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British Journal of Radiology 75 (2002),220-228 © 2002 The British Institute of Radiology

Full Paper

Dynamic contrast enhanced MRI of the axilla in women with breast cancer: comparison with pathology of excised nodes

A D Murray, FRCR, FRCP1, R T Staff, PhD2, T W Redpath, PhD2, F J Gilbert, FRCR, FRCP1, A K Ah-See, FRCS3, J A Brookes, PhD2, I D Miller, FRCPath4 and S Payne, FRCPath4

Departments of 1 Radiology, 2 Biomedical Physics, 3 Surgery and 4 Pathology, University of Aberdeen and Aberdeen Royal Infirmary, Foresterhill, Aberdeen AB25 2ZN, UK


   Abstract
Top
 Abstract
Introduction
 Materials and methods
 Results
 Discussion
 References
 
Axillary lymph node status is the most important prognostic factor in breast cancer patients and is currently determined by surgical dissection. This study was performed to assess whether dynamic gadopentetate dimeglumine (Gd) enhanced MRI is an accurate method for non-invasive staging of the axilla. 47 women with a new primary breast cancer underwent pre-operative dynamic Gd enhanced MRI of the ipsilateral axilla. Lymph node enhancement was quantitatively analysed using a region of interest method. Enhancement indices and nodal area were compared with histopathology of excised nodes using a receiver operating characteristic (ROC) curve approach. 10 patients had axillary metastases pathologically and all had >=1 lymph node with an enhancement index of >21% and a nodal area of >0.4 cm2. 37 patients had negative axillary nodes pathologically. 20 of these had enhancement indices <21% and nodal areas <0.4 cm2. Using this method, a sensitivity of 100%, a specificity of 56%, a positive predictive value of 38% and a negative predictive value of 100% could be achieved. Using this method of quantitative assessment, dynamic Gd enhanced MRI may be a reliable method of predicting absence of axillary nodal metastases in women with breast cancer, thereby avoiding axillary surgery in women with a negative MRI study.


   Introduction
Top
 Abstract
 Introduction
Materials and methods
 Results
 Discussion
 References
 
The presence of metastases in ipsilateral axillary lymph nodes is the most important single predictor of long-term survival in patients with a new primary breast cancer [1]. At present, axillary status is determined by surgical axillary lymph node sampling or clearance. These procedures are not without long-term morbidity, which can include lymphoedema, seroma formation and occasionally nerve damage. It is not clear whether axillary node dissection offers improved survival and, in the majority of patients, surgical axillary node removal should be considered as a staging rather than a therapeutic procedure [2, 3].

In women with small primary tumours (<2 cm), the status of axillary nodes will determine the need for adjuvant therapy. However, axillary surgery is not usually indicated in the initial management of those with large primary tumours or those with unfavourable histology, as the results of surgery will not alter the indication for adjuvant therapy [4]. There has been an increase in the diagnosis of small primary breast cancers with the advent of mammographic screening [5]. Such small tumours are less likely to have associated axillary lymph node metastases. Thus, an increasing proportion of women are undergoing unnecessary axillary surgery with its associated morbidity. A non-invasive method of staging the axilla would therefore be highly desirable and should ideally have a negative predictive value of 100%.

It is well recognized that most primary breast cancers show rapid enhancement on MRI following gadopentetate dimeglumine (Gd) [6–8], and enhancement has also been noted in axillary lymph node metastases [9]. MRI without the use of Gd is inaccurate in staging the axilla [10]. Attempts to predict axillary node status from characteristics of the primary tumour on Gd enhanced MR mammography have shown some success [11].

The aim of this study was to prospectively compare dynamic Gd enhanced MRI of the axilla in women with small breast cancers with the histopathology of surgically excised axillary lymph nodes.


   Materials and methods
Top
 Abstract
 Introduction
 Materials and methods
Results
 Discussion
 References
 
Patient group
47 women with newly diagnosed primary breast cancer were recruited into the study, 20 from the breast screening clinic and 27 from the symptomatic clinic. Primary tumour sizes ranged from 8–15 mm in the screen-detected cancers and 5–31 mm in the symptomatic cancers. Histopathological types of the primary breast carcinoma were tubular in 3 patients, lobular in 2, mucinous in 2, papillary in 1, mixed tubular and lobular in 1, mixed ductal and lobular in 1 and invasive ductal carcinoma of no special type in the remaining 37 patients. Patients were scheduled to undergo excision of the primary tumour with axillary node sampling to level II, which is the usual surgical protocol for women with small primary breast cancers in our institution. All patients underwent MRI prior to surgery. The age range of patients was 50–87 years (mean 63 years). All patients gave informed consent and the study was approved by the Joint Ethical Committee of our institutions.

Imaging protocol
Patients were imaged in the supine position using a Siemens Magnetom Impact system (Erlangen, Germany) operating at 0.95 T. A large, flexible, receive-only surface coil was wrapped around the outer aspect of the upper arm to include the axilla ipsilateral to the primary breast tumour. A surface coil was chosen owing to superior signal-to-noise ratio, allowing greater spatial and temporal resolution than could have been achieved with the body coil. Prior to imaging, an intravenous cannula and long line flushed with saline were inserted to avoid patient movement during injection of Gd.

Details of the imaging parameters are shown in Table 1Go. Prior to injection of Gd, a multislice coronal T1 weighted (T1W) fast spin echo (FSE) sequence (echo train length=3) was performed to provide anatomical orientation. A three-dimensional T1W fast low angle shot (FLASH) sequence was then acquired in 44 s, covering the whole of the axilla in an oblique sagittal plane. This plane was chosen to optimize coverage of the axilla with the number of slices available for the given acquisition time. The T1W FLASH sequence was then repeated 10 times as a dynamic series, with injection of Gd (0.1 mmol kg-1) (Magnevist; Schering AG, Berlin, Germany) into a contralateral arm vein at the start of the third acquisition. This protocol was chosen based on a previously described protocol for dynamic Gd enhanced MRI of the breast [12]. Following the dynamic sequences, a further coronal T1W FSE sequence was acquired post Gd. The total imaging time, including localizing sequences, was less than 20 min.


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  		Table 1. Sequence parameters

 
Image processing
Following imaging, data were transferred to a Sun SPARC workstation (Sun Microsystems Inc., Mountain View, CA). All post processing and manipulation was done using MAPS 10,000 image processing software (Link Medical Ltd., Guildford, UK). A single, blinded, experienced observer examined each data set for lymph nodes. Each slice of interest was then viewed during the dynamic acquisition period as a cine loop to identify enhancing nodes and to assess any patient movement. Regions of interest (ROIs) were drawn around every enhancing node identified and around a region of homogeneous adjacent fat (see Figure 1bGo). The mean signal intensity within these ROIs was calculated for the first and fourth frames of the dynamic series. Two enhancement indices, (En and Ef), were then calculated for each enhancing node using Equations 1 and 2GoGo:






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  		Figure 1. (a) Oblique sagittal T1 weighted fast low angle shot (T1W FLASH) image of an axilla containing several metastatic lymph nodes (arrows) before gadopentetate dimeglumine (Gd). (b) Oblique sagittal T1W FLASH image in the same position as (a) after Gd, showing enhancement in several enlarged lymph nodes (arrows). Regions of interest have been drawn around an enhancing node and an adjacent area of fat (arrowheads).

 
where Sn1 is the mean signal in a lymph node in frame 1 of the dynamic series, Sn4 is the mean signal in the lymph node in frame 4, Sf1 is the mean signal in an adjacent area of fat in frame 1 and Sf4 is the mean signal in the adjacent area of fat in frame 4. En is the signal change in an enhancing node expressed as a ratio of the baseline signal intensity and Ef is the signal change in an enhancing node normalized to the signal in an adjacent area of axillary fat. These two indices were chosen based on previous work on MR detection of recurrent breast cancer [12]. For each enhancing lymph node, a separate, immediately adjacent ROI of fat of constant area was defined. This procedure was repeated for all enhancing lymph nodes in all patients. The maximum cross-sectional area A in the oblique sagittal plane was also recorded for each node analysed. Although the number of positive axillary lymph nodes in any one patient may be inversely related to the duration of disease-free survival [13], in practice a single lymph node containing metastatic tumour is sufficient to categorize a patient as "axillary node positive" and therefore alter subsequent management. Thus, only the maximum values of En and Ef for each patient are considered.

Pathological analysis
The histopathological technique employed involved bisection of small lymph nodes or 2 mm macrosection of larger nodes. Samples were stained with haematoxylin and eosin, embedded in paraffin and 5 µm slices mounted on slides. In samples from women with primary lobular carcinoma, additional immunocytochemical staining for cytokeratin was employed using a broad spectrum antibody (CAM 5.2, Becton Dickinson: catalogue number 349205).


   Results
Top
 Abstract
 Introduction
 Materials and methods
 Results
Discussion
 References
 
All 47 patients completed their MRI study satisfactorily. The mean number of nodes removed from each patient at surgical axillary sampling was 8 (range 3–14). A total of 24 positive nodes was identified in 10 patients, ranging from 1–10 nodes per patient. In one of the "node positive" patients, a single micrometastasis (<2 mm) was detected in one node only. The remaining 37 patients had no evidence of nodal disease. Figures 1a,b and 2a,bGoGo show examples of positive and negative axillary MRI studies, respectively. In both figures, part (a) is an oblique sagittal image before Gd and part (b) is the same image post Gd. ROIs have been drawn around an enhancing node and an adjacent area of fat in Figure 1bGo.



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  		Figure 2. (a) Oblique sagittal T1 weighted fast low angle shot (T1W FLASH) image of a normal axilla before gadopentetate dimeglumine (Gd). (b) Oblique sagittal T1W FLASH image in the same position as (a) after Gd. There are two small lymph nodes (arrows) which were normal histopathologically.

 
The distributions of En and Ef values for women with negative and positive nodal histopathology are shown in Figures 3 and 4GoGo. Similarly, the distribution of the largest nodal cross-sectional area A for both groups is given in Figure 5Go. Table 2Go shows the mean values of En, Ef and A for both histopathological groups as well as a statistical comparison between the groups using an unpaired t-test. There is a significant difference between the values of Ef and A for the two histopathological groups, but no difference for En. However, the results for nodal area are skewed somewhat by two uncharacteristically large nodes that were more than three times the size of the next largest node.



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  		Figure 3. A plot of maximal nodal enhancement ratio En for each patient.

 


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  		Figure 4. A plot of maximal node/fat ratio Ef for each patient.

 


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  		Figure 5. A plot of the largest node area A (cm2) for each patient.

 

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  		Table 2. Mean (and standard deviation) enhancement indices En and Ef and mean area A for the histopathologically positive and negative groups

 
These results indicate that, in general, patients who are "axillary node positive" have larger nodes that enhance more following Gd. The usefulness of such an examination depends on the definition of a threshold of significance of some measurement and then calculation of the sensitivity and specificity of the technique. Taking thresholds of Ef<21% and A<0.4 cm2 as the obvious cut-offs in Figures 4 and 5GoGo, the sensitivity, specificity, positive predictive value, negative predictive value and precision can be calculated and are shown in Table 3Go.


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  		Table 3. Discriminatory performance measures of the technique using thresholds of significance of Ef<21% and A<0.4 cm2

 
Assessment of any technique is task dependent, that is the usefulness of an examination is defined in terms of the discriminatory function you wish to perform. If the task is to identify women with axillary metastases, then this method performs poorly with such low specificity. However, if the task is to exclude axillary metastases with a high degree of confidence, this method performs very well.

A more complete way to describe the relationship between sensitivity and specificity is to plot a receiver operating characteristic (ROC) curve. ROC curves for Ef and A are shown in Figure 6Go. These curves were produced using a continuous ROC approach [14]. A common figure of merit in ROC analysis is the area under the curve, and these areas are also shown for Ef and A in Figure 6Go. A simple way of combining Ef and A into a diagnostic strategy is to consider only those nodes above a certain size as potentially positive and to consider those axillae with no nodes above this size as negative. Using an area A threshold of 0.4 cm2 and plotting a continuous ROC curve as before, we can see an improved performance when compared with using Ef or A alone. The ROC curves were compared using a univariate z-score between the two curves at a true positive fraction of 0.1 [15]. The results show a significant difference comparing the combined Ef and A curve with both the Ef and the A ROC curves (p=0.045 and p=0.035, respectively), but not between the Ef and the A curves (p=0.29). Using this combined Ef and A approach, true negatives could have been predicted in 20 (54%) of the 37 women with no histopathological evidence of axillary metastases.



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  		Figure 6. Receiver operating characteristic (ROC) curves for the various diagnostic approaches. The dotted line is the ROC curve for nodal area A<0.4 cm2; the grey line is the ROC curve for maximal node/fat ratio Ef<21%; and the upper bold line is the ROC curve for A<0.4 cm2 and Ef<21% combined. AUC, area under curve.

 

   Discussion
Top
 Abstract
 Introduction
 Materials and methods
 Results
 Discussion
References
 
This study shows that Gd enhanced MRI can reliably exclude axillary lymph node metastases in more than one-half of women with negative nodes pathologically. The protocol employed, with its relatively short imaging time in the supine position, was well tolerated by patients. Many different methods of quantifying enhancement in breast lesions have been described [6, 8, 11, 12, 16–22]. Normalizing signal change to fat has been shown to be superior to signal change ratio [23]. Owing to inhomogeneity of fat signal in the axilla, in this study a separate ROI of fat adjacent to each individual node was chosen for calculation of Ef. Regardless of the method chosen, any post processing has the inevitable disadvantage of being time consuming.

The principal disadvantage of the technique was respiratory motion artefact during the dynamic series, as has been found in another MR study of axillary nodes using ultrasmall particulate iron oxide contrast [24]. This meant that a potential problem was spurious enhancement of small lymph nodes owing to movement out of the imaging plane and replacement with high signal fat. Careful examination of adjacent slices was required to avoid such misinterpretation, but some loss of contrast resolution is inevitable with 4 mm slice thickness owing to signal averaging. This could be minimized by reducing slice thickness for the dynamic acquisition and improving spatial resolution, but this results in an inevitable reduction of temporal resolution for the same anatomic coverage. This problem will decline as more sophisticated MR systems become available. The number of dynamic acquisitions could be reduced from 10 to 3 without any loss of information, as maximum enhancement occurred during the first or second post-contrast sequence. No patients showed late nodal enhancement.

Normal axillary lymph nodes vary in size from 1–10 mm. They are anatomically classified into five groups: lateral, 4–6 nodes lying medial and posterior to the axillary vein; anterior, 4–5 nodes inferior to the lower margin of the pectoralis minor; posterior, 6–7 nodes in the inferior margin of the posterior axillary wall; central, 3–4 nodes lying posterior to the pectoralis minor; and apical, 1–12 nodes superior to the upper margin of the pectoralis minor. Surgically, nodes are classified as level I, corresponding to the anterior group; level II, corresponding to the central group; and level III, corresponding to the apical group. We did not attempt to match nodes identified on MR with nodes removed at axillary surgery owing to loss of anatomical landmarks in excised tissue. Rather, each was considered as a "stand alone" technique that was either negative or positive for each patient. Although it would be desirable to correlate the MR characteristics of each node with the histopathological results, in practice this is virtually impossible.

MRI of the axilla will not demonstrate metastases to internal mammary nodes. However, this is not relevant because no attempt is made to stage internal mammary nodes in normal practice, as the morbidity associated with surgical dissection of these is too great to justify any advantage gained from improved staging [25].

Surgical staging of the axilla depends upon the histopathological technique employed for examination of the excised nodes. Use of fine sectioning of nodes and immunocytochemical techniques may increase the diagnosis of occult axillary node metastases in up to 41% of those diagnosed as being axillary node negative using standard techniques [26]. Such occult metastases are most likely to be found in women with lobular carcinoma and in women less than 50 years of age. However, the significance of such occult metastases or of micrometastases (<2 mm diameter) is not clear. Some studies show no difference in survival [13, 27, 28], while others claim reduced disease-free survival [26, 29–31] or reduced overall survival on prolonged follow-up in such patients [32–34]. However, while micrometastases possibly affect long-term survival, there is great debate about whether their presence should alter patient management [35]. The one patient in this study with a single micrometastasis had a positive MR study. Although the histopathological size of this micrometastasis was <2 mm, the node in which it was present was enlarged.

A previous study has shown no correlation between axillary lymph node size and the presence of metastases [10], and a recent publication, which showed good sensitivity and specificity for Gd enhanced MRI, did not find a correlation with the presence of nodal metastases with increased size [36]. However, neither of these studies examined the negative predictive value of small nodal size that was found in this study.

A variety of methods have been used to stage the axilla. Clinical examination and mammography are inaccurate [37, 38]. Similarly, ultrasound and CT have insufficient sensitivity and negative predictive values [39–41] to replace surgical staging. Scintimammography using 99Tcm sestamibi has shown moderately high negative predictive values (82–87%) in excluding axillary node metastases [42, 43]. The most promising techniques for axillary staging recently have been positron emission tomography using 18F-fluorodeoxyglucose [44–46], scintigraphy using combined monoclonal antibodies labelled with 123I [47], and sentinel node lymphoscintigraphy with lymphadenectomy [48–51]. The last method is, of course, not non-invasive but replaces axillary node dissection with minimally invasive excision of a single lymph node that can be performed under local anaesthesia. A future strategy for staging the axilla in women with small breast cancers might include dynamic Gd enhanced MRI to exclude a proportion of those with negative nodes, followed by sentinel lymphadenectomy in those with a positive MRI study.

This study has shown that dynamic Gd enhanced MRI is a feasible method of non-invasively identifying a significant proportion of women with breast cancer who are axillary node negative. This is particularly relevant to the breast screening population who have smaller cancers and are less likely to have axillary metastases. There were no false negatives in this study, therefore axillary surgery with its associated morbidity and cost could potentially be avoided in those with a negative MRI examination.


   Acknowledgments
 
Dr Jason A Brookes died in a tragic climbing accident on 17th January 2000.


   Footnotes
 
This study was supported by funding from Aberdeen Royal Hospitals Endowments Trust and a Pump Priming Grant from the Royal College of Radiologists, London, UK. Back

Received for publication July 30, 2001. Revision received October 25, 2001. Accepted for publication November 6, 2001.


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 Abstract
 Introduction
 Materials and methods
 Results
 Discussion
 References
 

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H. Abe, R. A. Schmidt, K. Kulkarni, C. A. Sennett, J. S. Mueller, and G. M. Newstead
Axillary Lymph Nodes Suspicious for Breast Cancer Metastasis: Sampling with US-guided 14-Gauge Core-Needle Biopsy--Clinical Experience in 100 Patients
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