Original Research
Nuclear Medicine and Molecular Imaging
November 23, 2012

Supraclavicular Lymph Nodes Detected by 18F-FDG PET/CT in Cancer Patients: Assessment With 18F-FDG PET/CT and Sonography

Abstract

OBJECTIVE. The purposes of this study were to assess the diagnostic accuracy of 18F-FDG PET (FDG PET) for the detection of metastatic supraclavicular lymph nodes (LNs) and to propose an optimal diagnostic strategy with additional sonography, contrast-enhanced CT (CECT), or both.
MATERIALS AND METHODS. One hundred supraclavicular LNs initially detected using FDG PET were examined using sonography. Regardless of the imaging findings, all 100 supraclavicular LNs underwent sonography-guided fine-needle aspiration biopsy. The maximum standardized uptake values (SUVsmax) of the supraclavicular LNs were measured, and a receiver operating characteristic (ROC) analysis was performed to determine the cutoff SUVmax. Then we evaluated the diagnostic performance of FDG PET and figured out the optimal combination of FDG PET and sonography or CECT to improve the diagnostic accuracy of the imaging studies and minimize procedures.
RESULTS. In total, 86 of 100 PET-detected supraclavicular LNs were malignant. With application of the cutoff value obtained by ROC analysis (SUVmax = 3.0), the diagnostic accuracy of FDG PET was 75.0% with a sensitivity of 74.4% and specificity of 78.6%. For supraclavicular LNs with an SUVmax of more than 3.0, FDG PET showed a positive predictive value of 95.5%; for supraclavicular LNs with an SUVmax of 3.0 or less, sonography excluded all false-negative FDG PET cases and showed a high negative predictive value of 100%. When sonography was selectively applied to cases with an SUVmax of 3.0 or less, the overall diagnostic accuracy increased to 92%.
CONCLUSION. Our study revealed a high incidence rate of metastasis in PET-detected supraclavicular LNs in cancer patients. We believe that our proposed diagnostic workflow could decrease unnecessary diagnostic procedures in the evaluation of PET-positive supraclavicular LNs in cancer patients with reliability.
Cervical lymph node (LN) metastasis generally indicates a worse clinical prognosis and the impossibility of potentially curative treatment particularly in patients with primary cancer below the clavicle [1, 2]. Therefore, detection of these nodes before treatment or during posttreatment follow-up is very important for therapeutic control. Furthermore, the involvement of supraclavicular LNs is especially important to identify because they are commonly involved in cancers of the abdomen and pelvis [3].
Fluorine-18-FDG PET (FDG PET) is widely used for the initial evaluation of tumors or monitoring treatment response in many cancers. FDG PET can detect small cervical LN metastases before they are palpable [1, 4]. Furthermore, FDG PET can be used to screen the entire body to detect distant metastases that could be missed by conventional staging workup. However, FDG is a metabolic tracer and not a tumor-specific tracer. Some benign lesions such as inflammation may reveal a high rate of glucose metabolism. In addition, false-negative results can also occur in cancers with low FDG avidity or in small malignant lesions. Therefore, pathologic examination is still necessary to determine the nature of these suspicious LNs while formulating a treatment plan.
The role of sonography in evaluating cervical lymphadenopathy using gray-scale and power Doppler features has been well established [57]. Furthermore, ultrasound-guided fine-needle aspiration biopsy (FNAB) allows cytologic examination of small nodes that have suspicious imaging findings with reliable diagnostic accuracy [810]. Therefore, sonography examination with sonography-guided FNAB may be a proper procedure to confirm the diagnosis of cervical LNs including supraclavicular LNs.
Most supraclavicular LNs detected by FDG PET are routinely examined on sonography and sequentially ultrasound-guided FNAB. However, few reports have been published in the literature regarding guidelines that can be used to select suitable patients to be evaluated by sonography-guided FNAB. To our knowledge, no data of large groups have been published to establish criteria for ultrasound-guided FNAB after FDG PET. The purpose of our study was to elucidate an efficient diagnostic strategy by complementary application of sonography and contrast-enhanced CT (CECT) for PET-detected supraclavicular LNs in cancer patients.

Materials and Methods

Subjects

The institutional review board of our university approved this study and waived the informed consent requirement. We retrospectively reviewed the medical records of cancer patients who underwent initial FDG PET from December 2007 to July 2009. We included supraclavicular LNs either showing any discernible FDG uptake on PET images or measuring larger than 1 cm on CT images regardless of FDG uptake. Among them, we included only cases with sonography studies and cytology results from FNAB. Finally, 100 supraclavicular LNs of 89 patients were enrolled in this study (40 men and 49 women; mean age, 55 years; age range, 32–78 years).

FDG PET and Contrast-Enhanced CT

All patients underwent FDG PET on a PET/CT unit (Discovery STe, GE Healthcare; or Biograph TruePoint 40, Siemens Healthcare). All patients fasted for at least 6 hours before imaging, and the glucose level in peripheral blood was confirmed to be 140 mg/dL or less before FDG injection. A dose of approximately 5.5 MBq/kg of body weight of FDG was administered IV 1 hour before image acquisition. After the initial low-dose CT study (Discovery STe, 30 mA, 130 kVp; Biograph TruePoint, 36 mA, 120 kVp), a standard PET protocol was used to scan from the neck to the proximal thighs with an acquisition time of 3 minutes per bed position in the 3D mode. Images were then reconstructed using ordered subset expectation maximization (2 iterations, 20 subsets).
CECT was performed on a 16-MDCT unit (Somatom Sensation 16, Siemens Healthcare) or a 64-MDCT unit (Sensation 64, Siemens Healthcare). Scanning was performed using the helical technique during a single breath-hold after injection of contrast material with patients in the supine position. A total of 100–130 mL of iopromide (Ultravist 300, Bayer HealthCare) was administered IV at a rate of 3–4 mL/s to all patients using a power injector (Envision CT, Medrad). Scan acquisition was initiated immediately after enhancement of the thoracic aorta had reached 100 HU as measured using a bolus-tracking technique. To obtain CT images, we used the following parameters: 120 kVp, 130 effective mAs, 0.5-s gantry rotation, 0.75-mm collimation, and a 0.5-mm interval. Two image sets were reconstructed with thicknesses of 5.0 and 1.0 mm, respectively, using a standard algorithm from the same raw data. The scanning area ranged from the neck to the proximal thighs. All scans were analyzed in the mediastinal and lung window settings. All CT images were retrieved on a PACS (Centricity, GE Healthcare) so readers could freely handle the images for the evaluation of lesions.
Sonography was performed for evaluation of supraclavicular LNs using an HDI 3000 or 5000 unit (ATL–Philips Healthcare) or Sequoia 512 unit (Acuson).

Image Analysis

FDG PET images were reviewed at interactive workstations by two nuclear medicine physicians. Readers were blinded to the results of the other imaging modalities and to cytopathologic results at the time of review. For semiquantitative analysis, a region of interest (ROI) was drawn for primary tumors and supraclavicular LNs on the transverse section where the lesion appeared to have the largest uptake according to size and intensity. The maximum standardized uptake value (SUVmax) was calculated at ROIs on supraclavicular LNs.
CECT images were retrospectively evaluated in consensus by two experienced radiologists who did not have knowledge of the other imaging results or clinical data. LNs with diameters larger than 1 cm were defined as malignant. The presence of central necrosis was also considered another sign of malignancy, and the presence of a fatty hilum within an LN was considered a sign of benignity regardless of node size [1113].
For the evaluation of sonography, we considered a supraclavicular LN to be malignant if it showed any suspicious findings for malignancy. Suspicious findings for malignancy were as follows: marked hypoechogenicity or hypoechogenicity [14], round or irregular shape [1, 2, 46], eccentric cortical thickening or replaced fatty hilum [79], and a short axis of greater than 0.8 cm [4, 1013].

Statistical Analysis

LNs were divided into two groups, malignant and benign, on the basis of cytopathologic results and were further evaluated by the location of the primary tumor. SUVmax values of primary tumors and LNs were measured. To evaluate the diagnostic performance of FDG PET in differentiating malignant LNs from benign ones, we obtained a cutoff value of SUVmax by receiver operating characteristic (ROC) curve analysis and then calculated the diagnostic performance of FDG PET in terms of sensitivity, specificity, positive predictive value (PPV), negative predictive value (NPV), and accuracy.
Because the purpose of our study was to propose an efficient diagnostic algorithm for PET-detected supraclavicular LNs in everyday practice, we considered sonography and CECT as complementary modalities to FDG PET. Under a given PET criterion, we sequentially applied sonography and CT criteria to reduce either false-negative or false-positive results to achieve better diagnostic accuracy while minimizing diagnostic procedures. All differences were considered statistically significant at p < 0.05.

Results

Patient Characteristics

The primary types of cancers were as follows: lung (n = 22), breast (n = 14), stomach (n = 10), uterine cervix (n = 9), ovary (n = 6), thyroid (n = 6), esophagus (n = 3), Hodgkin lymphoma (n = 3), parotid gland (n = 3), pancreas (n = 2), larynx (n = 2), colon (n = 1), maxillary sinus (n = 1), and skin (n = 1). Metastasis from any cancer below the diaphragm (n = 39) always involved the supraclavicular LNs on the left side, whereas other cancers above the diaphragm did not show any side predilection.
Supraclavicular LNs were confirmed to be malignant by FNAB in 86 of the 100 enrolled subjects. The remaining 14 patients were determined to have benign lesions including eight instances of reactive hyperplasia, one instance of tuberculosis, and five cases without specific findings. Of the 86 supraclavicular LN metastases, 54 cases involved the left supraclavicular LNs (63%) and 32 cases, the right supraclavicular LNs (37%).

PET Findings

The mean SUVmax value (± SD) of the supraclavicular LNs in patients with confirmed metastasis was 5.99 ± 4.00 (range, 1.05–18.18), whereas that of benign lesions was 2.76 ± 2.40. The SUVmax values of metastatic lesions were significantly higher than those of benign lesions (p < 0.05) (Table 1).
ROC curve analysis indicated that the cutoff value with the best diagnostic accuracy was 2.94, which provided a sensitivity of 76.7%, specificity of 78.6%, and area under the ROC curve of 0.790. When we simplified the cutoff value as 3.0, sensitivity, specificity, accuracy, PPV, and NPV were 74.4%, 78.6%, 75.0%, 95.5%, and 33.3%, respectively.
TABLE 1: Maximum Standardized Uptake Values (SUVsmax) in Malignant and Benign Supraclavicular Lymph Nodes
With 3.0 as the cutoff value for SUVmax, there were three false-positive and 22 false-negative cases. Of the three false-positive cases, two were confirmed as reactive hyperplasia and the other was negative for malignancy. In the false-negative group, LNs were significantly smaller (mean ± SD, 1.11 ± 0.44 cm vs 1.88 ± 0.91 cm, respectively) and the SUVmax values of their primary cancers were lower (mean ± SD, 6.52 ± 4.08 vs 9.54 ± 5.27) than those in the true-positive group.

Diagnostic Workup Flow With FDG PET and Sonography

The PPV of FDG PET was as high as 95.5%, but its NPV was only 33.3%. To improve diagnostic accuracy, we designed a diagnostic workup flow by combining modalities to decrease the number of false-negative cases. The sonography and CECT findings of supraclavicular LNs with an SUVmax of 3.0 or less are summarized in Table 2. When the sonography criterion was applied for supraclavicular LNs with an SUVmax of 3.0 or less (n = 33), its sensitivity was 100% and sonography could exclude all metastases from 22 cases with false-negative FDG PET findings. The same analysis was performed with CECT criterion, and we found that only 11 false-negative cases of FDG PET could benefit from application of the CECT criterion. As a result, when sonography was used to assess supraclavicular LNs with FDG uptake values of 3.0 or less, the diagnostic performance of the imaging workup could be improved (Table 3).
TABLE 2: Diagnostic Performance of Sonography and Contrast-Enhanced CT (CECT) in the Differentiation of Supraclavicular Lymph Nodes With a Maximum Standardized Uptake Value of 3.0 or Less
The suggested diagnostic workflow is illustrated in Figure 1; when this workflow was applied to our cases, we found that the sonography study could be omitted in 67 cases with an SUVmax of greater than 3.0 and that biopsy could be selectively performed on supraclavicular LNs with any suspicious sonography finding; as a result, only three cases remained misdiagnosed.

Discussion

Because of the high lesion-to-background contrast of the supraclavicular fossa, FDG PET can be used to detect any small focus with increased FDG uptake. Our results showed the high PPV of FDG PET in differentiating benign from malignant supraclavicular LNs and suggested a diagnostic workflow of imaging modalities by combining FDG PET and selective sonography.
The incidence of malignant supraclavicular LNs in this study was higher than those in previous studies that reported rates of 55–80% [1416]. Despite the difference in inclusion criteria and diagnostic modalities, our results are consistent with previous findings in that any supraclavicular LN detected by PET in cancer patients had a high prevalence of metastasis. Most primary sites of cancers of enrolled patients were below the clavicles, and supraclavicular LN metastasis is indicative of inoperability and a poor prognosis. Therefore, we suggest that an aggressive diagnostic approach be required for cases with FDG uptake in the supraclavicular fossa especially in cancers below the clavicles. Regarding the involved side, there was no significant side predilection among cancers above the clavicle, but all cancers below the diaphragm involved the left supraclavicular LNs. Our results do not differ from previously reported data [14, 17].
Regarding the diagnostic accuracy of FDG PET in this study, the NPV could be irrelevant because we included only PET-positive supraclavicular LNs. However, our study focused on the next diagnostic procedure after a supraclavicular LN was detected on FDG PET not on the detectability of metastatic supraclavicular LNs. For convenience, we determined the cutoff for SUVmax to be 3.0 after ROC analysis revealed that diagnostic performance was best at a cutoff value of 2.94. The increase from 2.94 to 3.0 resulted in a slight decrease of sensitivity and PPV but accuracy was not affected. We also tried a cutoff value of 2.9, but there was sacrifice of accuracy. FDG PET is a modality for functional imaging, so it can be expected to show higher diagnostic accuracy than sonography, a modality for anatomic imaging. In some cases, FDG PET was superior to both sonography and CECT (Figs. 2A, 2B, and 2C), but the relatively large number of false-negative FDG PET cases resulted in lower accuracy. Among the three modalities, differential diagnosis based on our sonography grading scale was the most reliable in differentiating malignant LNs from benign lesions. Moreover, recent technical advances in ultrasound probes enable higher resolution of sonography, so sonography has become superior to other imaging modalities in evaluating morphologic changes of superficial structures including the cervical LNs (Figs. 3A, 3B, and 3C).
TABLE 3: Change of Diagnostic Performance with Complementary Application of Sonography and Contrast-Enhanced CT (CECT)
CECT showed diagnostic accuracy comparable to that of FDG PET, but the low predictive values of CECT compromised its reliability. Regarding CECT, the most reliable criterion was lesion size in our study. Because of the diversity in primary cancers, the incidence of necrotic or coalescent LNs was relatively low when compared with published data for patients with head and neck cancer. Moreover, the morphologic evaluation of CECT was inevitably inferior to that of sonography, particularly for small LNs, which can account for the low diagnostic performance of CECT in our study.
The diagnostic capability of FDG PET is often limited by cellular activity. The degree of FDG uptake varies according to the pathology of the lesion, and the diagnostic accuracy of FDG PET is low in cancers with low FDG avidity. A correlation between FDG uptake and pathology could not be fully elucidated in this study because the enrolled subjects presented with a variety of cancers. However, SUVmax values of the primary site in the false-negative group were significantly lower than those of the true-positive group in this study. It is likely that supraclavicular LN metastases from primary cancer with low metabolic activity also have low metabolic activity, resulting in low sensitivity.
Fig. 1 Schematic diagram shows suggested diagnostic workflow of PET-detected supraclavicular lymph nodes. SUVmax = maximum standardized uptake value, PPV = positive predictive value.
Fig. 2A 47-year-old woman with left breast cancer.
A, PET scan shows focal areas of increased FDG uptake with maximum standardized uptake value of 5.79 in left supraclavicular fossa.
Fig. 2B 47-year-old woman with left breast cancer.
B, Contrast-enhanced CT scan reveals lymph node is less than 1 cm.
Fig. 2C 47-year-old woman with left breast cancer.
C, False-negative sonography. Sonogram shows well-defined, 0.68-cm, oval lymph node (cursors). Biopsy results confirmed presence of metastasis.
FDG uptake by small tumor cell deposits is often poorly depicted owing to the partial volume effect [18]. Moreover, the spatial resolution of PET scanners has a technical limit of 4–5 mm. This limitation is consistent with our result that the smallest PET-detected LN was 5.6 mm in diameter. However, the detectability of malignant lesions by PET was inconsistent because all subjects had supraclavicular LN lesions detected by PET. Such technical limits appeared to bias the evaluation of FDG uptake and calculation of SUV. This effect typically occurs whenever the size of the tumor is less than threefold the full width at half-maximum (FWHM) of the reconstructed image resolution [19]. We concluded that the spatial resolution limitations of FDG PET were responsible for the false-negative PET results in this study. The use of PET scanners with a higher resolution or tumor-specific tracers may increase the capacity of PET to detect small LN metastases.
Our next step was to determine methods to complement the accuracy of PET when it was performed as an initial diagnostic procedure. FDG PET showed the highest PPV of 95.5%, but the high incidence of false-negatives was the main cause of its low NPV. The false-negative group had significantly smaller lesion diameters, which would hinder PET from reflecting the actual metabolic activity of the tumors. In this study, the key to this problem was sonography. Published studies reported high specificity values of sonography ranging from 81% to 97% [2024], but to our knowledge, no data specific for PET-positive cervical LNs have been published in the literature. In our study, sonography showed a sensitivity of 100%, specificity of 42.9%, PPV of 91.5%, and NPV of 100% (data not shown); however, these results seemed statistically less significant because of the narrowed selection criteria. We suppose another probable explanation is the characteristics of involved supraclavicular LNs; in other words, the high incidence of metastatic LNs in this study might have contributed to the relatively low specificity. Nevertheless, it is noteworthy that sensitivity and NPV of sonography were very high.
Fig. 3A 64-year-old man with stomach cancer.
A, PET image shows focal areas of mildly increased FDG uptake with maximum standardized uptake value of 1.45 in left supraclavicular fossa.
Fig. 3B 64-year-old man with stomach cancer.
B, Contrast-enhanced CT scan reveals multiple lymph nodes that are about 1 cm.
Fig. 3C 64-year-old man with stomach cancer.
C, Sonogram shows round, 1.2-cm hypoechoic lymph node (cursors) with replaced fat hilum. Biopsy of largest lymph node was performed and confirmed metastasis.
We propose an efficient diagnostic workup that is based on our results (Fig. 1). When a supraclavicular LN had an SUVmax of greater than 3.0 on the FDG PET scan, we could reliably presume that the LN was malignant with a PPV of 95.5% (64/67). Otherwise, complementation of FDG PET findings with sonography would help in the differential diagnosis; sonography could exclude all benign LNs among 33 supraclavicular LNs with an SUVmax of 3.0 or less. In this proposed diagnostic workup, we could significantly minimize the number of additional diagnostic steps with good diagnostic reliability. In addition, based on our results, CECT appeared to be ineffective for further evaluation of PET-detected supraclavicular LNs when considering the extra radiation exposure without incremental outcome in comparison with sonography.
There were limitations to our study. First, the retrospective nature of our study resulted in selection bias. Only PET-positive LNs are not subject to biopsy; in other words, supraclavicular LNs detected on CT are frequently biopsied regardless of FDG uptake. On the contrary, ultrasound-guided FNAB was not actually performed on every PET- or CT-detected supraclavicular LN, particularly when supraclavicular metastasis had no influence on the therapeutic plan or when metastasis was obvious on radiographic imaging. According to our review, only approximately 25% of PET-detected supraclavicular LNs underwent biopsy in our institute and clinicians' decision about whether to recommend biopsy mainly depended on whether sonography and biopsy results would change the therapeutic plan. As a result, there is a lack of information on PET-detected supraclavicular LNs excluded in this study for such reasons and the incidence of supraclavicular metastasis reported here may not reflect the true incidence.
Second, our study size was small, and enrolled subjects had a high incidence of malignancy. This condition might statistically exaggerate the false-negative rate and explain the low specificity of each imaging modality. The number of enrolled patients was insufficient to permit further evaluation based on specific cancers. Further investigation is required to evaluate the diagnostic performance based on tumor pathology and to devise a pathology-specific diagnostic workup.
Third, the diagnostic value and availability of CECT could differ according to types of cancers, specifications of CT machines, and protocols of studies. We suggest additional CECT was inefficient for the further evaluation of supraclavicular LNs; however, for lung and for head and neck cancers, CECT is indispensable for a baseline study and can cover bilateral supraclavicular fossae. Moreover, such CT machines usually have higher resolution and more imaging protocols than CT units that are integrated in PET/CT scanners.
In conclusion, our study revealed a high incidence rate of metastasis in PET-detected supraclavicular LNs in cancer patients. For supraclavicular LNs with SUVmax values of greater than 3.0, FDG PET had a high PPV that could minimize the need for further diagnostic procedures. Regarding supraclavicular LNs with SUVmax values of 3.0 or less, additional sonography could complement the low diagnostic performance of PET, and differential diagnosis by sonography produced reliable results in this group. We found that the diagnostic workup of PET-detected supraclavicular LNs could be optimized by selective application of sonography with reliability.
APPENDIX 1: AJR Journal Club

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Information & Authors

Information

Published In

American Journal of Roentgenology
Pages: 187 - 193
PubMed: 22194496

History

Submitted: April 8, 2011
Accepted: July 21, 2011

Keywords

  1. cancer
  2. FDG PET
  3. oncologic imaging
  4. sonography
  5. standardized uptake value
  6. supraclavicular lymph node

Authors

Affiliations

Jae-hoon Lee
Department of Radiology, Division of Nuclear Medicine, Research Institute of Radiological Science, Yonsei University College of Medicine, 134 Shinchon-dong, Seodaemun-gu, Seoul 120-752, South Korea.
Jinna Kim
Department of Radiology, Research Institute of Radiological Science, Yonsei University College of Medicine, Seoul, South Korea.
Hee Jung Moon
Department of Radiology, Research Institute of Radiological Science, Yonsei University College of Medicine, Seoul, South Korea.
Arthur Cho
Department of Radiology, Division of Nuclear Medicine, Research Institute of Radiological Science, Yonsei University College of Medicine, 134 Shinchon-dong, Seodaemun-gu, Seoul 120-752, South Korea.
Mijin Yun
Department of Radiology, Division of Nuclear Medicine, Research Institute of Radiological Science, Yonsei University College of Medicine, 134 Shinchon-dong, Seodaemun-gu, Seoul 120-752, South Korea.
Jong Doo Lee
Department of Radiology, Division of Nuclear Medicine, Research Institute of Radiological Science, Yonsei University College of Medicine, 134 Shinchon-dong, Seodaemun-gu, Seoul 120-752, South Korea.
Won Jun Kang
Department of Radiology, Division of Nuclear Medicine, Research Institute of Radiological Science, Yonsei University College of Medicine, 134 Shinchon-dong, Seodaemun-gu, Seoul 120-752, South Korea.

Notes

Address correspondence to W. J. Kang ([email protected]).

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