Annals of Oncology Advance Access originally published online on December 12, 2006
Annals of Oncology 2007 18(3):473-478; doi:10.1093/annonc/mdl425
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© 2006 European Society for Medical Oncology
breast cancer |
A comparative study on the value of FDG-PET and sentinel node biopsy to identify occult axillary metastases
1 Scientific Director
2 Division of Nuclear Medicine
3 Division of Senology
4 Division of Epidemiology and Biostatistics
5 Division of Pathology, European Institute of Oncology, Milan
6 School of Medicine, University of Milan, Milan
7 Division of Anesthesiology, European Institute of Oncology, Milan, Italy
* Correspondence to: Dr U. Veronesi, Scientific Director, Istituto Europeo di Oncologia, Via G. Ripamonti 435, 20141 Milan, Italy. Tel: + 39 02 57489 224; Fax: + 39 02 57489 210; E-mail: umberto.veronesi{at}ieo.it
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Abstract |
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Background: Sentinel node biopsy (SNB) has become a standard treatment in staging axillary lymph nodes in early breast cancer. SNB, however, is an invasive procedure and is time-consuming when the sentinel node is analysed intra-operatively. Breast cancer is frequently characterised by increased 2-fluoro-2-deoxy-D-glucose uptake and many studies have shown encouraging results in detecting axillary lymph node metastases. The aim of this study was to compare SNB and -positron emission tomography (-PET) imaging, to assess their values in detecting occult axillary metastases.
Patients and Methods: In all, 236 patients with breast cancer and clinically negative axilla were enrolled in the study. 18-FDG-PET was carried out before surgery, using a positron emission tomography (PET)/computed tomography scanner. In all patients, SNB was carried out after identification through lymphoscintigraphy. Patients underwent axillary lymph nodes dissection (ALND) in cases of positive FDG-PET or positive SNB. The results of PET scan were compared with histopathology of SNB and ALND.
Results: In all, 103 out of the 236 patients (44%) had metastases in axillary nodes. Sensitivity of FDG-PET scan for detection of axillary lymph node metastases in this series was low (37%); however, specificity and positive predictive values were acceptable (96% and 88%, respectively).
Conclusions: The high specificity of PET imaging indicates that patients who have a PET-positive axilla should have an ALND rather than an SNB for axillary staging. In contrast, FDG-PET showed poor sensitivity in the detection of axillary metastases, confirming the need for SNB in cases where PET is negative in the axilla.
Key words: occult axillary metastases, positron emission tomography (PET), sentinel node biopsy
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introduction |
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TopAbstractintroductionpatients and methodsresultsdiscussionAcknowledgementsReferences |
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Axillary lymph node dissection (ALND) has been for a century an obligatory component of the surgical treatment of breast cancer. More recently, the increasing number of early breast cancer cases has lead to a reconsideration of the need for axillary dissection, as the majority of patients with carcinoma of the breast show no evidence of axillary lymph nodes involvement. Moreover, the dissection is today carried out mainly as a staging procedure, to know if occult metastases are present in the lymph nodes.
In the last 10 years, the procedure of sentinel node biopsy (SNB) has been progressively introduced to avoid unnecessary axillary dissection when the sentinel lymph node is not pathologically involved. SNB method, although simple and well accepted by the patients, prolongs the surgical session, requiring an extra time by the team of pathologists for extensive histological examination. In addition, there is a limited number of cases in whom the sentinel node (SN) is not identified.
For these reasons, and thanks to the progress of imaging research, there are many attempts to reach the diagnosis of axillary node involvement with non-invasive methods. One of them is positron emission tomography (PET) with fluorine-18-labelled 2-fluoro-2-deoxy-D-glucose (FDG), a method which may be able to detect clinically occult metastases. Many studies indicate that FDG-PET is able to identify, in a variable percentage of cases, occult axillary node metastases in patients with breast carcinoma with good results according to some authors [1–2] and less satisfactory ones according to others [3–6]. A good positive predictive PET value in case of maximal standardised uptake value index superior or equal to 1.8 was reported by Wahl et al. [3], with nevertheless a low sensitivity. Current data indicates that the accuracy of FDG-PET may change according to the method the pathologist uses for nodal specimen examination [7]. In fact, the implementation of serial slicing or immunohistochemistry applied to the SN has recently improved the diagnosis of micrometastases, which are usually not detected by PET scan.
The purpose of this study is a comparison of the two methods, SNB and FDG-PET imaging, to assess the respective values in detecting occult axillary metastases in early breast cancer.
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patients and methods |
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TopAbstractintroductionpatients and methodsresultsdiscussionAcknowledgementsReferences |
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From September 2003 to April 2005, 236 consecutive patients with breast carcinoma and clinically negative axilla were enrolled in the study. Neither patients with ductal carcinoma in situ nor those who had received neo-adjuvant chemotherapy were candidates. Patients with T1, T2 and T3 primary carcinomas were eligible for the study, provided that there was no clinical evidence of axillary metastases. All patients had a cytologically or histologically proven carcinoma, through fine-needle aspiration, core biopsy or excisional biopsy. The distribution of patients according to main characteristics is shown in Table 1.
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All patients underwent FDG-PET examination and SNB. If both procedures were negative, no axillary dissection was done. If one of the two, either PET or SNB, was positive, a total axillary dissection was carried out with the removal of the lymph nodes of all three levels.
FDG-PET imaging
PET scan was carried out for 1–15 days before surgery. In order to improve image quality and to suppress myocardial glucose utilisation, patients were asked to withdraw carbohydrates starting 24 h before the examination and to fast for at least 6 h before injection. Serum glucose was determined, selecting for the procedure patients with blood glucose levels <140 mg/dl. The glucose analogue fluorine-18-labelled FDG was supplied and quality controlled by IASON Labormedizin GesmbH & Co. KG, Graz-Seiersberg, Austria.
Intravenous (i.v.) administration of 5.3 MBq/kg of [18F]FDG was done in the arm opposite the primary breast tumour. After the injection, patients rested quietly for 45 min; they were asked to drink three glasses of water and to empty their bladder before positioning on the tomograph bed.
Images were obtained using a PET/computed tomography (CT) scanner (Discovery LS; GE Medical Systems, Waukesha, WI). Whole-body scan, starting 45 min after i.v. injection, was acquired from head basis to pelvis, with patients in supine position with arms extended above the head. The tomographic raw data were corrected for attenuation using transmission data derived from CT scan carried out before emission imaging.
Attenuation-corrected images were reconstructed in transaxial, coronal and sagittal planes and were separately interpreted by three experienced nuclear medicine physicians, on the basis of available clinical information (location and size of primary tumour). CT images were also available for evaluation. The interpreting physicians were blinded to any pathological assessment of the axilla. Visual analysis was carried out on digital transaxial CT, PET and fused images and evaluated with the following categories: 0 normal, 1 equivocal, 2 probably abnormal and 3 abnormal. Quantitative measurement of the single-pixel maximal standardised uptake value normalised to body weight (SUV bw max) was done on any breast and axillary area subjectively scored as one or higher. The study aimed at detecting subclinical nodal metastasis, any focal uptake greater than background activity was considered and PET findings were conclusively interpreted as abnormal if SUV bw max was 1.2 or greater (Figure 1).
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sentinel node biopsy
In all patients, the radioactive tracer was injected the evening before surgery. Nanocolloid particles of human serum albumin ASA (Nanocoll) were from Nycomed Amersham Sorin (Saluggia, VC, Italy). Nanocoll (NC) was reconstituted with 740 MBq of 99mTc in 3 ml of saline. Each single dose of 99mTechnetium-NC contained 7–10 MBq of 99mTc in a volume of 0.2 ml. The products were checked for free technetium, according to the manufacturer's instructions; in all cases <5% of free technetium was found.
Radiocolloids were injected in correspondence of the cutaneous projection of the lesion, as previously described [8]. After the administration, patients were invited to make a light, short massage on the injection point, in order to support the migration of the radiotracer.
Planar scintigraphic scans of the involved breast and axillary region, in anterior and anterior-oblique projections, were obtained 10–30 min after the radiotracer injection, collecting 150 kcounts per view. The skin projection of the first node (or nodes) taking up the tracer (defined as the SN) was marked with a suitable pen while the patient was supine with arm extended laterally at 90° to the body during the last acquisition. If no tracer was observed in the axillary region, at 30 min, additional planar scans were acquired up to 3 h after injection.
Fourteen to 20 h after the injection of tracer, SNB was carried out during breast surgery. A gamma ray-detecting probe in a sterile glove was used to identify the radioactive SN and facilitate its removal as previously described [8].
histopathology
The SN was bisected along its major axis, embedded (cut surfaces up) in optimum cutting temperature compound (CellPath) and frozen in isopentane cooled with liquid nitrogen. Lymph nodes <5 mm in diameter were embedded and frozen uncut [9].
For each node that was large enough to be cut, 15 pairs of frozen sections were cut at 50-µm intervals in each half of the node, amounting to about 60 sections per node. If residual tissue was left, additional pairs of sections were cut at 100-µm intervals until the lymph node had been sampled completely. One section of each pair of section was stained with haematoxylin and eosin (H&E). In case of findings suspicious for malignancy in H&E-stained preparations, the other section was stained for cytokeratins by means of a rapid method (EPOS cytokeratin reagent horseradish peroxidase, Dako Glostrap, Denmark) and stained for the mAb MNF116 [10]. Whole procedure was done intra-operatively.
If the SN contained metastases, the dimensions of the metastatic focus or foci were recorded. The definition of micrometastases was applied when a single metastatic focus with the larger diameter <2 mm was present.
The lymph nodes removed during complete axillary dissection were examined by standard techniques. Three to six sections were obtained from each lymph node at different levels 100–500 µm apart and stained with H&E.
evaluation
The two methods FDG-PET and SNB were evaluated by comparing their results separately with the final histology. The pathologists were blinded to the FDG-PET results. The results were classified as true positive (TP), true negative (TN), false positive (FP) and false negative (FN).
The evaluation of the results was based on calculation of sensitivity [TP/(TP + FN)], specificity [TN/(TN + FP)], positive predictive value [TP/(TP + FP)] and negative predictive value [TN/(TN + FN)].
The overall accuracy was calculated as the percentage of all TP and TN cases out of the total number of cases.
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results |
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TopAbstractintroductionpatients and methodsresultsdiscussionAcknowledgementsReferences |
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positive FDG-PET
FDG-PET was positive in the axilla in 43 cases (18.2%). These cases all had a total ALND following SNB. In 34 cases the SNB was also positive, while in nine cases the SNB was negative. Among these nine cases, axillary dissection showed negative nodes in five cases and positive nodes in four cases. In this subgroup of patients, SNB was therefore more informative than FDG-PET in five cases, while FDG-PET identified a positive axilla in four cases that were negative at the SNB (Figure 2).
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negative FDG-PET
FDG-PET was negative in 193 patients (81.8%). In 128 patients the SNB was also negative, while in 65 the SNB was positive. Therefore, in this latter group, FDG-PET was unable to detect occult axillary metastases in one-third of cases (Figure 2). The results of the FDG-PET are summarised in Table 2, where it appears that specificity and positive predictive value have acceptable values while sensitivity and negative predictive value show unacceptable low percentages.
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value of FDG-PET and SNB according to different variables
When patients were analysed according to age and menopausal status, FDG-PET showed increased overall accuracy in older age and in post-menopausal women. A number of variables (size, proliferative rate, grade and peritumoural vascular invasion of primary carcinoma) were also evaluated (Table 3). No important differences were found in the various subgroups of patients. If we split the results by histological type, however, we observe that the overall accuracy of the lobular type is inferior to that of the ductal type (Table 3). Nevertheless, the false-negative rate is similar in both categories: 37% (10 out of 27) for the lobular versus 35% (51 out of 144) for the ductal category.
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An analysis according to the size of the primary carcinoma shows that the risk for positive axillary nodes increases with diameter as expected. We had 43 cases with a maximum diameter <1 cm, with axillary involvement in 12 cases (28%). In the 24 cases >4 cm, 15 had a positive axilla (62%). The overall accuracy of FDG-PET, however, did not change between the two groups (79% in cases with very small tumours and 75% in very large tumours).
A specific evaluation was done considering the uptake of the FDG in the primary carcinoma and its proliferative rate. In 49 patients, FDG-PET was negative in the primary carcinoma. In all cases the axilla was also PET negative. The majority of these cases had no axillary metastases (38 out of 49, 77%), so that the FDG-PET negativity on the primary carcinoma might be considered a good predictive marker. Among the 187 patients, where the primary carcinoma was PET positive, axillary metastases were present in 88 (47%), so that PET positivity of the primary carcinoma appeared to be an unfavourable factor. Subdividing the patients according to the proliferative rate (Ki67) showed that the specificity of FDG-PET is good in all cases, while its sensitivity is low, although somewhat better in cases with higher proliferative rates. FDG-PET was unable to identify micrometastases in the lymph nodes: out of 28 cases with micrometastatic axillary involvement (<2 mm) only in three of them FDG-PET was positive. When SN metastases were 2–5 mm in size, the ability of PET to identify them was also very low (six out of 25 cases, 24%). When the size of the metastases was >5 mm (51 cases), PET was positive in 57% of the cases (Table 4). This observation is in line with the recent study of Reinhardt et al. [11] on pulmonary metastases reporting a reduced sensitivity of FDG-PET for lesions <11 mm.
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discussion |
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TopAbstractintroductionpatients and methodsresultsdiscussionAcknowledgementsReferences |
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The study presented here is part of a programme aimed at reducing invasive procedures in staging of the regional lymph nodes.
There is evidence that axillary dissection is not an essential therapeutic procedure, but mainly important as a staging method as demonstrated by the National Surgical Adjuvant Breast and Bowel Project (NSABP) trial 04 [12], which showed no difference in survival between patients receiving immediate axillary dissection versus patients receiving axillary dissection only when axillary metastases occurred during follow-up. Similar results were obtained in our study [13] which showed no survival difference in women with small primary tumours and a clinically negative axilla, who received no primary treatment to the axilla versus radiotherapy to the axilla, at the time of primary breast surgery.
The introduction of SNB represented an important advance and today has largely replaced traditional axillary dissection, when axillary nodes are clinically negative [14].
The increasing progress in imaging techniques, however, stimulates further researches into refining the use of SNB which, although well tolerated by patients, requires a prolonged surgical session, the execution of lymphoscintigraphy and a considerable pathological work-up.
There are two promising lines of development, the first with the use of FDG-PET and the second with advanced techniques of ultrasound examination of axillary nodes assisted with fine-needle biopsy which, however, requires further investigation.
We believe that in future, if the next generation of clinical study will validate the two methods, a ‘wait and see’ policy may be considered possible, especially in patients with primary carcinoma of small size. This policy is reinforced by two additional considerations. The first is that the presence of a micrometastasis in the sentinel lymph node in the future might not require a dissection if the randomised trial in progress will show no differences in outcome between the axillary dissection and the wait and see policy [15]. The second is that the role of regional node mapping in the staging of breast cancer will likely lose importance in the future as more sophisticated biological and biomolecular markers will be available from the analysis of the primary carcinoma.
In the present study, we have evaluated the ability of FDG-PET examination of the axillary nodes to detect occult metastases. The results obtained in this large series are in agreement with several previous studies which demonstrated poor sensitivity of the examination in detecting axillary node metastases in early breast cancer [16–21] and with a recent study published by Reinhardt et al. [11] mentioning the sensitivity PET values for the detection of lung metastases according to its size. The important finding in our study is that in 38 out of 43 cases with positive axillary FDG-PET, the lymph nodes contained metastases of various sizes, some very tiny. Therefore, whenever the FDG-PET shows axillary uptake, the likelihood of metastases in axillary nodes is very high and the patients might be submitted directly to the axillary dissection without the need of SNB. On the contrary, when FDG-PET is negative at the axilla, its reliability is very low and axillary SNB becomes imperative.
Whether the advantage to avoid the SNB in limited number of FDG-PET-positive axilla will justify an extensive use of this expensive procedure is a matter of discussion. We believe that a selection of cases will be needed. As an example, we would consider reasonable the use of pre-operative FDG-PET in those cases where clinical examination of the axilla shows the presence of palpable nodes suspicious of involvement. Also in clinically positive cases, the confirmed positivity by FDG-PET makes the dissection imperative. On the other hand, it must be underlined that FDG-PET whole-body examination is a staging procedure which might make other traditional examinations such as bone scan and liver ultrasound examination unnecessary, provided that bone metastases are not purely osteoblastic [22–23)]. Nevertheless, an evaluation in economic terms of FDG-PET examination at first and then lymphoscintigraphy with SNB technique in case of PET negativity could be succinctly evoked and eventually deeply carried out in a subsequent study. Finally, as in some 25% of the cases primary carcinomas are FDG-PET negative, the assessment of Glut-1 presence [24–25] on biopsy specimen may be considered to select patients who are likely to have a FDG-avid cancer in order to have a rationale for imaging in staging and during the follow-up.
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Acknowledgements |
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TopAbstractintroductionpatients and methodsresultsdiscussionAcknowledgementsReferences |
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We wish to acknowledge Associazione Italiana per la Ricerca sul Cancro, American Italian Cancer Foundation and Jacqueline Seraussi Foundation for their support.
Received for publication June 16, 2006. Revision received October 6, 2006. Accepted for publication October 16, 2006.
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TopAbstractintroductionpatients and methodsresultsdiscussionAcknowledgementsReferences |
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