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10.1245/ASO.2006.03.035
Annals of Surgical Oncology 13:677-684 (2006)
© 2006 Society of Surgical Oncology
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Original Article

18F-2-Fluoro-2-Deoxy-D-Glucose Positron Emission Tomography Scanning Affects Surgical Management in Selected Patients With High-Risk, Operable Breast Carcinoma

Elisa Rush Port, MD1, Henry Yeung, MD2, Mithat Gonen, PhD3, Laura Liberman, MD4, James Caravelli, MD4, Patrick Borgen, MD1 and Steven Larson, MD2

1 Department of Surgery, Memorial Sloan-Kettering Cancer Center, 1275 York Avenue, New York, New York 10021
2 Department of Nuclear Medicine, Memorial Sloan-Kettering Cancer Center, 1275 York Avenue, New York, New York 10021
3 Department of Biostatistics, Memorial Sloan-Kettering Cancer Center, 1275 York Avenue, New York, New York 10021
4 Department of Radiology, Memorial Sloan-Kettering Cancer Center, 1275 York Avenue, New York, New York 10021

Correspondence: Address correspondence and reprint requests to: Elisa Rush Port, MD; E-mail: porte{at}mskcc.org.


   ABSTRACT
TOP
 ABSTRACT
INTRODUCTION
 MATERIALS AND METHODS
 RESULTS
 DISCUSSION
 REFERENCES
 
Background: The role of positron emission tomography (PET) scanning in determining the extent of disease in patients with breast cancer has not been defined. We investigated the utility of 18F-2-fluoro-2-deoxy-D-glucose (FDG)-PET scanning compared with conventional imaging with computed tomographic scanning and bone scanning in determining the extent of disease in patients with high-risk, operable breast cancer.

Methods: This was a prospective study of patients who presented to Memorial Sloan-Kettering Cancer Center for operative treatment of breast cancer. Eighty eligible patients were enrolled and underwent computed tomographic chest, abdomen, pelvis, and bone scans, followed by FDG-PET. Changes in treatment based on scan findings were recorded by the operating surgeons. Imaging findings were verified by biopsy or long-term follow-up.

Results: Eight (10%) of 80 patients were found to have metastatic disease that was seen on both conventional imaging and PET. Four additional patients (5%) had additional foci of disease on PET that affected treatment decisions. No patient had findings on conventional imaging alone. Conventional imaging studies resulted in a higher number of findings that generated additional tests and biopsies that ultimately had negative results (17% vs. 5% for PET). There was a statistically significant difference in specificity for PET compared with conventional imaging (P = .01).

Conclusions: Conventional imaging and PET were equally sensitive in detecting metastatic disease in patients with high-risk, operable breast cancer, but PET generated fewer false-positive results. FDG-PET scanning should be further studied in this setting and considered in the preoperative evaluation of selected patients with breast cancer.

Key Words: 18F-2-fluoro-2-deoxy-D-glucose-positron emission tomography • Breast cancer • High risk • Extent of disease


   INTRODUCTION
TOP
 ABSTRACT
 INTRODUCTION
MATERIALS AND METHODS
 RESULTS
 DISCUSSION
 REFERENCES
 
Breast cancer is the most common solid malignancy to affect women in the United States.1 With increased mammographic screening, the detection of earlier, smaller tumors has become more common; ductal carcinoma-in-situ constitutes approximately 25% of all newly diagnosed cases, and the mean tumor size for invasive cancers is decreasing.1 Determining the extent of disease at the time of diagnosis can significantly influence treatment decisions. Patients who have recently received a diagnosis and for whom surgery is planned may be diverted to primary medical treatment if metastatic disease is discovered.

For patients with clinically early-stage disease, the yield of such tests in discovering metastatic disease is extremely low. Puglisi et al.2 demonstrated that when chest radiography, liver ultrasonography, and bone scan were performed as preoperative tests in 516 patients, the yield in detecting metastatic disease was 0% for chest radiography and liver ultrasonography and was 5% for bone scan among stage I and II patients. Similarly, Samant and Ganguly3 showed that preoperative bone scan and liver imaging demonstrated metastatic disease in 1% and 0%, respectively, of patients with early-stage breast cancer. Because of this historically low rate of findings, current National Comprehensive Cancer Network guidelines do not recommend performing extent-of-disease evaluations in asymptomatic patients with stage I and early stage II disease.4 However, these guidelines are not stringent, and practice patterns vary widely.

In patients with larger tumor sizes and clinically positive nodes, the yield of an extent-of-disease evaluation is higher. In the Puglisi study,2 in contrast to patients with early-stage disease, who showed a low incidence of metastatic disease, among patients with stage III disease, 14% had positive bone scans, 6% had positive liver scans, and 7% had positive chest radiographs. However, no specific guidelines exist regarding which screening tests to perform. Because the pattern of metastatic spread of breast cancer includes bone, brain, liver, and lung, evaluation for extent of disease can include one or more of the following tests: bone scan; computed tomographic (CT) scan of the chest, abdomen, and pelvis; chest radiography; liver ultrasonography; liver function tests; and others. Thus, no individual test or combination of tests has been recognized as the standard for evaluating the extent of disease in patients with breast cancer. New imaging technologies may help to refine the process of evaluating for extent of disease in breast cancer and to further clarify appropriate patient selection.

Positron emission tomography (PET) scanning uses 18F-2-fluoro-2-deoxy-D-glucose (FDG), a glucose analogue that is preferentially taken up by tumor cells because of their high metabolic requirement.5 A whole-body scan is then generated that can potentially image a primary tumor, as well as regional and distant metastatic sites.

Previous work in other tumor types, such as lymphoma and esophageal and lung cancers, has led to the incorporation of PET scanning into the standard of care for patients with these malignancies.6–8 The role of PET scanning in patients with breast cancer remains to be fully defined. The purpose of this study was to determine the utility of FDG-PET compared with conventional imaging in evaluating extent of disease and affecting surgical treatment in patients with high-risk, operable breast cancer.


   MATERIALS AND METHODS
TOP
 ABSTRACT
 INTRODUCTION
 MATERIALS AND METHODS
RESULTS
 DISCUSSION
 REFERENCES
 
Patients who presented for operative treatment of breast cancer to the staff surgeons at Memorial Sloan-Kettering Cancer Center (MSKCC) were identified between October 2001 and March 2004 and enrolled in this prospective trial. Participating patients all signed informed consent. To maximize yield from screening tests, patients with "high-risk" disease were identified, and eligibility criteria included a tumor > 5 cm (T3) and/or clinically positive axillary lymph nodes (N1/2). To be eligible, patients must have been operative candidates on the basis of clinical findings, and only patients who intended to undergo treatment at MSKCC were eligible so that scan results could be correlated with pathology findings. Once enrolled, patients underwent CT of the chest, abdomen, and pelvis, as well as bone scanning and PET scanning.

CT scans were performed helically on a General Electric QX/i scanner (GE Medical Systems, Waukesha, WI) by using ≤ 7.5-mm sections after administration of oral and intravenous contrast, unless contraindicated. Scans that were performed at outside facilities but within 1 month of the patient’s entry into the study were considered acceptable. All CT scans were reviewed by a single staff radiologist (J.C.) without knowledge or review of PET or bone scan images or reports.

Bone scans were performed approximately 2 hours after the intravenous injection of 925 MBq (25 mCi) 99mTc methylene-diphosphonate. Whole-body images were acquired in anterior and posterior projections on a dual-head gamma camera (ADAC laboratories, Milpitas, CA).

All PET scans were performed at MSKCC. For each patient, bone and PET scans were reviewed by separate staff nuclear medicine physicians (H.Y. and S.L.). All patients were imaged by using a standard clinical PET protocol: 555 MBq (15 mCi) of FDG was injected intravenously, and images were acquired from the skull base to the upper thighs approximately 45 to 60 minutes afterward. At the beginning of the study, all PET scans were performed with an Advance PET tomograph (GE Medical Systems). Emission and transmission images were each acquired for 4 minutes per bed position. Transmission data were used for attenuation correction in all cases. Beginning in 2002, studies were also acquired on combined PET/CT tomographs: either a Biograph (Siemens/CTI, Knoxville, TN) or Discovery LS (GE Medical Systems). Both machines combine a multislice CT with a state-of-the-art PET tomograph. The CT data were used for attenuation correction. When studies were performed on PET/CT, the interpreting nuclear medicine physician was blinded to CT images and results. For all patients, a mammogram dated within 3 months of presentation was either reviewed or performed by one full-time staff mammographer (L.L.).

All imaging studies were evaluated by the reader by using a five-point scale (Table 1Go), with 4 and 5 categorized as positive results. After completing the imaging studies, patients returned to the treating staff surgeon, who then completed a data sheet describing the findings and operative plan based on CT and bone scan results. Also noted were any findings necessitating further testing or biopsy before proceeding with surgery. The surgeon was then provided with the PET scan results, and changes in the treatment plan based on PET results were documented. Any additional imaging studies required as a result of positive findings were documented, and, when feasible, biopsy was performed of any suspicious lesions. In a few cases in which biopsy was not feasible, suspicious findings were followed up with subsequent repeat scans to document change. In a few cases, findings were considered suspicious enough by the clinician to warrant a change in treatment without verification by biopsy.


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  		TABLE 1. Rating scale for imaging findings
 
The study was designed to enroll 100 patients, which would have provided approximately 80% power to detect a difference of 20% between the accuracy (area under the receiver operating characteristic curve) of PET and CT/bone scan (5% type I error; two-sided). In this study, results relating to sensitivity and specificity are reported; receiver operating characteristic curve analysis will be reported separately.


   RESULTS
TOP
 ABSTRACT
 INTRODUCTION
 MATERIALS AND METHODS
 RESULTS
DISCUSSION
 REFERENCES
 
Ninety-six patients were identified as eligible at presentation. Of these, 16 patients did not complete the study requirements and were therefore deemed ineligible for one of the following reasons: (1) not all screening tests were completed; (2) screening tests were completed but surgery was ultimately performed elsewhere, and therefore no pathologic correlation could be made; or (3) the patient decided to undergo neoadjuvant chemotherapy despite being an operative candidate. The remaining 80 patients were included in this analysis.

Patient population characteristics are listed in Table 2Go. Most patients had infiltrating ductal carcinoma. Those with tumors of unknown histology included patients with occult primary breast tumors and those in whom metastatic disease was discovered on scans, and biopsy of the distant site could not distinguish the specific histological type of breast cancer.


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  		TABLE 2. Patient population characteristics (n = 80)
 
Results for true-positive imaging findings are listed in Table 3Go. Eight (10%) of 80 patients were found to have distant metastatic disease, and in all, findings were seen on both conventional imaging studies and PET (Fig. 1Go). Biopsy of distant sites to prove stage IV disease was performed in all eight of these patients. Although none had distant metastatic disease detected by PET alone, four (5%) patients had additional foci of disease seen on PET scan only that affected treatment decisions; three had supraclavicular nodal disease that led to chemotherapy (Fig. 2Go). For all three patients, supraclavicular nodes were seen on CT < 1 cm in diameter, and these cases were therefore considered negative by CT (case 1, 1x.5 cm and rated 3, or equivocal; case 2, .6x.4 cm and rated 2, or probably normal; case 3, the patient had a minute lymph node that was rated 1, or definitely normal). The final patient with disease seen on PET alone had known cancer in the left breast; a synchronous contralateral breast primary tumor was detected by PET and was not seen on mammography or other conventional imaging studies. The contralateral primary lesion was a .6-cm invasive ductal cancer with surrounding ductal carcinoma-in-situ. This patient underwent a left modified radical mastectomy and a right total mastectomy with sentinel node biopsy as a result of these findings.


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  		TABLE 3. Sensitivity and specificity
 

Figure 1
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  		FIG. 1. Metastatic bone disease seen on (a) bone scan and (b) positron emission tomography (arrows point to foci in the pelvis and spine seen in both studies).

 

Figure 2
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  		FIG. 2. Supraclavicular nodal disease seen on positron emission tomography scan.

 
None of the 80 patients had metastatic or additional foci of disease seen on conventional imaging alone. In two patients, CT identified suspicious internal mammary nodes. PET scans were negative for internal mammary uptake in both of these patients. On the basis of location, biopsy was not thought to be feasible, and surgery proceeded without a change in plan. Follow-up CT scans in both of these patients revealed no change in one patient and disappearance of nodes in the second. These two cases were not counted among the false-positive or false-negative results, because biopsy could not be performed to verify findings as benign or malignant and because the findings did not influence treatment decisions.

Two patients had false-negative PET and conventional imaging studies. In one patient, a CT scan of the abdomen demonstrated a "suspicious" liver lesion for which additional imaging was recommended. A magnetic resonance imaging study of the liver was performed that demonstrated the liver lesion to be a hemangioma but that also detected two incidental lumbar spine lesions. Dedicated lumbar spine magnetic resonance imaging confirmed the presence of suspicious lesions, and bone biopsy was positive for metastatic breast cancer. This patient’s bone and PET scans were both negative. In the second patient, all scans were found to be negative, with "low-suspicion" tiny lung nodules seen on CT; however, a follow-up CT scan performed within 1 month demonstrated larger lung masses suggestive of metastatic breast cancer, which was confirmed by biopsy.

Thus, metastatic disease was present in 10 (12.5%) of 80 patients in this high-risk group. By stage, metastatic disease was seen in 4 (8.5%) of 47 patients who originally presented with stage IIB disease, 5 (24%) of 21 with stage IIIA disease, and 1 (8%) of 12 with locoregionally recurrent disease.

The sensitivity of PET and conventional imaging was equivalent in detecting metastatic disease (80%); however, the overall sensitivity of PET in detecting breast cancer-related findings that affected treatment was 86%, compared with 57% for conventional imaging. This difference was not significantly different (P = .13; McNemar’s test).

Incidental separate primary neoplasms were discovered in three patients: CT alone detected a .6-cm primary lung cancer in one patient, bone scan detected a meningioma in another, and PET detected a tubulovillous adenoma of the colon in the third. None of these three patients had occult primary breast cancer; therefore, these separate neoplasms were known second primary tumors.

In 14 (17%) patients, conventional imaging yielded findings that required additional imaging and subsequent biopsy or follow-up (minimum 6 months) that ultimately proved negative (Tables 3Go and 4Go). For 12 of 14 patients, findings were identified on CT scan, whereas 2 of 14 had findings on bone scan. Two of these 14 patients with conventional imaging findings that ultimately proved negative had the same false-positive finding on PET. PET demonstrated false-positive findings in two additional patients. Thus, the overall false-positive rate of PET scanning was 5% (4 of 80) for this patient population. The specificity of PET in detecting metastatic disease was 94% and was statistically significantly higher than that of conventional imaging, which was 79% (P = .01; McNemar’s test).


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  		TABLE 4. Description of false-positive results
 

   DISCUSSION
TOP
 ABSTRACT
 INTRODUCTION
 MATERIALS AND METHODS
 RESULTS
 DISCUSSION
REFERENCES
 
The role of PET scanning in breast cancer has been extensively investigated. Early studies focused on determining the limit of resolution for detecting primary breast lesions. These studies demonstrated that PET could detect virtually all large lesions yet lacked sensitivity for smaller-volume primary disease. In 1991, Wahl et al.9 showed that PET visualized all of 10 primary tumors that had a median diameter of 6 cm, the smallest of which was 3.2 cm. In 1993, Nieweg et al.10 demonstrated that PET was able to detect 10 of 11 primary tumors by using FDG-PET, yet all tumors visualized were > 1.8 cm, and the 1 missed lesion was 1.0 cm. Although the limits of resolution have improved and current technology can detect lesions as small as 5 mm, PET fares poorly compared with mammography, which can reliably detect microscopic disease, and magnetic resonance imaging, whose role in screening continues to expand. In our study, PET was able to detect one 6-mm primary breast cancer that was not seen on other imaging modalities; however, its use is not advocated for primary screening purposes on the basis of this incidental finding.

The use of PET scanning to determine axillary lymph node status before surgery has also been investigated.11–14 Recent studies have shown low false-positive rates for PET in determining axillary node status, thereby potentially obviating the need for sentinel node biopsy should PET demonstrate positive nodes in the axilla. However, as with the detection of primary tumors, where the ability to detect small-volume disease is the main limitation of its use, PET does not detect minimally or microscopically involved nodes. Thus, a negative PET scan would still require axillary nodal staging. The utility of PET for determining the extent of disease in breast cancer depends largely on the selection of an appropriate patient population for screening.

For all imaging modalities, in patients with clinically early-stage breast cancer, the yield of findings that would influence staging or treatment is low. Previous studies have demonstrated that baseline studies at the time of diagnosis in patients with clinical stage I or II disease have limited value. As early as 1988, Ciatto et al.15 demonstrated that detection rates of metastatic disease were < 1% each for chest radiography, bone scan, and liver ultrasonography in 3627 asymptomatic patients with early-stage disease. More recently, in a meta-analysis of Canadian patients undergoing screening for breast cancer, Myers et al.16 demonstrated positive bone-scan and liver ultrasonography rates of 1% and 0%, respectively, for stage I patients. Although it is possible that low detection rates represent a low sensitivity of these tests, they are more likely to be accurate given the large proportion of patients with early-stage disease who enjoy long-term recurrence-free survival.

Although screening in early-stage patients is a low-yield endeavor, the yield is higher when the population of patients selected for screening has more advanced-stage disease at presentation. van der Hoeven et al.17 demonstrated that 8% of patients who presented with locally advanced breast cancer were upstaged from stage III to IV on the basis of PET findings. In our patient population, a larger proportion of patients with stage IIIA disease, 24%, were found to have distant metastatic disease. Our population of patients included different groups with ostensibly biologically heterogenous disease; those with local recurrence may differ substantially from those with large tumors and negative nodes. Our goal was to determine the impact and value of PET scanning in a range of breast cancer patients for whom extent-of-disease evaluation is appropriate. A larger study with more patients would be necessary to provide more extensive information regarding the value of PET scanning in specific subpopulations of patients, such as those with local recurrence, which is a relatively uncommon event.

Previous studies have shown PET to fare comparably to conventional imaging in determining extent of disease. Schirrmeister et al.18 prospectively compared PET with chest radiography, bone scan, and liver ultrasonography in 117 patients. Metastatic disease was seen on PET and conventional imaging in four patients, and PET upstaged an additional three patients among a group of patients with predominantly early-stage disease. Bone scan was falsely positive in an additional four patients.

To our knowledge, our study is the first to compare CT and bone scan with PET in high-risk operable breast cancer patients in a prospective fashion with systematic biopsy or long-term follow-up to verify findings and results. Although PET and conventional imaging were equivalent in demonstrating metastatic disease, in a small number of patients, PET demonstrated supraclavicular disease that resulted in upstaging to IIIC disease and a change in treatment. Whereas supraclavicular nodes can be identified on CT and were seen in these 3 patients, CT relies solely on size to determine the level of suspicion, with all nodes < 1 cm being indeterminate at worst. This underscores the unique property of PET: providing metabolic information. However, although PET provides metabolic information that cannot be obtained from other imaging modalities, it has its own limitations: there can be variability in the detection of lesions on PET depending on tumor:background ratios, which can be inconsistent across different histological types. In addition, the ability to localize findings on PET can be problematic and typically involves obtaining additional imaging studies to specify the anatomical location of an abnormality and determine whether biopsy is feasible. Current technology does not allow biopsy to be performed via PET scan guidance alone. The integration of PET/CT combined scanners is the current state of the art for PET technology. PET/CT fusion imaging can eliminate the problem of localization of findings identified on PET; however, it must be noted that CT performed in combination with PET has limitations (related to motion, patient position, lack of intravenous and oral contrast, and misregistration issues) compared with diagnostic CT.

This study demonstrated a significantly higher specificity with PET. This is not unexpected given that the limit of resolution of PET scanning does not typically allow visualization of lesions smaller than 5 mm. CT is capable of visualizing small lesions, even 2 to 3 mm, that often prove to be clinically insignificant. The finding of fewer false-positive results generated by PET requires further study with more patients to verify these findings. Higher specificity would make treatment algorithms more efficient. The potential benefit to patients involves a reduced number of additional tests and/or biopsies to endure and a decreased likelihood of delay in definitive treatment because of a need to perform additional studies. Issues that remain to be addressed, however, include the current high cost of performing a PET scan. Although there is no question that reducing the need for additional tests and biopsies improves the patient’s experience, the high cost of PET scanning may potentially cancel out any financial benefit related to the reduction of these additional tests. A cost analysis is currently under way to determine the relative costs of performing PET compared with conventional imaging in these patients.

Other areas of exploration regarding PET involve investigating the significance of PET’s standardized uptake value related to pathology findings and determining whether this value has any added utility in predicting the prognosis or response to treatment.

In summary, the use of PET for determining extent of disease in patients with breast cancer may be appropriate in selected patients at high risk for harboring relevant findings. The increased specificity seen with PET compared with conventional imaging techniques should be further investigated from both patient-care and cost standpoints.


   ACKNOWLEDGMENTS
 
This study was funded by a grant from The Susan G. Komen Breast Cancer Foundation.

Received for publication March 4, 2005. Accepted for publication October 19, 2005.


   REFERENCES
TOP
 ABSTRACT
 INTRODUCTION
 MATERIALS AND METHODS
 RESULTS
 DISCUSSION
 REFERENCES
 

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