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1 Department of Radiology, Puget Sound Veterans Affairs Health Care System, 1660
S Columbian Way, S-113-RAD, Seattle, WA 98108.
2 Division of Nuclear Medicine, University of Washington School of Medicine,
1959 NE Pacific St., Seattle, WA 98195-7115.
3 Department of Radiology, University of Washington School of Medicine, Seattle,
WA 98195-7115.
4 Division of Medical Oncology, University of Washington School of Medicine,
Seattle, WA 98195-7115.
5 Department of Radiation Oncology, University of Washington School of Medicine,
Seattle, WA 98195-7115.
Received December 4, 2003;
accepted after revision February 19, 2004.
Supported by grants CA72064, CA42045, and CA90771 from the National
Institutes of Health.
Abstract
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MATERIALS AND METHODS. The medical records of 125 consecutive patients with recurrent or metastatic breast cancer referred for FDG PET from January 1998 through May 2002 were retrospectively reviewed. The rationale for FDG PET referral and the impact of FDG PET on subsequent treatment decisions for patients were determined by chart review. The impact of FDG PET on defining the extent of disease was determined by comparing the FDG PET interpretation at the time of the examination with findings from conventional imaging (CI) performed before FDG PET. FDG PET results were confirmed in nearly half (n = 61) of the patients by histopathology (n = 23) or follow-up imaging (n = 38; mean follow-up interval, 21.3 months).
RESULTS. Patients were referred for FDG PET for the following reasons: evaluation of disease response or viability after therapy (n = 43 [35%]), local recurrence, with intent of aggressive local treatment (n = 39 [31%]), equivocal findings on CI (n = 25 [20%]), evaluation of disease extent in patients with known metastases (n = 13 [10%]), and elevated tumor markers with unknown disease site (n = 5 [4%]). Compared with CI findings, the extent of disease increased in 54 (43%), did not change in 41 (33%), and decreased in 30 (24%) of 125 patients using FDG PET. Results of FDG PET altered the therapeutic plan in 40 (32%), directly helped to support the therapeutic plan in 34 (27%), and did not change the plan devised before FDG PET in 51 (41%) of 125 patients. FDG PET altered therapy most frequently in the patients suspected of having locoregional recurrence and in those being evaluated for treatment response versus other referral categories (p = 0.04). For patients with confirmation of FDG PET findings, the sensitivity, specificity, and accuracy of FDG PET were 94%, 91%, and 92%, respectively.
CONCLUSION. FDG PET contributes significantly to defining the extent of disease and deciding on treatment of patients with advanced breast cancer.
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The purpose of this study was therefore threefold: to assess the referral patterns for FDG PET at our institution for patients with advanced breast cancer, to evaluate the impact of FDG PET on defining the extent of disease, and to evaluate the impact of FDG PET on the management plan. We hypothesized that the impact of FDG PET on the therapeutic plan may be greater in some subgroups of patients with advanced breast cancer who are referred for FDG PET for restaging than in others, thereby identifying which patients may benefit most from FDG PET. Although ours is a retrospective study with all the inherent limitations of a retrospective approach, the analysis provides insight into current clinical uses of FDG PET for breast cancer and provides preliminary data for future prospective studies of the impact of FDG PET on the treatment of patients with breast cancer.
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Assessment of the Impact of FDG PET on Defining the Extent of Disease and on the Management Plan
The rationale for FDG PET referral and the impact of FDG PET on subsequent
treatment decisions for patients were determined by review of medical records.
Categories for referral rationale included the evaluation of disease response
or viability after therapy, local recurrence with intent to treat aggressively
for local control, equivocal findings on CI, evaluation of disease extent in
patients with known metastatic disease, and elevated tumor markers with
unknown disease site. These categories were based on observation of common
referral patterns at our institution and from prior preliminary analysis on
the impact of FDG PET on staging and treatment of patients with advanced
breast cancer (Cortese T et al., presented at the 1997 annual meeting of the
Radiological Society of North America).
The impact of FDG PET on defining the extent of disease was determined by comparing the prospective FDG PET interpretation with findings at clinical examination and on CI, including CT, MRI, and bone scans performed before PET. CI was performed before FDG PET with a mean time interval of 17.9 days (range, 0-95 days). The effect of FDG PET on defining the extent of disease was placed in one of three categories: increased, decreased, or no change. FDG PET increased the extent of disease if it showed one or more sites of radiotracer uptake not detected or equivocal on CI, including detection of additional metastatic foci in patients with stage IV cancer. The effect of FDG PET was to decrease the extent of disease if no abnormal radiotracer uptake was present at sites that were equivocal on CI; PET was not used to downstage findings on CI that were unequivocally positive.
FDG PET results were confirmed in nearly half (n = 61) of the patients by histopathology (n = 23) or follow-up imaging (n = 38; mean follow-up time, 21.3 months). For follow-up imaging, the presence of disease was confirmed if new lesions appeared or previously identified lesions increased in size on CI (predominantly CT) regardless of whether the patient was undergoing systemic therapy. Confirmation of FDG PET findings was based on the period of 2 months after FDG PET scanning. The absence of disease was confirmed if no disease was detected on follow-up imaging at least 2 months after FDG PET with the patient not undergoing any therapy. False-negative status was determined when sites of recurrent or metastatic disease developed on follow-up CI within 2 months of negative findings on PET. FDG uptake was considered false-positive when no progression was evident at this site on follow-up imaging with the patient not undergoing any therapy. Status of disease was considered indeterminate if there was no significant change or decrease in lesion size on follow-up CI while the patient was undergoing systemic therapy or if the patient had not undergone follow-up imaging.
The impact of FDG PET on the management plan devised by the managing team of oncologists (medical, surgical, and radiation) before PET was placed into one of three categories: altered, supported, or no change. "Altered status" was applied if there was a documented change in the therapeutic plan based on the FDG PET results; this included several outcomes that were classified as either inter- or intramodality treatment changes. "Intermodality change" was an alteration from one treatment modality to another, such as surgery to systemic medical treatment or from medical or surgical treatment to no treatment. "Intramodality change" was one that was made within a treatment modality, such as an alteration in systemic chemohormonal therapy or radiation field. FDG PET was considered supportive of the management plan if the oncologists cited FDG PET results as improving their confidence in defining the extent of disease and as being an important part of the decision to implement the management plan even if the FDG PET results did not change the plan that had been considered before FDG PET imaging. For patients who were referred for evaluation of treatment response, data from the first posttreatment FDG PET scan were used to evaluate the impact on the management plan if the patient also had a baseline FDG PET scan before initiation of therapy. Otherwise, the first FDG PET scan was used in the evaluation of disease extent and impact on treatment plan in patients who underwent serial FDG PET.
FDG PET Technique
FDG PET imaging was performed with an Advance scanner (GE Healthcare). FDG
was prepared using the method of Hamacher et al.
[13] and had radiochemical
purity greater than 95% and specific activity greater than 47 GBq/µmol. The
patients fasted for at least 4 hr and typically 6-12 hr before the
examination. A blood sample for determination of glucose was obtained before
FDG administration (concentrations ranged from 66 to 118 mg/dL) to ensure
euglycemia. Beginning approximately 45 min after IV injection of FDG (dose
range, 244-400 MBq [6.6-10.8 mCi]; mean dose, 363 Mbq [9.8 mCi]), whole-body
imaging with the patient in a supine position was performed. All images were
acquired in 2D high-sensitivity mode with 35 imaging planes covering an axial
field of view (FOV) of 15 cm (4.0-mm axial full-width at half-maximum at the
center of the tomograph) and in-plane intrinsic resolution of 4-5 mm
[14,
15]. One of two survey imaging
protocols was used. For patients with suspected widespread disease, the
emission scanning survey consisted of five adjacent 15-cm axial FOVs (7 min
per FOV) extending from the inferior pelvis to the superior thorax. More
detailed imaging in anatomic areas of interest was later performed with 15-cm
axial FOV emission scanning (15-25 min per FOV) followed by transmission
scanning (25-50 min per FOV before implementation of segmentation of
transmission and maximum 7 min per FOV for all five FOVs after implementation
of segmentation of transmission). For patients with suspected locoregional
disease, a limited torso survey from the neck to the bottom of the liver was
obtained using three adjacent 15-cm axial FOV emission scans (10 min per FOV)
and three adjacent 15-cm FOV postinjection transmission scans (15 min per FOV
[before implementation of segmentation of transmission]) or postinjection
transmission scanning data from all five FOVs (maximum 7 min per FOV [after
implementation of segmentation of transmission]).
Transmission scans were obtained with a rotating germanium-68 rod source. Quantitative analysis was applied to the attenuation-corrected images by computing the maximum standard uptake value (SUV) of areas of focal FDG accumulation [16]. Images were reconstructed onto a 128 x 128 matrix using a Hanning filter, which resulted in an effective in-plane resolution (full-width at half-maximum) of approximately 10-12 mm [14, 15]. The reconstructed images were displayed in axial, coronal, and sagittal planes on a workstation, as needed.
FDG PET Interpretation
The extent of disease from FDG PET findings was based on the retrospective
review of the interpretation of the FDG PET examination performed
prospectively at the time of the examination by consensus of two or more
nuclear medicine physicians with experience in FDG PET imaging, as per
clinical routine. A coauthor provided interpretations for most of the FDG PET
examinations. PET images were correlated with clinical data and CI studies
available at the time of interpretation. The attenuation-corrected images were
used primarily for the final interpretation. Overall interpretation was based
on qualitative visual interpretation and comparison of mean maximum SUV in
positive sites of disease with normal background uptake. No strict SUV
threshold value was used to differentiate benign from malignant tissue. The
overall interpretation of each FDG PET scan was categorized as positive,
negative, or equivocal. Equivocal status was applied to sites of increased
uptake different from the expected background that could not be clearly
classified as abnormal, even after comparison with available data from CI.
Statistical Analysis
The likelihood of FDG PET-induced alterations in the treatment plan and
change in extent of disease among the referral categories was performed with
contingency tables using chi-square likelihood ratio or Fisher's exact test. A
p value of less than 0.05 was considered significant.
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Overall, FDG PET was positive at one or more sites in 94 (75%), negative in 26 (21%), and equivocal in five (4%) of 125 patients. The mean maximum SUV was 5.1 (range, 1.1-17.5). The extent of disease evaluated by FDG PET was different (either increased [n = 54] or decreased, [n = 30]) from CI in 84 (67%) and did not change in 41 (33%) of 125 patients. FDG PET showed a change in extent of disease most frequently in the locoregional subgroup versus all other referral categories (p = 0.04). There were 91 sites of potential disease detected on FDG PET not identified on CI in the 54 patients who had an increased extent of disease on FDG PET. The predominant site of uptake in these patients was in nodal regions or the chest wall (65/91 [71%]; mediastinal [n = 24], supraclavicular or cervical [n = 17], axillary [n = 10], internal mammary [n = 9] and abdominal nodes [n = 2], and chest wall [n = 3]), compared with visceral or skeletal sites (26/91 [29%]: bone [n = 10], liver [n = 8], and lung [n = 8]).
Results of FDG PET altered the management plan in 40 (32%), supported the plan in 34 (27%), and had no impact on the plan in 51 (41%) of 125 patients. Figure 1 shows the impact of FDG PET on the management plan by category of referral. There was a significant difference for the impact on treatment among the different referral categories (p < 0.01 for differences between all categories). FDG PET had a significantly greater impact on altering therapy for patients in the locoregional disease and response to treatment categories (p = 0.04 for these categories vs the others). FDG PET altered the management plan most frequently in patients suspected of having locoregional disease (17/39 [44%], p = 0.06 vs all other referral categories) (Fig. 2A, 2B). FDG had the least impact on the management plans in the subset of patients with known metastases referred for evaluating the extent of disease (altered the plan in 1/13 [8%] and no change in 11/13 [85%], p = 0.01 vs all other referral categories).
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FDG PET altered (n = 40) or supported (n = 34) the treatment plan in 74 (59%) of 125 patients. Findings from FDG PET altered or supported the treatment plan most frequently in patients being evaluated for treatment response (32/43 [74%], p = 0.08 vs all other referral categories) (Fig. 3A, 3B).
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For patients in whom FDG PET showed an increase in the extent of disease (n = 54), the therapeutic plan was altered in 30 (55%), supported in five (9%), and not changed in 19 patients (36%). For patients in whom FDG PET findings were instrumental in altering the therapeutic plan (n = 40), the change in treatment plan was intermodal in 23 (58%) and intramodal in 17 (42%) patients (Table 1). The overall sensitivity, specificity, and accuracy of FDG PET was 94%, 91%, and 92%, respectively, for patients with confirmation of FDG PET findings (n = 61). Twenty-three patients had pathologic confirmation: 20 had true-positive findings, and one each had true-negative, false-negative, and false-positive findings. Among patients who had confirmation by follow-up imaging (n = 38), the majority (27/38 [71%]) showed progression of disease (true-positive findings), nine had true-negative findings, and two had false-negative findings. Of the three confirmed false-negative FDG PET findings, one patient developed skeletal metastases that were negative on FDG PET (Fig. 4A, 4B), the second patient had a second breast primary (1.2-cm invasive ductal carcinoma with steroid-receptor status different from that of the original tumor in the same breast) that was excised 9 days after a negative FDG PET examination, and the third patient had small (< 1 cm) pulmonary nodules on CT that were negative on FDG PET and confirmed metastases on follow-up CT. The one confirmed false-positive FDG PET finding occurred in a patient who had FDG uptake in a level III axillary node (SUV, 3.2) but no pathologic evidence of malignancy in these nodes after surgical removal.
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Our study showed the significant incremental value of FDG PET with CI to define the extent of disease and induce change in therapy for patients with recurrent breast cancer. Other studies have shown the ability of FDG PET to improve restaging in similar patient populations, primarily through an increase in sensitivity in detecting sites of local or distant recurrence [1-4, 9]. The extent of disease increased in 43% and decreased in 24% of patients in our study who underwent FDG PET after restaging with CI. Local or distant nodal uptake accounted for most of the sites of unsuspected disease on CI; this finding was also reported in two separate retrospective studies of patients with clinical suspicion of local or distant recurrence who underwent CI and FDG PET [18, 19]. In a prospective study evaluating the impact of whole-body FDG PET on staging and treating patients with breast cancer, Yap et al. [12] showed that FDG PET changed the clinical stage in 36% of patients.
The change in the extent of disease shown by FDG PET, as reported in our study, is expected to be more frequent than the change in clinical stage because not all patients whose disease extent is greater or less become up-staged or downstaged, respectively. As for the patients in whom FDG PET findings indicated a decrease in extent of disease in our study, most (19/30 [63%]) of the cases were probably due to overestimation of disease based on CI; 11 of these patients had no confirmed disease at these sites on follow-up imaging with the patient undergoing no systemic therapy. In eight patients (27%), FDG PET likely underestimated the extent of disease on the basis of follow-up imaging; these patients were predominantly those who had been previously treated for distant metastases (bone or liver), showed equivocal findings on CI and no FDG uptake, and then whose disease subsequently progressed at these sites on follow-up imaging. These findings suggest that therapy may suppress FDG uptake at some sites of treated but viable tumor and that this possibility should be taken into account in interpreting studies in recently treated patients. Three patients (10%) had no follow-up imaging or clinical evaluation.
The Centers for Medicare & Medicaid Services has approved medical insurance reimbursement for the use of FDG PET in restaging patients with advanced breast cancer. This decision was based in part on several retrospective studies showing the improved sensitivity and accuracy of FDG PET compared with CI in restaging these patients [1-4]. However, patients with recurrent breast cancer are a heterogeneous group with diverse clinical presentations and therapeutic options for disease control. Depending primarily on the extent of disease and the clinical situation, some patients may benefit more than others from FDG PET as a restaging tool. This retrospective study helps to identify subgroups among patients with local or distant recurrences who would most likely benefit from FDG PET restaging.
Taking impact on therapy as the most direct gauge of the benefit derived from FDG PET, we found that patients with suspected locoregional recurrence have the highest frequency (44%) of FDG PET-induced changes in treatment. Most therapeutic changes (76%) were major or intermodality. Surgery was avoided in 11 of these patients because of detection of more widespread disease by FDG PET compared with CI. This finding underscores the need for accurate restaging in this group of patients who have a variety of treatment options available to them including surgery, radiation, chemotherapy, hormonal therapy, or a combination of the these choices.
FDG PET also had significant impact on the treatment of patients with disease recurrence. The assessment of response to therapy is often problematic when it is based on clinical and CI parameters, particularly when disease is localized in the skeleton [17] or soft-tissue sites previously treated with surgery or radiation [20]. The status of treatment efficacy is crucial in determining whether current therapy should be continued, stopped, or changed to a more aggressive regimen. In our study, FDG PET altered the treatment plan in 33% (14/43) and supported the plan in 42% (18/43) of patients being evaluated for response to therapy. This outcome suggests that the FDG PET findings increase the oncologists' confidence in evaluating the extent of disease and have a strong positive impact on implementing a specific treatment plan in this group of patients. The index lesions being evaluated were located in the skeleton (53%), liver (19%), lung (17%), and soft tissue and nodes (11%). As expected, most of the changes were intramodal (8/14 [57%]) when systemic therapy was changed either to another chemotherapy regimen or from chemotherapy to hormonal therapy or vice versa. More interesting, in two patients, treatment was withheld on the basis of FDG PET findings. One patient had a solitary liver metastasis treated with chemotherapy and a persistent focal abnormality on CT after treatment. FDG PET showed no uptake at the site of this abnormality on CT, and instead of undergoing radiofrequency ablation, the patient was observed. In the other patient, chemotherapy was withheld after FDG PET showed a complete response of skeletal metastases. The utility of FDG PET in the evaluation of response to treatment in the skeleton [21] and at other distant metastatic sites [22] has previously been reported.
Findings on CI can be equivocal for potential sites of disease if imaging findings are not characteristic enough to differentiate benign from malignant tissue, especially for patients who have undergone prior therapy, such as surgery or radiotherapy, which may alter tissue characteristics. FDG PET can provide increased specificity in these cases because malignant tissue is more metabolically active than benign tissue [23]. Among the 25 patients referred for equivocal CI findings in our study, FDG PET showed an uptake consistent with disease recurrence in five (20%) of 25, lack of uptake consistent with absence of disease in 17 (68%) of 25, and equivocal degree of uptake in three (12%) of 25. FDG PET induced management changes in five (20%) of these 20 patients, and in four of these patients, FDG PET showed uptake consistent with disease recurrence.
FDG PET has been shown useful in patients suspected of recurrence with elevated tumor markers but no visible evidence of disease on CI [5, 9, 24]. It is difficult to draw a significant conclusion about the utility of FDG PET in restaging this subgroup in our study because the number of patients was so few (n = 5); however, FDG PET induced a change in treatment in three (60%) of five patients.
The impact on treatment plan was least significant among patients with known metastases who were being referred to evaluate the extent of disease. Even though FDG PET showed an increase in the extent of disease in nine (69%) of 13 of these patients in our study, the treatment plan was altered in only one patient. This patient had a suspected recurrence in the contralateral axilla only, and after FDG PET showed suspicious uptake in mediastinal and bilateral supraclavicular nodes, she was treated with chemotherapy and radiation to the FDG PET-positive sites of disease, including the mediastinum.
Our results confirm the results of other investigations into the clinical impact of FDG PET on patients with a variety of primary malignancies [12, 25-31], including studies concerning restaging of breast cancer [12]. The frequency of FDG PET-induced management changes in these studies ranges from 24-63%. In the prospective study by Yap et al. [12] based on responses from referring physician questionnaires, 58% of patients had a change in treatment plan based on FDG PET results. This result is almost identical to the frequency of patients (59%) in our study in whom FDG PET was instrumental in supporting or directly altering the management plan. Our results should not be used as a justification for the routine use of FDG PET for staging or restaging of patients with suspected recurrence or distant metastases. Instead, our results indicate that FDG PET is most helpful when used to address specific questions after completion of conventional staging studies.
Our study had several limitations. Because it was retrospective, we relied almost entirely on review of medical records to determine the impact of FDG PET findings on patient treatment. In most cases, this determination was easily based on the oncologists' notes; however, a prospective study with questionnaire-directed physician responses before and after FDG PET would improve accuracy in this regard. Our patient population was highly selected from a tertiary care center and as such may not be representative of the general patient population with recurrent or metastatic disease. One advantage of a retrospective study like ours is that one can determine if the proposed treatment plan after FDG PET was actually implemented.
Another limitation was the lack of histologic or follow-up imaging confirmation of FDG PET findings in most patients; only 23 (18%) of 125 patients underwent biopsy or resection to confirm the extent of disease. This limitation is a reflection of the standard clinical practice in patients with advanced breast cancer who may have metastases that are widespread or difficult to access, making biopsy impractical. As for the group of patients who had no confirmation of FDG PET findings (n = 64), a subset of patients (n = 23) was followed up exclusively with serial FDG PET examinations because their disease was difficult to evaluate on CI. We did not include these patients in our analysis for the accuracy of FDG PET findings because the gold standard in those cases would have been FDG PET, the same test whose accuracy we were evaluating. Another 41 patients had no confirmation, either because there was no histopathology report; the findings of follow-up imaging were indeterminate on the basis of our criteria, typically because of the confounding influence of concurrent therapy; or there was no follow-up imaging at all.
In conclusion, FDG PET helped to define the extent of disease and determine the treatment plan in a significant number of patients with advanced breast cancer in this retrospective study. FDG PET was significantly more sensitive for the detection of potential disease in nodal regions but also detected more sites of bone and visceral disease compared with CI. The treatment plan was altered by FDG PET findings most frequently in the subset of patients suspected of having locoregional recurrence. Prospective studies are needed to define more accurately the role of FDG PET in this highly selected population.
Acknowledgments
We thank Erin Schubert and Lisa Dunnwald for help with image preparation,
Pam Pham and the nuclear medicine technologist staff and the radiochemistry
and physics group at our institution for technical assistance with the imaging
studies, and the staff of the Breast Cancer Specialty Center for help with
patient referrals.
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