregnancy or lactation, having previously undergone radiation or laser therapy, having received immunosuppressive therapy and having been treated with chemotherapy in the past 3 months. In addition, women with a history of grand mal seizures, severe cerebrovascular disease, haemolytic anaemia, or dialysis treatment; women who were receiving anticoagulation therapy; and women with breast implants were excluded. Patients were also excluded if their lesion was outside the margins of safety for ultrasound ablation, consisted only of microcalcifications, or had extensive intraductal components.

MRIgFUS
All MRI data were acquired with the GE 1.5 T MRI unit (Signa; GE Medical Systems, Milwaukee, WI) using a breast coil. The MRIgFUS treatments were performed by different versions of the ExAblate system developed by InSightec Inc. (Haifa, Israel and Dallas, TX). The MRIgFUS system and procedure have been described in detail previously [3]. Briefly, the patient is prone on the focused ultrasound table inside the MRI magnet bore. An acoustic ultrasound beam generated by a multielement phased-array transducer focused on a point that was thermally ablated. The location of the focal point was verified by the thermally sensitive fast spoiled gradient-echo MRI sequence [3]. Multiple adjacent focal points covering the entire tumour were treated sequentially to complete the FUS ablation.

Post-treatment MRI
The MR images used in this study were recorded both immediately and at a follow-up visit 3–14 days after the MRIgFUS but before conventional surgery. Among the 25 treated patients, six had their post-treatment evaluation 3 days after ultrasound ablation, 17 patients 7 days after ultrasound ablation (18 tumours), one patient 10 days and one patient 14 days after ultrasound ablation (Table 1Go). The timing of the post-treatment examination depended on the availability of the MRI scanner and on the scheduling of the surgery. DCE-MR images were acquired before and after injection of the MR contrast agent gadopentetate dimeglumine (Berlex Canada Inc., Lachine, Canada; 0.1 mmol kg–1 body weight) using a three-dimensional fast spoiled gradient echo (FSPGR) sequence with fat saturation (repetition time (TR) = 6.4 ms; echo time (TE) = 2.4 ms; preparation time = 22 ms; flip angle = 10°, slice thickness = 4 mm; no intersection gap; 256 x 128 points; number of images = 32; acquisition time = 3.2 min).

Analysis of DCE-MRI data
To calculate the most enhancing pixel (1 mm2) within the entire tumour in the DCE-MR images, a utility program was written using MATLAB programming (Mathworks, Natick, MA) operating on Linux software. From a spherical ROI centred on the original tumour centre and covering the entire tumour region in the intensity vs phase image series, a Bézier curve was constructed by picking the control points (phase) to identify the most enhancing pixel. DCE-MRI parameters at the most enhancing pixel were evaluated by the FUNCTOOL version 2.5.36b software program (GE Medical Systems, Fremont, CA) from time-signal intensity curves. The dynamic contrast uptake at the most enhancing point was evaluated by calculating two parameters: percentage increase in signal intensity (ISI) and the positive enhancement integral (PEI). ISI corresponds to the percentage of the maximal increase in signal intensity after the injection of contrast agent (SIpost) relative to the pre-contrast signal intensity (SIpre): ISI = (SIpost–SIpre)/SIpre x 100. PEI is the integral of the area under the enhancement curve observed after the injection of contrast agent for the time-signal intensity graph acquired for a time t:


Formula 001

. Data were analysed separately for all patientstaking into account the time interval between the MRIgFUS and the DCE-MRI exam.

Surgery and histopathological evaluation
Patients underwent a routine segmental tumour resection 3–21 days after MRIgFUS, which included resection of wide margins around the area treated by focused ultrasound. Three-dimensional macroscopic and microscopic histopathological measurements were performed on the resected mass by a pathologist immediately after surgery [3, 24]. The total tumour volume, the volume of tumour in the treated zone and the volume of necrosed tumour were determined. Volumes (V) were determined by measuring the largest tumour dimensions in each axis (i.e. distances a, b, and c) and performing an ellipsoid volume calculation: V = ({pi}/6) abc.

Statistical analysis
Correlation coefficients between the DCE-MRI parameters ISI and PEI, and the percentage of residual tumour volume determined by histopathology were determined by a Pearson analysis. Correlations were considered significant at p<0.05 with r values > 0.50. Comparison of the correlation coefficients was performed using a t-test [25]. A receiver operating characteristic (ROC) curve analysis was performed for both DCE-MRI parameters. Statistical analyses were performed using the SPSS software version 9.0.1 (SPSS Inc., Chicago, IL).


   Results
Top
 Abstract
 Introduction
 Patients and methods
 Results
Discussion
 References
 
Processing of DCE-MRI data
Our home written program allowed rapid and automatic determination of the most enhancing point in the DCE-MR images acquired at the post-treatment exam. This method was found to be reliable and exactly reproducible on repeated measurements.

Histopathological data
Histopathology results of the excised mass following the MRIgFUS of breast carcinomas show a variable degree of success, as summarized in Figure 1Go and Table 1Go. Among the 26 treated tumours, seven tumours showed no detectable residual cancer at the site of MRIgFUS, 11 tumours had residual cancer below 10%, and seven tumours showed a larger percentage of residual cancer, which ranged between 20% and 90%.


Figure 1
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  		Figure 1. Graph showing the percentage of residual tumour determined by histopathology following MRI-guided focused ultrasound surgery(MRIgFUS) for 26 breast tumours in 25 patients. A variable degree of success was achieved at various stages of development of the technique.

 
DCE-MRI results
In general, complete tumour necrosis should be reflected by the absence of enhancement in the time-signal intensity DCE-MRI curves. Figure 2Go presents two types of time-signal intensity curves before, immediately after and several days after MRIgFUS observed for patients 19 (Figure 2a–cGo) and 21 (Figure 2d–fGo). Before treatment, a strong enhancement is observed in all cases at the most enhancing point of the breast tumour region (Figure 2a,dGo). In the case of patient 19, the tumour necrosis determined by histopathology was complete (Figure 1Go, Table 1Go) and no apparent enhancement was observed 7 days after treatment (Figure 2cGo). However, this assessment could not have been made immediately after treatment since a slowly enhancing curve was observed (Figure 2bGo). When residual cancer was present, as was the case for patient 21, a significant enhancement (Figure 2fGo) was observed with a steep washout pattern similar to the patterns observed before treatment (Figure 2dGo). In that case, the enhancement patterns were very similar immediately and 3 days after MRIgFUS (Figure 2e,fGo).


Figure 2
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  		Figure 2. Dynamic contrast-enhanced magnetic resonance imaging(DCE-MRI) signal intensity curves as a function of image number (6.0 s/image) at the maximally enhancing pixel for patient 19 (a) before, (b) immediately after and (c) 7 days after MRI-guided focused ultrasound surgery (MRIgFUS), and for patient 21 (d) before, (e) immediately after and (d) 3 days after MRIgFUS. The absence of signal enhancement in (c) is consistent with the absence of residual tumour and the progressive signal enhancement in (b), (e) and (f) is attributable to benign tissue phenomena occurring in the first few days following focused ultrasound ablation.

 
Correlation between DCE-MRI and histopathology data
Figure 3a,bGo presents the correlations between the ISI parameter and the percentage of residual tumour volume determined by histopathology for all tumours and for the 20 tumours evaluated at least 7 days after the MRIgFUS, respectively. Similar correlations are presented in Figure 3c,dGo between the PEI parameter and the percentage of residual tumour volume determined by histopathology for all patients and for the patients having been evaluated at least 7 days post-treatment, respectively. Strong correlations between the DCE-MRI parameters ISI (r = 0.749) and PEI (r = 0.778), and the percentage of residual tumour volume were found. When six patients who had their evaluation only 3 days after MRIgFUS were excluded from the analysis, the correlations were much stronger, the correlation coefficients for ISI increasing to 0.962 (Figure 3bGo) and for PEI to 0.934 (Figure 3dGo). Using a t-test to compare the correlation coefficients for the ISI and PEI parameters for all values and for values obtained more than 7 days after treatment [25], a statistically significant difference was found for ISI (p<0.01) and an almost significant difference for PEI (p = 0.055).


Figure 3
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  		Figure 3. Graphs showing the correlation between parameters calculated from the post-treatment dynamic contrast-enhanced magnetic resonance imaging(DCE-MRI) data and the percentage of residual viable cancer determined by histopathology on the excised mass for breast tumours treated by MRI-guided focused ultrasound surgery (MRIgFUS): increase in signal intensity (ISI) for (a) all patients (r = 0.749) and (b) patients who had their post-treatment evaluation at least 7 days after treatment (r = 0.962); positive enhancement integral (PEI) for (c) all patients (r = 0.778), and (d) patients who had their post-treatment evaluation at least 7 days after treatment (r = 0.934). Points corresponding to patients whose post-treatment was performed 3 days after MRIgFUS are shown as asterisks (*) in (a) and (c).

 
Due to the presence of enhancement in practically all cases, no correlation could be found between the ISI and PEI parameters and residual tumour volume for data acquired immediately after treatment.

ROC curve analysis
Receiver operating characteristic (ROC) curves are presented in Figure 4Go for the ISI parameter. When the data for all tumours were used, the area under the curve was 0.853 with a p-value of 0.005 for asymptotic significance (Figure 4aGo). The same analysis was made for the 20 tumours whose DCE-MRI data were recorded 7 days or more after treatment, which yielded an area under the curve of 0.986 with a p-value of 0.001 for asymptotic significance (Figure 4bGo). The cut off ISI value for both curves corresponded to 7% with a sensitivity of 100% and a specificity of 83%. The ROC curve analysis for the PEI parameter showed an area under the curve of 0.732 without asymptotic significance (p = 0.067) for all tumours, and an area under the curve of 0.785 without asymptotic significance (p = 0.055) for patients whose DCE-MRI exam was performed 7 days or more after treatment. The cut off value for PEI was 4% with a sensitivity of 67% and a specificity of 83%.


Figure 4
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  		Figure 4. Receiver operating characteristic curves for the increase in signal intensity(ISI) parameter calculated from the dynamic contrast-enhanced magnetic resonance imaging (DCE-MRI) data for (a) 26 tumours analysed 3–14 days after the MRI-guided focused ultrasound surgery (MRIgFUS) and (b) 20 tumours analysed 7–14 days after the MRIgFUS. The areas under the curves were (a) 0.853 and (b) 0.986 and the p-values for asymptotic significance were (a) 0.005 and (b) 0.001. A significant improvement is obtained when only data for patients examined 7 days or more after MRIgFUS are considered.

 

   Discussion
Top
 Abstract
 Introduction
 Patients and methods
 Results
 Discussion
References
 
The calculation of the ISI and PEI parameters from DCE-MR images requires an accurate determination of the most enhancing point in the tumour area. The strategy of using the automatically identified most enhancing pixel was based on the conclusions of previous work clearly demonstrating improved results with this strategy compared with using large regions of interest [26]. This was achieved by using a home written program which allowed rapid identification of this point, thus significantly reducing the time for analysis compared with the manual location of this point used in our previous report [5]. This study has also the advantage of using volumes for histological quantitation of tissue. In previous studies, diameter values were utilized. As tumour and non-tumour masses are generally not spherical, the volume calculation leads to increased accuracy.

The analysis of DCE-MRI data recorded immediately after performing MRIgFUS showed enhancement patterns in practically all cases and no correlation could be found between the ISI or PEI parameters and the percentage of residual tumour determined by histopathology. These enhancements are attributable to benign phenomena such as haemorrhage, fibrosis, inflammation or oedema caused by the treatment and which prevent accurate assessment of the percentage of residual tumour by DCE-MRI.

Analysis of the post-treatment DCE-MRI data acquired 3–14 days after MRIgFUS of small breast tumours revealed that the ISI and PEI parameters correlate strongly with the percentage of residual tumour determined by histopathology. The correlation coefficients for the two parameters are very similar (0.749 for ISI and 0.778 for PEI) based on data from 26 treated tumours whose volume of residual tumour determined by histopathology varied between 0 and 90%. When data for six tumours analysed less than 7 days after treatment were not considered, the correlation coefficients significantly improved, reaching 0.962 for ISI and 0.934 for PEI. These results stress the importance of the time interval between MRIgFUS therapy and post-treatment evaluation. In previous reports, the importance of the time interval between treatment and DCE-MRI was discussed for invasive treatments of breast lesions [19, 20, 22, 23]. In a study of 68 patients whose breast lesions were treated by lumpectomy, an interval of 28 days after treatment was recommended before the DCE-MRI examination [23]. When conventional surgery was performed, time intervals of 9–12 months were necessary to obtain reliable data [19, 20, 22]. As conventional surgical treatments cause a much larger perturbation of the tissue, the fact that the interval necessary is much longer than for MRIgFUS is consistent with the difference in severity between the two procedures.

For some patients the correlation between DCE-MRI parameters and percentage of residual tumour volume was especially poor, such as for patient 21 whose time-signal intensity curves displayed abnormally high enhancement leading the ISI and PEI parameters to show as outliers on the correlation curves with the percentage of residual tumour. This unexpected enhancement is attributable to the fact that residual tissue is not residual tumour, but rather consists of enhancing benign tissue such as inflammation, necrosis, fibrosis or oedema at the site of MRIgFUS. It is known that the post-treatment contrast enhancement resulting from such phenomena limits the positive predictive value and specificity for the diagnosis of residual disease [23, 27]. In our case, two arguments support this explanation. The first argument is that patient 21 was evaluated only 3 days after the MRIgFUS. When the six patients who had their evaluation only 3 days after treatment were excluded from the analysis, the results were more reliable as assessed by higher correlation coefficients and larger areas under the ROC curves. The second argument in favour of non-tumour tissue for patient 21 pertains to the shape of the time-signal intensity curve at the post-treatment examination. The pattern of this curve does not correspond to the expected curve profile of a malignant tissue [21]; it displays a slow rate of enhancement in comparison with the time-signal intensity enhancement curve at the pre-treatment exam and it continues to rise over the course of the examination. Malignancies typically display an irregular border at the histological analysis; they enhance very rapidly and display a distinct early washout phase in the DCE-MRI curves. For breast cancers, Figure 2a,cGo represents a typical pattern. Previous studies have concluded that the presence of contrast enhancement alone is not specific for residual cancer, and that the shape of the enhancement curve is a very important factor to consider [21, 28, 29]. Additional consideration of the morphology and internal architecture of the excised mass and a critical analysis of the time-signal intensity curves can be used to help distinguish residual tumours from benign processes. In a previous publication [3], histological slides were presented for a patient analysed 3 days after MRIgFUS which clearly show these phenomena. Obviously, these benign processes depend on the sensitivity of each patient, and are strongly influenced by the time interval between MRIgFUS and post-treatment evaluation. Consequently, the accuracy of DCE-MRI for predicting residual disease is affected by these processes.

Comparison of the ROC curves for all patients and for the patients examined 7 days and more after MRIgFUS shows a significant improvement with an area under the curve of the ISI parameter increasing from 0.853 to an almost perfect 0.986 for the latter group. The same trend was observed for the PEI parameters although lower values were obtained. These results confirm the importance of the post-treatment time interval and suggest that the ISI parameter is a better parameter to evaluate treatment outcome. The cut-off value for the determination of residual tumour was around 7% for ISI and 4% for PEI.

The main limitation of this study is the low number of patients with a high percentage of residual tumour. Although our group has reported the largest number of patients treated by MRIgFUS, the accuracy of our correlations could be improved if more patient data were available. Most of our patients showed less than 10% residual tumour. At low percentages, the accuracy of the technique is reduced. This situation is unlikely to improve as the treatment technique is increasingly successful. Nonetheless, our results demonstrate a high degree of specificity and sensitivity for the DCE-MRI parameters.

In summary, our results demonstrate that DCE-MRI parameters such as ISI and PEI are both useful in determining the effectiveness of MRIgFUS in breast carcinomas, provided the measurements are performed sufficiently long after treatment, i.e. approximately 7 days, based on our data. Benign phenomena caused by the treatment are responsible for abnormal enhancement in the first few days. The accuracy of our analysis could be improved by increasing the sample size and by evaluating patients longitudinally at different time intervals after MRIgFUS.


   Acknowledgments
 
The authors thank Mr Martin Ruel, BSc, Dr Assia Belblidia, MD, and the radiology technologists at Hôpital Saint-Luc du CHUM for data acquisition. They are grateful to Dr Sharon Thomsen, MD, for assistance with histopathological analyses. The financial support from InSightec, Inc., Haifa, Israel and Dallas, TX and from the Canadian Institutes of Health Research, Ottawa, Canada is acknowledged.


   Footnotes
 
Sources of support: InSightec, Inc. (Haifa, Israel and Dallas, TX) and the Canadian Institutes of Health Research (Ottawa, ON, Canada).

Received for publication June 7, 2005. Revision received August 15, 2005. Accepted for publication September 15, 2005.


   References
Top
 Abstract
 Introduction
 Patients and methods
 Results
 Discussion
 References
 

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