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Annals of Surgical Oncology 10:622-627 (2003)
© 2003 Society of Surgical Oncology

ORIGINAL ARTICLES

Evaluation of Fluorodeoxyglucose Positron Emission Tomography in the Detection of Axillary Lymph Node Metastases in Patients With Early-Stage Breast Cancer

Emmanuel Barranger, MD, Dany Grahek, MD, Martine Antoine, MD, Françoise Montravers, MD, Jean-Noel Talbot, MD and Serge Uzan, MD

From the Departments of Gynecologic and Breast Cancers (EB, SU), Nuclear Medicine (DG, FM, J-NT), and Pathology (MA), Hôpital Tenon, Paris, France.

Correspondence: Address correspondence and reprint requests to: Emmanuel Barranger, MD, Department of Gynecologic and Breast Cancers, Hôpital Tenon, 4 rue de la Chine, 75020 Paris, France; Fax: 011-33-156-016-855; E-mail: emmanuel.barranger{at}tnn.ap-hop-paris.fr


   ABSTRACT
TOP
 ABSTRACT
INTRODUCTION
 PATIENTS AND METHODS
 RESULTS
 DISCUSSION
 REFERENCES
 
Background: The aim of this study was to assess the capacity of positron emission tomography (PET) with fluorodeoxyglucose (FDG) to determine axillary lymph node status in patients with breast cancer undergoing sentinel node (SN) biopsy.

Methods: Thirty-two patients with breast cancer and clinically negative axillary nodes were recruited. All patients underwent FDG-PET before SN biopsy. After SN biopsy, all patients underwent complete axillary lymph node (ALN) dissection.

Results: The SNs were identified in all patients. Fourteen patients (43.8%) had metastatic SNs (macrometastatic in seven, micrometastatic in six, and isolated tumor cells in one). The false-negative rate of SN biopsy was 6.6% (1 in 15). FDG-PET identified lymph node metastases in 3 of the 14 patients with positive SNs. The overall sensitivity, specificity, and positive and negative predictive values of FDG-PET in the diagnosis of axillary metastasis were 20%, 100%, 100%, and 58.6%, respectively. No false-positive findings were obtained with FDG-PET.

Conclusions: This study demonstrates the limitations of FDG-PET in the detection of ALN metastases in patients with early breast cancer. In contrast, FDG-PET seems to be a specific method for staging the axilla in breast cancer. SN biopsy can be avoided in patients with positive FDG-PET, in whom complete ALN dissection should be the primary procedure.

Key Words: Fluorodeoxyglucose • Positron emission tomography • Sentinel lymph node • Breast cancer


   INTRODUCTION
TOP
 ABSTRACT
 INTRODUCTION
PATIENTS AND METHODS
 RESULTS
 DISCUSSION
 REFERENCES
 
Carcinoma of the breast is the most common female malignancy. Its incidence has been increasing in Europe and the United States, but the fatality rate has remained stable.1,2 It was estimated that approximately 200,000 new cases of female breast cancer would be diagnosed in the United States in 2001, of which 75% to 80% would be stage I or II disease.2 In the United States, approximately 40,000 women will die each year from breast cancer, despite aggressive therapy including surgery, chemotherapy, and irradiation.

Axillary lymph node (ALN) dissection has been an integral part of the surgical management of breast cancer since the introduction of Halsted radical mastectomy. Recently, management of the axilla in patients with operable breast cancer has become one of the most controversial topics in clinical oncology, regarding the value and optimal extent of surgical dissection as well as the morbidity and cost. The main role of ALN dissection is to provide staging and prognostic information; local control of axillary disease is a secondary function. However, only 30% of women with an invasive breast tumor with a diameter of <=20 mm have ALN metastases.3 ALN dissection confers no survival advantage when the lymph nodes are not involved.

Sentinel node (SN) biopsy, introduced by Krag et al.4 and Giuliano et al.5 in the early 1990s, represents a new standard of care for axillary node staging in patients with early-stage, clinically node-negative breast cancer. The goals of SN biopsy are to decrease the morbidity of breast cancer surgery by avoiding unnecessary ALN dissection, to preserve control of regional disease, and to improve staging of the regional lymph node basin. The most critical factor is the false-negative rate, which ranges from 0% to 25%.6

Positron emission tomography (PET) with fluorodeoxyglucose (FDG) is a noninvasive method of detecting clinically occult metastases. Various studies indicate that FDG-PET can accurately predict the axillary node status of patients with breast cancer.7,8 However, these studies compared the results of FDG-PET with those of standard histopathologic evaluation of dissected nodes and not with those of SN biopsy.

The purpose of this study was to evaluate FDG-PET in the preoperative detection of axillary metastases in patients with early-stage breast cancer requiring SN biopsy.


   PATIENTS AND METHODS
TOP
 ABSTRACT
 INTRODUCTION
 PATIENTS AND METHODS
RESULTS
 DISCUSSION
 REFERENCES
 
From March to September 2001, 32 consecutive patients with a malignant breast tumor and clinically negative axillary nodes were enrolled in this prospective study. Exclusion criteria included pregnancy, diabetes, and neoadjuvant therapy. All the patients signed an informed consent form, and each procedure was approved by our institutional review board. One week before FDG-PET, all patients had cytologically or histologically proven breast cancer, on the basis of core needle biopsy or fine-needle aspiration.

After FDG-PET imaging, all patients underwent SN biopsy, preceded in most cases by lymphoscintigraphy to establish the regional draining basin. All SN biopsies were followed by ALN dissection, including level I and II nodes. One surgeon (E.B.) participated in the study.

FDG-PET Imaging
One or 2 weeks before SN biopsy, all patients underwent preoperative FDG-PET examination with a triple-headed hybrid gamma camera with coincidence detection (Irix; Marconi Corp., Cleveland Heights, OH). The patients were asked to fast for at least 6 hours before the examination. Serum glucose levels were measured to ensure euglycemia (<7 mmol/L). FDG (4 MBq/kg IV; Flucis; Cis Bio International, Saclay, France) was then injected with a saline infusion. One hour after the injection, a whole-body scan and abdominal tomoscintigraphy were systematically performed in the supine position, followed by thoracic tomoscintigraphy in the prone position with the arms in extension, by using a mammoscintigraphy table. Each tomoscintigraphic acquisition, which involved an effective field of view of 35 cm, was performed by using 30 steps of 6° each, lasting 30 seconds at the start of acquisition (and then longer as 18F decayed). Only photons with an energy of 511 ± 102 keV were accepted. Slices were reconstructed by using an iterative algorithm (maximum likehood-expectation maximization) and a 128 x 128 matrix. Attenuation correction by an external source and postfiltering were not used.

SN Biopsy Technique
Four peritumoral injections of 0.2 mL (30 MBq each) of unfiltered 99mTc sulfur colloid (Nanocis; CIS Bio International) were made on the day before surgery. The injections were made under ultrasound guidance when the tumor was nonpalpable (n = 9 patients). Scintigraphic images, including the breast and axilla, were obtained 1 hour after the injections and then every 30 minutes until the SN was visualized, by using the same Irix gamma camera as for FDG imaging. Five-minute static, anterior, and lateral projections were acquired with a low-energy/high-resolution collimator and a matrix of 512 x 512 pixels. If the SN was not visualized on the day of the injection, a final image was acquired the following day, 2 hours before the surgical procedure.

After the induction of general anesthesia, patients received a subdermal injection of 2 mL of patent blue dye (Bleu Patenté V; Guerbet Laboratory, Issy les Moulineaux, France) above the tumor, followed by breast massage for 3 minutes. Fifteen minutes after the injection, breast surgery (mastectomy or lumpectomy) was performed, followed by SN detection with a CdTe probe (Gammed 2; Eurorad, Strasbourg, France). SN biopsy was performed through an incision, in accordance with radical nodal dissection just below the axillary hairline where the gamma probe showed the highest nodal radioactivity. The SN was located by following a blue lymphatic channel to a lymph node and/or by using the gamma probe to detect radioactive nodes. SN biopsy was followed by standard axillary dissection.

Histopathologic Evaluation
Each half-SN was sectioned at 3-mm intervals. Each 3-mm section was analyzed by four additional levels of 150 µm and four parallel sections; one level was used for hematoxylin and eosin (H&E) staining, and H&E-negative sections were examined by immunohistochemistry (IHC) with an anticytokeratin antibody cocktail (Cytokeratin AE1-AE3; Dako Corp., Glostrup, Denmark). Non-SNs in the axillary dissection specimen were evaluated with H&E-stained sections.

The size of nodal metastases was estimated with an eyepiece micrometer. Micrometastasis was defined as a single focus of metastatic disease per node, measuring no more than 2 mm. The presence of single noncohesive tumor cells was recorded. SNs were recorded as positive when they contained macrometastases, micrometastases, or isolated tumor cells.

Analysis
SNs were recorded as blue stained and/or "hot" (ex vivo count exceeding three times the background). The false-negative rate was defined as the number of procedures with a negative SN and one or more positive non-SNs divided by the number of procedures with any positive ALN. The surgeon and pathologists were blinded to the FDG-PET results.

FDG-PET images were visually interpreted by two experienced nuclear medicine physicians blinded to all clinical data. A consensus was reached as to the presence or absence of abnormal uptake in the axillary basin and on the degree of uptake, ranked on a simple three-point scale relative to cardiac uptake.

The evaluation of FDG-PET results was based on calculated sensitivity, specificity, accuracy, and positive and negative predictive values relative to the histopathologic status of the SN and non-SN, as follows:


(1)


(2)


(3)


(4)


(5)

where TP is true positive, TN is true negative, FP is false positive, and FN is false negative.


   RESULTS
TOP
 ABSTRACT
 INTRODUCTION
 PATIENTS AND METHODS
 RESULTS
DISCUSSION
 REFERENCES
 
Lymphatic mapping was performed with patent blue dye plus radioactive colloid in 28 patients (87.5%) and with patent blue alone in 4 patients (12.5%). In the 28 patients with combined tracers, lymphoscintigraphy visualized one focus or several foci of uptake corresponding to an SN. The patient demographics and tumor characteristics are listed in Table 1. Most patients (56.3%) had clinical stage T1 disease. Twenty-nine patients (90.6%) underwent breast-conserving therapy, and three (8.4%) underwent mastectomy.


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  		TABLE 1. Patient demographics and tumor characteristics
 
The mean number of lymph nodes obtained during axillary dissection was 11 (range, 4 to 19). The SNs (mean number per patient, 2.4; range, 1 to 5) were identified in every case.

Metastatic disease was found in the SN of 14 patients (43.8%). The SN was macrometastatic in seven patients and micrometastatic in six patients. In the last case, the SN contained isolated tumor cells. Additional axillary node macrometastases were found in five patients (35.7%). Metastatic disease was confined to a single SN in eight patients. The SN was falsely negative in one patient (6.6%). In this patient, SN biopsy was performed by combined detection.

No FDG uptake by the primary tumor was observed in 10 (31.3%) of the 32 patients. At pathologic examination, the tumors measured from 8 to 40 mm in their largest diameter. All the tumors were histologically classified as invasive ductal carcinoma.

In 20 of the 32 patients, FDG-PET correctly identified positive or negative lymph node status. FDG-PET identified lymph node metastases in 2 of the 14 patients with a positive SN (Fig. 1). These two patients (primary lesions of 32 and 24 mm) had macrometastases at SN biopsy and massive lymph node involvement at axillary dissection. In the first patient, the two metastatic SNs measured 20 and 9 mm. The median size of the nine additional metastatic non-SNs was 9 mm (range, 2–23 mm). In the second patient, the two involved SNs measured 10 and 12 mm, and the median size of the five additional metastatic non-SNs was 7 mm (range, 1–9 mm). The patient who had a negative SN with one metastasis in a non-SN (metastatic node of 3 mm) also had signs of axillary metastasis at FDG-PET. FDG uptake was also observed in the primary tumor in these three patients with positive FDG-PET in the axillary basin. The characteristics of the patients with false-negative FDG-PET findings are listed in Table 2. No false-positive findings were encountered with FDG-PET. The overall sensitivity, specificity, accuracy, positive predictive value, and negative predictive value of FDG-PET in the diagnosis of axillary metastasis were 20%, 100%, 62.5%, 100%, and 58.6%, respectively. No abnormal FDG uptake was ever detected in the internal mammary region.



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  		FIG. 1. Fluorodeoxyglucose positron emission tomography (PET): coronal section of a patient with breast cancer (T). The PET shows axillary lymph node metastases (N).

 

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  		TABLE 2. Characteristics of patients with false-negative FDG-PET (n = 12)
 

   DISCUSSION
TOP
 ABSTRACT
 INTRODUCTION
 PATIENTS AND METHODS
 RESULTS
 DISCUSSION
REFERENCES
 
We evaluated FDG-PET in the detection of ALN metastases in patients with early-stage breast cancer undergoing SN biopsy. The sensitivity of FDG-PET was only 20%, taking SN biopsy and IHC as a reference.

Several teams have evaluated the value of FDG-PET in the detection of ALN metastases7–13 and have obtained sensitivities of 79% to 100%.7,8,11–13 Thus, in a series of 74 patients with breast cancer, Rostom et al.12 obtained sensitivity, specificity, and accuracy rates of 86%, 100%, and 90%, respectively, for FDG-PET detection of ALN metastases. Likewise, Schirrmeister et al.13 reported sensitivity, specificity, and accuracy rates of 79%, 92%, and 89%, respectively, in 85 patients. Greco et al.7 even suggested that FDG-PET could avoid histological assessment of ALN status in patients with early-stage breast cancer (stage T1). Our results do not support this view. Several possible explanations can be forwarded for the far lower sensitivity of FDG-PET in our study. First, previous studies involved selected patients with more advanced disease than generally reported in the SN literature. Indeed, Avril et al.9 reported that FDG-PET was less sensitive in patients with stage T1 breast cancer (33%) than in the overall sample of 18 patients, only 6 of whom had ALN. Furthermore, in recent studies of patients with early-stage breast cancer and clinically negative axillary nodes, the sensitivity of FDG-PET for detection of ALN metastases ranged from 25% to 50%.14–16

The second and most likely explanation for the lower sensitivity observed in our study is the higher detection rate of lymph node metastases by SN biopsy with step sections and IHC. Indeed, previous studies used H&E staining of ALNs as the gold standard.9–13 It has been shown that the SN procedure step sections and IHC increase the detection rate of micrometastases in ALNs.5 In contrast, FDG-PET can visualize only small lymph node metastases: none of the six patients with micrometastatic SNs in our study had positive FDG-PET findings. Acland et al.17 also recently reported that FDG-PET had zero sensitivity for the detection of SN micrometastases in patients with cutaneous malignant melanoma undergoing SN biopsy.

The low sensitivity of FDG-PET in our study cannot be explained by technical factors. Indeed, the performance of our coincidence gamma camera was optimal, with three detectors (instead of the usual two), 19-mm crystals (instead of 16 mm), and image reconstruction with an iterative algorithm (instead of filtered back-projection). Moreover, our results are similar to those obtained by Van der Hoeven et al.16 with dedicated PET systems. Those authors reported an FDG-PET sensitivity of 25% for the detection of ALN metastases in patients with early-stage breast cancer and clinically negative axillary nodes undergoing SN biopsy. However, in this study, the size of the ALN metastases detected by FDG-PET was not reported. Similarly, in recent studies published by Guller et al.,14 who also used a dedicated PET system, the sensitivity for ALN metastases was only 43%. Taken together, these results suggest that SN biopsy is clearly superior to FDG-PET for the detection of axillary metastasis in patients with early-stage breast cancer (stage T1). FDG-PET may be used to extend the indications of the SN biopsy toward larger tumors, where SN experience is limited with an increased false-negative result of SN biopsy.

FDG-PET detected ALN metastasis with very high specificity and gave no false-positive results. These results are similar to those of FDG-PET studies.7–9 It seems that SN biopsy can be dispensed with when FDG-PET is positive in the axilla and that such patients should undergo complete ALN dissection as the primary procedure. This approach would reduce the costs.

To our knowledge, this is the first study in which FDG-PET was found to reduce the false-negative rate of SN biopsy. Indeed, the patient who had a negative SN but one non-SN metastasis had FDG-PET signs of a suggestive axillary node. This is somewhat surprising, because the non-SN metastasis detected by FDG-PET was only 3 mm in diameter. We initially thought that ALN dissection after SN biopsy might have left one or several macrometastatic axillary nodes, but this patient had normal FDG-PET findings 8 months after surgery. It is possible that the superficial nature of the metastasis in this thin patient (body mass index, 19.7 kg/m2) made it easier to detect by FDG-PET. In the literature, the smallest lymph node metastases detected by FDG-PET range from 3 to 5 mm in diameter.13,15

Breast cancer can drain to the internal mammary chain. A large study by Li and Shen18 showed that the risk of internal mammary node metastasis was higher in patients with central and inner-quadrant tumors. Internal mammary node status is also an important prognostic factor.19 The isotopic SN procedure can visualize involved SNs in the internal mammary chain during preoperative lymphoscintigraphy. The removal of these internal mammary SNs is controversial, because the incidence of internal mammary node involvement, established by breast lymphoscintigraphy and lymphatic mapping, is reported to be between 1% and 6%.20 Moreover, neither excision nor radiotherapy of the internal mammary chain has convincingly been shown to improve the survival rate.21–23 No abnormal FDG uptake by the internal mammary region was detected in our study. However, Schirrmeister et al.13 reported that FDG-PET revealed foci corresponding to internal mammary node metastases in 33% of their patients. The high specificity of FDG-PET in detecting ALN metastases suggests that most of these parasternal lesions correspond to true-positive findings. FDG-PET might thus be useful for detecting internal mammary lymph node metastases in patients with central and inner-quadrant breast tumors undergoing SN biopsy. This could facilitate staging and, thus, patient selection for adjuvant systemic therapy.

In summary, we found that FDG-PET contributed little relative to the SN procedure in patients with early-stage breast cancer and no palpable ALNs. Because of its high false-negative rate, FDG-PET cannot replace histological evaluation of axillary node status. In contrast, FDG-PET emerged as a specific method for staging the axilla. For patients with positive FDG-PET findings, SN biopsy seems not to be indicated, and complete ALN dissection should be performed as the primary procedure.


   FOOTNOTES
 
Use of fluorodeoxyglucose positron emission tomography contributed little relative to the sentinel node procedure in patients with early-stage breast cancer and no palpable axillary lymph nodes.

Received for publication December 26, 2002. Accepted for publication March 31, 2003.


   REFERENCES
TOP
 ABSTRACT
 INTRODUCTION
 PATIENTS AND METHODS
 RESULTS
 DISCUSSION
 REFERENCES
 

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