10.1245/s10434-006-9019-7
Annals of Surgical Oncology 14:3-13 (2007)
© 2007 Society of Surgical Oncology
Positron Emission Tomography (PET) and Mammography (PEM) for Breast Cancer: Importance to Surgeons
Lorraine Tafra, MD
The Breast Center, Anne Arundel Medical Center, 2002 Medical Parkway, Suite 120, Annapolis, MD 21401, USA
Correspondence: Address correspondence and reprint requests to: Lorraine Tafra, MD; E-mail: ltafra{at}aahs.org
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INTRODUCTION
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The unique aspect of positron emission tomography (PET) is the ability of the image to represent the physiology or metabolism of the area of interest as opposed to just its anatomic appearance. Malignancies frequently function at a higher metabolic rate than normal tissue and therefore concentrate [F-18]-fluorodeoxyglucose (FDG, the most commonly used intravenous agent) to a higher degree than normal tissue.
Use of PET for the evaluation of breast cancer was initiated with a study published in 1989 evaluating 17 breast cancer patients with advanced disease.1 The patients’ primary tumors (all greater than 5 cm), axillary, liver, and bone metastases were well-visualized, and this spawned a series of studies to determine the usefulness of this technology in patients at various stages of disease. The initial trials were limited, secondary to selection bias (patients chosen with large tumors and advanced disease), and only in more recent studies has the actual accuracy of PET for the evaluation of breast disease been determined.
Fifteen years of evaluation has shown that most of its usefulness rests in the evaluation of patients with either an advanced breast cancer and/or those presenting with a recurrent breast cancer. As of October 1, 2002, the Centers for Medicare and Medicaid Services approved FDG PET for the staging of patients with distant disease, restaging for patients with locoregional recurrence or metastases, and for monitoring therapy. Although it has not been specifically approved for the initial diagnosis of breast cancer or for staging the axilla, it can be useful in patients with an advanced primary.
Although the sensitivity of whole-body PET is not very high, it is quite specific for the detection of metastatic disease. This has made the technology useful in patients with poor prognostic findings, such as numerous involved lymph nodes or local regional recurrence. The few number of false positives are secondary to inflammation, and infrequently, fibrocystic change and lactation.2,3 Despite the limited sensitivity, PET is important, as it better enables surgeons to tailor surgical management of these advanced disease patients who frequently have to balance aggressive treatment with limited survival and quality of life.
The development of newer technology that allows imaging specifically isolated to the breast, now referred to as positron emission mammography (PEM), has also been introduced. This technology has the potential for resolution down to 1.8 mm and had its origins in a device known as a microPET (a small animal PET scanner used for oncology research).4 PEM is now being investigated in clinical trials at a number of sites to determine its sensitivity and specificity, and initial results are discussed below.
A summary of the various aspects of PET imaging important for the surgeon caring for patients with breast disease is presented in this review. The specific topics will focus on 1) the technique of PET and use of SUVs (peak standard uptake values); 2) patients with newly diagnosed primary breast cancer; 3) newly diagnosed patients with advanced tumors or those receiving neoadjuvant chemotherapy; and 4) breast cancer patients presenting with a local or distant recurrence. Table 1
is an overview of recommendations for each clinical setting. The final discussions will include PEM imaging, and a review of the very limited, but promising, investigative work using PET technology.
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TECHNIQUE OF PET AND USE OF SUVS
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The technique of PET usually consists of fasting the patient 4–6 hours prior to scanning, determining a normal glucose level prior to scanning, using an injection site opposite the involved breast, and waiting 45–60 minutes after injection prior to scanning. The typical dose of FDG used ranges from 10–20 mCi (370–740 mBq), and whole-body scanning typically takes 45–60 minutes. Normal breast tissue will have some diffuse mild FDG uptake, particularly in glandular tissue, in patients taking hormone replacement therapy, and around breast implants. FDG activity in the milk of lactating women is low and, with a half-life of 110 minutes, poses no risk to the infant 24 hours following PET imaging of the breast-feeding mother.
As a component of the technology, PET scanning also has the ability to quantify the differential uptake of FDG. Peak standardized uptake values or "SUVs" are used to determine, in a quantitative fashion, the uptake of FDG into the area of interest. This measurement, which takes into account the injected dose and the patient’s weight, has been investigated for its potential to provide prognostic information on primary breast tumors. Theoretically, the more uptake of FDG into a tumor, the more aggressive the tumor and, therefore, the worse the prognosis. There is, however, variability in SUVs secondary to the length of the uptake phase of FDG, equipment differences, tumor geometry, plasma glucose levels, body habitus, and methods of reconstruction and attenuation correction.5 Most studies show some correlation, as would be expected, to histological grade and indices of cellular proliferation. SUVs do not appear to correlate with microvessel density, ER/PR status, axillary node status, or tumor size.6–8 At least one study has found worse relapse-free and overall survival in patients with a high FDG uptake compared to patients with low FDG uptake.9
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PET IMAGING AND PRIMARY BREAST TUMORS
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The initial reported series of PET for breast cancer in the 1990s was very promising. With larger series, however, it became clear that the low sensitivity did not allow the detection of small breast tumors. In addition to tumors smaller than 1 cm, PET is not sensitive for well-differentiated tumors or infiltrating lobular tumors. The best reported PET sensitivity of 1 cm tumors or less is reported to be 57%.8 Figures 1 and 2 show examples of PET in patients with a primary breast malignancy.
In addition, there has been significant variability of the uptake in primary breast tumors contributing to a high false negative rate. There is some speculation that the variability may be secondary to vascular characteristics of the tumor,10 specifically the vascular density and integrity. It is well-known that the biological aggressiveness of breast tumors can vary widely, and it is probably a complex combination of factors that contribute to the lack of consistent imaging of breast primaries. One study has noted a polymorphism in the gene for the vascular endothelial growth factor (VEGF), and these polymorphisms had an impact on uptake in breast cancer patients.11
To get around this variability, which leads to false negatives, investigators have attempted to use other labeled agents; however, it is doubtful that the resolution of the current technology will get lower than 1 cm. For this reason, there is no role for PET imaging in the screening evaluation for breast disease, as conventional mammography is more sensitive and does not require lengthy imaging time.
It was initially hoped that PET could predict the status of axillary lymph nodes and potentially spare patients an unnecessary axillary node dissection. During the introduction of PET, sentinel node biopsy emerged as the diagnostic procedure of choice for staging the axilla. There are now multiple multicenter trials showing a low false-negative rate, and the recommended management of the axilla can include performance of sentinel node biopsy on a routine basis. The sensitivity of PET for predicting the presence of disease in axillary lymph nodes12 in more recent studies has been consistently low (28–32%) compared to sentinel node biopsy. Although the positive predictive value of PET for axillary lymph nodes is quite high (87–90%),13–15 it is infrequently used for the evaluation of patients presenting with a primary tumor unless it is large and there is a high suspicion of distant metastatic disease (see Figs. 3, 4 and 5). It is unlikely that PET, given its current resolution capabilities, will ever be able to detect micrometastatic disease. The presence of a positive axilla on PET is helpful in sparing the patient the step of sentinel node biopsy and allowing for a completion axillary lymph node dissection as the initial management of the axilla. If the positive axilla on PET is an unexpected finding, it is not unreasonable to first perform an US-guided biopsy of the suspicious lymph node to confirm the presence of disease.
The usefulness of PET for the evaluation of internal mammary lymph nodes is not as clear. This is partially due to the lack of biopsy-proven pathology on suspicious findings. Figure 6 depicts a positive PET scan for internal mammary metastases. In one small study, 7 of 28 patients (25%) were found to have suspicious disease in the internal mammary lymph node basin and this correlated with poor prognosis.16 In the majority of these patients who have suspicious internal mammary lymph nodes on PET, the prognosis is already quite poor, so this additional information is of questionable benefit. Although it does provide better sensitivity, compared to conventional CT scanning,17 it remains to be determined whether radiation therapy, or other forms of local therapy, could improve survival or quality of life.
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FIG. 6. a Whole-body PET showing highly suspicious internal mammary lymph nodes in a breast cancer patient with a positive axillary lymph node. b CT images of the internal mammary lymph node.
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PET AND NEOADJUVANT CHEMOTHERAPY
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In patients who have elected or require preoperative chemotherapy, the ability to determine the extent of ongoing pathological response can be an important component of their care. PET can assist in determining the overall prognosis of the patient, tailoring chemotherapy in poor responders, and determining the appropriate surgical care. No modality, including physical exam, mammography, US, MRI, or PET, has been shown to be perfectly accurate in this setting: the persistence of a tumor mass on examination may represent fibrotic scar and not viable tumor, and the resolution of a tumor mass does not guarantee the absence of diffuse microscopic disease.
The sensitivity (80–90%) and specificity (50–80%) of PET’s ability to predict the pathological response varies with the definition of "response" or decreased FDG uptake.18,19 These definitions vary from center to center, and few studies have correlated the outcomes or survival data with the definitions. It does appear that PET can frequently determine an early response before other forms of imaging. It has been noted in the literature that there is a clinical need for standardized methodologies to establish firm cut-off values for discriminating between responders and nonresponders. PET is most informative if serial imaging is performed, but this is rather expensive and involves significant radiation exposure. PET will still occasionally miss large amounts of disease in patients receiving chemotherapy. This is speculated to be secondary to chemoresistance in the remaining tumor cells that take up less FDG than chemosensitive cells.
Both PET and MRI have been used to monitor response, and in at least one study the two modalities were found to complement each other: PET correctly predicted lack of pathologic response in five of six cases (83%); clinical breast exam and MRI predicted correctly in only 0–17%. When PET predicted response, MRI defined the extent of macroscopic pathologic residual disease accurately in nine of ten cases (90%). When post-therapy MRI showed complete response (CR) in eight cases, macroscopic pathologic complete response was observed in all eight cases (100%).7 The most cost-effective and safe approach may lie in combination imaging.
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BREAST CANCER PATIENTS WITH A RECURRENCE
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An important contribution of PET is the ability to detect distant metastatic disease in patients with a local or symptomatic distant metastasis. Between 16% and 30% of patients with a locoregional recurrence are diagnosed with PET as having distant metastases,15,20–23 and an additional 24% are found to develop a site of distant disease within 18 months of having a breast cancer recurrence.15,21 In addition, the management of a large number of patients (45% of 134 patients suspected of having a recurrence) is changed based on PET findings.24 The impact of PET on the subsequent choice of surgical options is significant and should be considered in any surgical patient presenting with a breast recurrence. Figures 7 and 8 show examples of recurrent breast cancer.
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FIG. 7. a–b. Patient with widespread unresectable metastatic breast cancer and repeat PET after three months of chemotherapy showing a partial response.
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Despite PET’s importance in the management of breast cancer patients with a recurrence, it alone, for the detection of metastatic disease, is probably not sufficient to find all sites of disease. For instance, bony metastases are the most common site for metastatic disease of the breast, but the current data indicate that PET may compliment bone scans; each detects aspects of bone metastases that the other cannot.8 Complimentary imaging of MRI and PET was also found to be beneficial in reducing the rate that a subsequent biopsy is required from greater than 50% to 17%.25
Prior to the use of PET imaging, most patients with a recurrent breast cancer were evaluated with brain MRI, a bone scan and a CT of the chest, pelvis and abdomen. PET, in studies comparing it to these standard anatomic imaging, has a higher sensitivity and specificity, especially for mediastinal, pulmonary, and liver metastases.12 The fusion of PET with CT scanning may provide the most accurate detection rate, in one study detecting 96% of the lesions. PET/ CT scanning, the technology of which is becoming more widespread, can make up for the lack of anatomical landmarks on PET functional imaging. It has been found to be superior to PET scanning alone in other malignancies, and the same will probably hold true for metastatic breast cancer.26
In a very few, well-selected, patients who are found by PET to have single site metastatic resectable disease (as depicted in Fig. 9), surgical excision may be offered and provide long-term survival. PET is obviously very helpful in planning the surgical procedure,27 as those patients with multiple-site disease are disqualified from aggressive surgical management.
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POSITRON EMISSION MAMMOGRAPHY (PEM)
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PEM technology uses two planar detectors integrated into a conventional mammography system that enables the coregistration of a mammographic and emission FDG image. Thompson et al.28 reported the first feasibility study on PEM technology in 1994 using two detector arrays arranged above and below a phantom breast. The predicted resolution is significantly better than whole-body PET, and currently is considered to be 1.8 mm.
Two groups of investigators working with a number of devices have published on two small pilot trials.29–34 The first report of the device used in patients by Levine et al. provided promising data.35 Eighteen lesions in 16 patients were evaluated by PEM images by drawing a region of interest at the biopsy site and comparing the count density in the region of interest with the background. This study determined a lesion-to-background ratio of >2.5 as a reasonable indicator of malignancy and yielded a sensitivity of 86%, a specificity of 91%, and an overall diagnostic accuracy of 89%.
Similarly, Rosen et al.36 demonstrated 20 focal abnormalities, of which 18 were malignant and two were benign. Both benign lesions represented areas of fat necrosis. The overall sensitivity of PEM for malignancy in this study was also 86% (95% confidence interval: 65%, 95%).
The first multicenter study of PEM was presented at the American Society of Breast Surgeons annual meeting in Los Angeles (2005),37 investigating 44 newly diagnosed breast cancer patients with PEM (Naviscan, Rockville, MD, Fig. 10). True to its hypothetical predictions of resolution, the smallest detectable disease visualized by PEM was a 2 mm duct of DCIS (Fig. 11). Although the technology visualized the majority of the index lesions (87%), it missed five lesions, which ranged in size from a 1 mm DCIS to a 1 cm infiltrating ductal carcinoma. Similar to whole-body PET imaging, it is probable that the variability in the metabolic activity of breast cancer cells will continue to pose a challenge to visualizing every lesion using this technology. Investigations into new agents for use with whole-body PET may also prove, in PEM, to offer a window of further technological improvements.
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FIG. 11. PEM shows a duct of DCIS extension with final pathology confirming the extension of DCIS in one duct in the same area.
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The trial of PEM also looked at the presence of extensive DCIS and was able to accurately predict the majority (75%) of the patients who would probably fail breast conservation. An example of a patient with multifocal disease is shown in Fig. 12. The surgeons in this study were blinded to the results and therefore planned their surgeries according to the data available to them from mammograms, ultrasounds, and in some cases, MRI.
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FIG. 12. PEM image of pathology-confirmed multifocal disease is well-visualized compared to mammography or MRI.
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In spite of advances in breast imaging, the re-excision rate for patients undergoing partial mastectomy in the literature ranges from 4 to as high as 60%, with approximately half of the re-excision specimens demonstrating residual tumor. Frequently, the positive margins are not from invasive tumor but from DCIS. Identifying an imaging device that accurately depicts DCIS has been elusive. If PEM can reliably visualize DCIS, it would be a valuable tool for surgical planning and potentially reduce the rate of re-excision.
The ability to use PEM technology to biopsy lesions38 has also been investigated and appears feasible. This is an important future component of the technology if it is to be useful clinically. In addition, further refinements, including combining PEM with tomographic acquisition (using detectors that rotate about the breast),39 has the potential to improve detection compared with the technology based on stationary detectors.
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THE FUTURE OF PET AND PET IMAGING
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The major developments in the next decade will probably focus on: the use of PET as an in vitro assay of tumor biology and tumor responsiveness; the cost-effective selection of patients for follow-up and evaluation of subclinical disease; and the detection of DCIS using PEM devices.
PET as an In Vitro Assay
The mechanism of FDG uptake in tumors (although probably oversimplified) is that FDG is trapped in the cell, since once phosphorylated (similar to the path taken by glucose), it can neither act as a substrate for enzymatic reactions, or be dephosphorylated to allow transfer across the cell membrane. Ongoing research is aimed at better understanding these mechanisms, and this will hopefully lead towards defining PET’s ability to provide information on tumor biology. The introduction of new agents such as [F-18]-fluoro-L-thymidine (marker for tumor cell proliferation), [F-18]-fluoromisonidazole (a marker for tumor hypoxia) and markers for angiogenesis may provide further insight.9,40–42
The most promising estrogen receptor imaging agent is a close analog of estradiol, estrogen 16
-[F-18]-fluoroestradiol-17ß (FES).4 The rationale behind estrogen receptor imaging is to predict clinical response. Biopsy material from a metastatic lesion may not always reflect the functional status of the ER receptor in all of the lesions and can be fraught with sampling error. The ability to assess the functional state of the entire volume of metastatic disease may assist better tailoring of treatment.8 The ability to synthesize [F18]-labeled Xeloda and other therapies may also improve the ability of the FDG to image important metabolic characteristics of breast malignancies.43
The Use of Whole-Body PET for the Detection of Subclinical Disease
Patients with a large or high-grade primary breast cancer and/or a large number of positive lymph nodes will most probably recur at some point. Attempting to find early recurrence has met with skepticism, as historical studies have not shown improved survival when subclinical disease has been detected and treated. These studies, however, can be criticized for their use of suboptimal imaging techniques, unsophisticated laboratory marker detection techniques, and lack of detailed clinical follow-up. It remains to be determined whether PET imaging of subclinical metastases, combined with more tailored therapy, improves either survival or quality of life.
We are now discovering that the search for subclinical metastatic disease poses significant challenges. Although surgically resecting the disease is a reasonable option, especially if it is an isolated lesion, finding a PET-detected metastatic lesion is not always straightforward. The need for an intraoperative probe that would detect a focus of disease that has FDG activity has been realized and is being investigated.47
It is possible that coupling PET imaging to tumor marker increases or the detection of circulating tumor cells may allow better selection of patients for PET follow-up.17,44 In our ongoing small pilot trial, we are combining PET imaging with a mammoglobin RT-PCR assay for circulating tumor cells. PET has detected subclinical disease in 4 of 30 (13%) patients.45,46
PEM for Detection of DCIS
This technology is in its infancy, but preliminary reports are promising for the detection of DCIS. No imaging device to date has been able to accurately image DCIS unless it happens to be associated with pleomorphic calcifications seen on mammography. Further refinements to the technology are needed, but its potential to detect early breast cancer is significant.
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SUMMARY
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Whole-body PET is useful in breast cancer patients with large tumors or recurrent tumors since it can rule out metastatic disease and help tailor surgical therapy. PEM may detect clinically significant DCIS and small tumors that have not been imaged with MRI, mammography or US, and may also help tailor breast-surgical procedures.
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ACKNOWLEDGMENTS
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I would like to thank Dr. Jack Van Geffen for providing the PET images and Ms. Sharon Mayrgundter for her efforts on manuscript preparation.
Received for publication August 1, 2005.
Accepted for publication May 1, 2006.
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INTRODUCTION
TECHNIQUE OF PET AND...
