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Current recommendations for MRI in the work-up and follow-up of breast cancer.

Introduction

Magnetic resonance imaging (MRI) of the breast is an important tool for the detection, characterisation and diagnostic work-up of breast disease. An understanding of the indications, benefits and potential drawbacks is required in order to optimise the clinical value of this imaging modality. This article will look at the background of breast MRI and describe the technical settings and clinical scenarios where MRI has proven benefit. The main focus of this article is the use of MRI in patients with breast cancer, although other indications will be briefly outlined.

Background

MRI of the breast has been in use since the mid-1980s. Breast cancers demonstrate significant enhancement with standard gadolinium-based contrast agents in comparison with normal breast tissue [1]. During the 1990s, time-intensity curves derived during dynamic contrast-enhanced imaging were shown to be useful in differentiating between benign and malignant lesions [2]. MRI has the highest sensitivity, specificity and positive predictive value for the detection of invasive, as well as non-invasive, cancers [3].

MRI of the breast should be performed in specialised units with experience in conventional breast imaging and image-guided needle biopsy techniques [4]. Centres offering breast MRI should perform at least 150 examinations per year, with the ability to refer onwards for MRI-guided biopsy of the breast where required. Organisations offering MRI-guided biopsy should perform more than 10 per year [4].

Technical considerations

In order to optimise spatial and temporal resolution, MRI of the breast should be performed using a high-field MRI scanner of at least 1.0 Tesla (T), preferably above 1.0T, using a dedicated breast coil [5]. The slice thickness should not exceed 3mm with a pixel resolution of 1mm or less. Good patient positioning is important to avoid motion artefact. Gadolinium contrast enhancement (0.1 mmol/kg) is required in the evaluation or detection of breast cancer but can be omitted in the evaluation of breast implants [6].

Sequences usually include a pre-contrast T1--and T2-weighted sequence, (fast/turbo spin-echo) with or without fat saturation, followed by a T1-weighted dynamic contrast-enhanced acquisition. This must include an initial pre-contrast sequence followed by multiple acquisitions after contrast administration. A fat-suppression technique can improve lesion conspicuity. A subtraction technique during post-processing is required if dynamic fat-suppression techniques are not available.

Timing and hormonal factors

Where possible, premenopausal women should be scanned between day 6 and day 13 of their menstrual cycle so that the background parenchymal enhancement is minimised, thus optimising lesion detection and characterisation [7].

Hormone replacement therapy can also cause an increase in breast tissue perfusion, causing problems with specificity of lesion detection [8]. Postmenopausal women who receive cyclic HRT should where possible be scanned during the postmenstrual phase of their artificial cycle. If HRT can be stopped, a gap of 4 weeks prior to MRI scanning may also improve the specificity of the scan [4].

Interpretation and reporting of breast MRI

In 2003 the American College of Radiology (ACR) Breast Imaging Reporting and Data System Atlas (BI-RADS[R] Atlas) [9] was published. This was to standardise breast MRI reporting, in order to aid clinicians in their understanding of results, and to facilitate scientific research by enabling direct comparison of imaging studies based on standardised MRI terminology.

In the United Kingdom most breast radiologists report according to an adapted version of the BI-RADS lexicon. The reporting radiologists should be experienced in both conventional and MRI breast imaging. Ideally, all relevant imaging (mammograms, ultrasounds and any previous biopsy results) should be available at the time of reporting.

As a minimum standard, the Royal College of Radiologists Breast Group recommends inclusion of the following information in any breast MRI report [10]:

* type of image acquisition;

* description of breast density;

* description of any lesions (type, morphology, three-dimensional size and enhancement pattern);

* a score assigned to give the likelihood of a lesion being benign or malignant, where 1 is normal, 2 benign, 3 probably benign, 4 suspicious of malignancy and 5 malignant.

A standardised reporting template by the NHS Breast Screening Programme [11] is currently out for consultation and its release, expected later this year, will further standardise MRI reporting within the United Kingdom.

Applications of breast MRI

* staging of biopsy-proven breast cancer, in selected patients;

* detection of breast cancer recurrence;

* detection of occult primary breast cancer with biopsy-proven nodal metastases;

* identification of inflammatory breast cancer;

* monitoring response to neoadjuvant chemotherapy;

* screening of high-risk premenopausal women;

* assessment of breast implants.

Staging of biopsy-proven breast cancer

The aim of pre-operative MRI in patients with a recent cancer diagnosis is to accurately assess disease extent in the ipsilateral breast and to exclude malignancy in the contralateral breast.

Several studies have shown MRI to be more sensitive than conventional imaging in assessment of tumour size and detection of occult multicentric/multifocal disease [12]. Whether this additional sensitivity confers any overall benefit to the majority of women with newly diagnosed breast cancer is debatable, and conflicting evidence remains.

Pre-operative MRI has been reported to change the surgical plan in approximately 12-32% of patients, usually to more extensive surgery [13,14]. Houssami et al. reported a rate of conversion from breast-conservation surgery to mastectomy of 8.1 %, and conversion of local excision to more extensive surgery in 11.3%. Subsequent pathologic examination did not identify any additional disease in 13.6% of the mastectomy group and in 52% of the local excision group [13].

The recent COMICE trial (Comparative effectiveness of MRI in breast cancer) [15] concluded that addition of MRI to triple assessment offers no benefit as regards reducing the re-operation rate. This trial prospectively studied 1623 women suitable for breast-conservation surgery between 2002 and 2007 and randomised them between a pre-operative MRI and no pre-operative MRI. The primary endpoint was the re-operation or mastectomy rate within 6 months. The results showed no significant difference between the two groups, which both had a re-operation rate of approximately 19%. Interestingly, COMICE also reported a lower-than-expected rate of contralateral disease (1.6% versus 4% in other studies [16]) and conversion to mastectomy in 27.6% of patients without any confirmation of disease extent by image-guided needle biopsy--and these findings have been used to question the overall robustness of the study.

Two retrospective, non-randomised studies have investigated patient outcome after pre-operative MRI, and have reported conflicting results. Fischer et al. in 2004 [17] reported a reduced rate of ipsilateral recurrence following MRI with no increase in the mastectomy rate, while Solin et al. in 2008 [18] reported no significant difference in recurrence rates between the MRI group and the non-MRI group.

Current evidence, therefore, does not support the use of routine pre-operative MRI for all patients with newly diagnosed breast cancer. There is likely to be benefit, however, in the following selected groups:

(a) Patients with newly diagnosed lobular carcinoma: research has shown some benefit from pre-operative MRI in this sub-group. In a study by Mann et al., surgical management was correctly altered in 28% of cases. There was a reduced rate of re-excision without a corresponding increase in the rate of mastectomy. Detection of additional occult ipsilateral lesions was reported in 32% of patients, and contralateral lesions in 7% [19].

(b) High-risk women who have already developed breast cancer: since these patients have a disproportionately high rate of multifocality and multicentricity [20].

(c) Patients who have a discrepancy of >1cm in tumour extent between mammography and ultrasonography [21].

This has led to similar recommendations by NICE (2009) [22], and the European Society of Mastology (EUSOMA) (2010) [4], in the utilisation of pre-operative MRI (Panels 1 and 2). EUSOMA further acknowledges the potential pitfalls of pre-operative MRI and recommends that:

(a) Patients being considered for pre-operative MRI should receive counselling concerning potential risks and benefits of further imaging.

(b) MRI findings which alter patient treatment should always be confirmed by percutaneous biopsy. Additionally, any management changes should be discussed and documented at a multidisciplinary team meeting (MDT).

(c) The total treatment delay caused by pre-operative MRI should not exceed 1 month.

MRI in recurrent breast cancer

MRI is not indicated in the routine follow-up of breast cancer as most relapses are either detected clinically or by conventional breast imaging. In cases where there is difficulty in distinguishing between surgical scarring and recurrent disease, MRI is of value. The majority of scars more than 6 months old do not enhance significantly, while all malignancies will generally show enhancement [23]. MRI in the post-surgical patient has a reported sensitivityof around 94%, specificityof approximately90%, positive predictive value of 62.5% and negative predictive value of 98.8% [23] for differentiating between scar and recurrent disease.

The addition of diffusion-weighted imaging in this clinical context has been shown further to improve the specificity and positive predictive value to 92.3% and 81.3% respectively [24].

MRI in occult primary breast cancer

The detection of a primary breast tumour in patients who have localised (axillary) metastatic disease has significant implications regarding treatment. It may enable targeted breast-conservation surgery to take place, avoiding blind quadrantectomy or mastectomy with or without axillary dissection surgery.

A recent review article by de Bresser et al. [25] looked at eight retrospective studies on breast MRI in occult primary breast cancer. It concluded that breast MRI should be routinely offered to patients with occult breast cancer as it can identify the primary tumour in approximately two-thirds of patients and may alter locoregional treatment. Breast-conserving surgery may be a possibility in approximately one-third of patients.

As with any other MRI-detected lesions, histological confirmation is required prior to any management decisions being made.

Inflammatory breast cancer

Inflammatory breast cancer (IBC) accounts for about 1-4% of all breast cancer cases and has a tendency to metastasise at an early stage, resulting in a poor prognosis [26,27]. Despite advances in imaging techniques and improved experience, it remains a challenge to distinguish IBC from acute mastitis (AM) as there is considerable overlap between the clinical manifestations and imaging characteristics of these two diseases.

Typical clinical manifestations for both IBC and AM are enlargement, tenderness, increased cutaneous temperature and dermal redness of the involved breast.

Both diseases present with non-specific features on conventional imaging, such as a focal or diffuse asymmetric density on mammography and ill-defined hypoechoic focal masses on ultrasound [28,29].

Several studies have looked at the added benefit of MRI in differentiating between IBC and AM, and most authors again report a large overlap of MRI morphologic and dynamic features [30-33].

One large retrospective study by Renz et al. [34], comparing 48 IBCs with 42 cases of AM, reported similar features of overlap between the two entities on contrast-enhanced MRI, but statistically significant differences on dynamic sequences. Despite these findings, discrimination between AM and IBC remains a diagnostic challenge.

The current consensus regarding the use of breast MRI in inflammatory carcinoma of the breast is for its use in selected cases where doubt exists about the presence of an underlying breast cancer following treatment of AM [4].

Monitoring response to neoadjuvant chemotherapy

Neoadjuvant chemotherapy (NAC) is a management option for locally advanced breast cancer. The goal of NAC is to reduce tumour volume for the purpose of local surgery, preferably breast conservation. Patient selection for NAC is usually decided at an MDT and generally includes:

* inoperable breast tumours at initial presentation (for example, those which are invading chest wall, skin, or pectoralis muscle);

* large, inoperable breast tumours (stage IIa, IIb, IIIa) not amenable to primary breast-conservation surgery.

The accurate assessment of residual tumour after NAC is a crucial prognostic factor for determining outcome and likely survival of the patient [35].

A number of studies evaluating the capability of contrast-enhanced MRI for monitoring response to chemotherapy have been conducted [36-38].

Although these have shown contrast-enhanced MRI to be superior to conventional breast imaging techniques in determining residual tumour volume, there were varying degrees of false-positive and false-negative rates reported [39-41].

A recent study by Woodhams et al. looked at 69 patients (70 lesions) treated by using NAC and followed up for residual disease with diffusion-weighted (DW) and contrast-enhanced MRI. Results were compared with the postoperative histopathologic findings. They reported a sensitivity of 93% and a specificity of 56% for dynamic contrast-enhanced MRI imaging; and a sensitivity of 97% and a specificity of 89% for diffusion-weighted sequences in the detection of residual breast cancer after NAC [42].

MRI provides better monitoring of response to NAC than conventional breast imaging, particularly for mass lesions. The reported rate of false negatives is higher for areas of non-mass-like enhancement [43] and for tumours showing non-concentric or dendritic shrinkage and those fragmented into multiple foci [44] following NAC.

MRI in patients who are candidates for NAC should be performed prior to their first course of chemotherapy where possible. Repeat MRI should be performed within 2 weeks of completion of NAC. Lesions should be measured and compared with the baseline scan according to the 2008 revised RECIST criteria [45].

Screening

Risk factors for breast cancer include increased mammographic density [46], previous breast cancer [47], a family history of breast cancer [48], genetic mutations; BRCA1 /BRCA2 [49], TP53 (Li-Fraumeni Syndrome) and PTEN Cowden and Bannayan-Riley-Ruvalcaba syndromes [50], a biopsy-proven diagnosis of atypia [51], lobular carcinoma in situ [52], radial scar [53] and previous mantle radiation for Hodgkin's disease (HD) [54,55].

The higher sensitivity of MRI [56], particularly in dense breast tissue, makes it a desirable technique for screening purposes; unfortunately, the lower specificity is a significant problem in terms of time, cost and additional patient anxiety [57].

Recommendations for the use of breast MRI as a screening tool based on the American Cancer Society (ACS) guidelines and the consensus opinion of the EUSOMA working groups are as follows:

Annual MRI should be offered to:

* patients with a proven BRCA mutation;

* first-degree relatives of a BRCA gene carrier who are as yet untested;

* patients with a lifetime risk of 20-25% or greater, as defined by a recognised family history model such as BRCAPRO [58];

* patients who have had previous mantle radiation for HD between the ages of 10 and 30 years, screening starting 8 years after their treatment;

* patients with Li-Fraumeni syndrome (TP53 gene mutation) and their first-degree relatives;

* patients with PTEN Cowden and Bannayan-Riley-Ruvalcaba syndromes (PTEN gene mutation) and their first-degree relatives.

Apart from the HD group, there is no clear guidance as to when screening should begin. Some experts have suggested 5 to 10 years before the earliest previous breast cancer in the family [59], while other studies suggest age 30 [60]. In the UK, MRI breast screening protocols are in the process of being finalised and will be conducted by the NHS Breast Screening Programme.

Breast implant assessment

The use of MRI in this clinical context is beyond the scope of this article. However, breast augmentation and breast reconstruction--either immediate or delayed--have become increasingly common operations. It is important therefore that breast radiologists are able to recognise the normal appearances of the more commonly used implants. MRI is particularly useful in the evaluation of the integrity of silicone breast implants and evaluation of the breast parenchyma in women with silicone gel implants or following free injection of polyacrylamide gel.

The reported sensitivity and specificity of MRI for implant rupture is 80-90% and 90% respectively: this contrasts markedly with mammographic imaging which has a sensitivity of approximately 25% [5].

In patients with breast prostheses, MRI is indicated for:

* patients with signs and symptoms suggestive of implant rupture;

* patients with symptoms of breast disease (for example, breast lump) where conventional imaging is inconclusive or non-diagnostic. MRI is currently not indicated for:

* the routine diagnosis of breast cancer in men;

* equivocal findings on conventional breast imaging where needle biopsy has not yet been performed;

* nipple discharge--except where ductal carcinoma in situ (DCIS) or Paget's disease is suspected or diagnosed in the absence of any conventional imaging abnormality.

Conclusions

Breast MRI is indicated in a number of specific clinical settings. Used incorrectly, breast MRI has the potential to cause significant delays in treatment, unnecessary intervention and/or surgery, increased cost and considerable patient anxiety.

Used appropriately, MRI of the breast has been shown to have several advantages in certain patient groups. These include screening of patients at high risk of breast cancer; pre-operative assessment of selected patients with a new diagnosis of breast cancer; monitoring treatment response to neoadjuvant chemotherapy; and evaluating patients with metastatic axillary carcinoma from an unknown primary. The high sensitivity of MRI can provide early cancer detection with a far greater accuracy than conventional imaging. Ultimately, this has the potential to reduce patient morbidity and mortality.

Careful consideration of the available evidence and strict adherence to imaging recommendations should allow maximal clinical benefit from this imaging resource. Further research is required to evaluate the longer-term advantages offered by MRI, including techniques such as diffusion-weighted imaging and MR spectroscopy in the evaluation of diseases of the breast.

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Panel 1: National Collaborating Centre for Primary Care, 2009 guidance for pre-operative MRI [22]

MRI of the breast should be offered:

* to patients with invasive breast cancer if there is a discrepancy regarding the extent of disease from clinical examination, from mammography, and from ultrasound assessment;

* for planning treatment if breast density precludes accurate mammographic assessment;

* to assess the tumour size if breast-conservation surgery is being considered for invasive lobular cancer.

Panel 2: EUSOMA working group, 2010 recommendations for pre-operative MRI for newly diagnosed breast cancer [4]

Pre-operative MRI is recommended for:

* patients with invasive lobular cancer;

* patients at high risk of breast cancer;

* patients under the age of 60 who have a discrepancy of >1cm between mammographic findings and ultrasonography findings;

* patients eligible for partial breast irradiation on the basis of conventional imaging.

Jennifer O'Brien and William Teh

Imaging Department, Northwick Park Hospital, Harrow, UK

Correspondence to: William Teh

Imaging Department, Northwick Park Hospital

Watford Road

Harrow HA1 3UW, UK

email: william.teh@nhs.net
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Publication:Advances in Breast Cancer
Date:Apr 1, 2010
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