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Head and Neck Cancer: Dedicated FDG PET/CT Protocol for Detection—Phantom and Initial Clinical Studies¹

¹ From the Department of Radiology, Nuclear Medicine Division, Duke University Medical Center, Durham, NC. Received January 9, 2006; revision requested March 9; revision received April 6; accepted May 10; final version accepted October 1. Address correspondence to Y.Y., Department of Radiology, Faculty of Medicine, Kagawa University, 1750-1 Ikenobe, Miki-cho, Kita-gun, Kagawa 761-0793, Japan (e-mail: yuka{at}kms.ac.jp).

	ABSTRACT

TOP ABSTRACT INTRODUCTION MATERIALS AND METHODS RESULTS DISCUSSION ADVANCE IN KNOWLEDGE References

 
Purpose: To retrospectively compare the sensitivity of a dedicated fluorine 18 fluorodeoxyglucose (FDG) positron emission tomography (PET)/computed tomography (CT) protocol versus a standard whole-body PET/CT protocol for detection of head and neck cancer, with biopsy and follow-up as reference standards.

Materials and Methods: Institutional review board approval and informed consent were obtained for this HIPAA-compliant study. Dedicated and standard PET/CT protocols were performed in a phantom and in 55 patients suspected of having head and neck cancer (28 men, 27 women; age range, 21–79 years). The neck phantom contained four 4.4–9.8-mm-diameter spheres. Standard protocol consisted of a midcranium to proximal thigh emission scan of 2–4 minutes per bed position. Dedicated protocol was an 8-minute head and neck scan. Reconstructed field of view and pixel size, respectively, were 30 cm and 2.34 mm for the dedicated and 50 cm and 3.91 mm for the standard protocol. FDG uptake was evaluated visually and semiquantitatively by using standardized uptake values (SUVs). Mean SUV was compared between dedicated and standard protocols with a t test modified for clustered sampling. Receiver operating characteristic (ROC) curves were calculated. A two-tailed P value was used.

Results: In the phantom study, a larger percentage difference (20%–27%) in sphere-to-background ratios with the dedicated than with the standard protocol was observed for 6.0–9.8-mm spheres. In the clinical study, a total of 149 lymph nodes were identified. Five malignant and six benign lymph nodes (mean diameter, 7.1 mm) were visually identified with the dedicated protocol only. SUVs with the dedicated protocol were significantly higher than those with the standard protocol (P < .001). Area under the ROC curve was 0.94 for the dedicated and 0.92 for the standard protocol (P = .56).

Conclusion: FDG PET with either the standard or dedicated protocol was more sensitive than CT for evaluating head and neck lymph nodes. The dedicated protocol improved the detectability of smaller nodes.

© RSNA, 2007

	INTRODUCTION

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Positron emission tomography (PET) with fluorine 18 fluorodeoxyglucose (FDG) is a well-established functional diagnostic oncologic imaging technique that provides glucose metabolism information about lesions (1). Whole-body FDG PET is increasingly used for staging and restaging in patients, including those with head and neck cancer (1–13). Hybrid PET/computed tomographic (CT) scanners have been developed that enable highly precise localization of the metabolic abnormalities seen at PET with high-spatial-resolution CT images (14–17).

With CT and magnetic resonance imaging in head and neck cancer, the sensitivity for detection of lymph node involvement ranges from 60% to 88%, and the specificity ranges from 58% to 86% (2–6). There have been many studies of FDG PET in the detection of lymph node involvement in head and neck cancer, and, overall, the data show that PET is both more sensitive (70%–95%) and more specific (78%–97%) than conventional imaging (2–6,18). PET instrumentation has improved since its development, and whole-body PET systems typically yield reconstructed images with a resolution of 6–9 mm. However, the ability of PET to depict small structures is limited by image quality, which includes the effects of limited counts (image noise) and spatial resolution. The final image resolution is affected by the system's intrinsic resolution and by any noise-controlling smoothing that has been performed, either overtly or with limited numbers of reconstruction iterations. For structures less than twice the reconstructed image resolution, the true amount of activity is not completely depicted (19). As a result, lesions less than 1 cm in diameter are detected less accurately than lesions greater than 1 cm in diameter. More than 40% of cervical lymph node metastases have been found to be present in lymph nodes smaller than 1 cm (20). Thus, the purpose of our study was to retrospectively compare the sensitivity of a dedicated FDG PET/CT protocol and a standard whole-body PET/CT protocol in the detection of head and neck cancer, with biopsy and follow-up as reference standards.

	MATERIALS AND METHODS

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PET/CT Scanner
All acquisitions were performed by using an integrated PET/CT scanner (21) (Discovery ST; GE Medical Systems, Waukesha, Wis). The imaging system enabled the simultaneous acquisition of 47 transverse PET images per field of view with intersection spacing of 3.27 mm, for a total transverse field of view of 15.7 cm. The intrinsic transverse PET resolution is approximately 6.1 mm full width at half maximum near the center of the field of view. PET scans were acquired in the two-dimensional mode. This PET/CT system also includes a 16–detector row helical CT scanner. The technical parameters used for CT imaging were as follows: a detector row configuration of 16 x 1.25 mm, a pitch of 1.375:1, a gantry rotation speed of 0.5 second, a table speed of 27.5 mm per gantry rotation, 140 kVp, and 30–300 mA. We used the system's current-modulation capability to achieve uniform image quality automatically over a range of body sizes.

Data Acquisition and Image Reconstruction
The CT images were used not only for image fusion but also for generation of the attenuation map for attenuation correction. PET images were reconstructed with ordered subsets expectation maximization by using two iterations and 30 subsets.

Standard protocol for PET component.—The PET emission images were acquired for a 2–4-minute acquisition period at each bed position, depending on the weight of the patient (2 minutes for patients < 68.0 kg, 3 minutes for patients 68.0–90.7 kg, and 4 minutes for patients > 90.7 kg). The field of view and pixel size of the reconstructed images were 50 cm and 3.91 mm, respectively, with a matrix size of 128 x 128.

Dedicated protocol for PET component.—The PET emission images were acquired for 8 minutes at a single bed position. The field of view and pixel size of the reconstructed images were 30 cm and 2.34 mm, respectively, with a matrix size of 128 x 128. It was expected that a higher-count study would yield lower-noise images (even if images were reconstructed at finer pixel sampling), potentially yielding improved imaging of small structures.

Phantom Study
A phantom study was performed to assess the differences in activity quantitation between the two protocols. An 11-cm-diameter and 12.6-cm-long cylindric phantom containing eight spheres of four diameters (Data Spectrum Corporation, Hillsborough, NC) was used. The phantom was about the same size as the neck of an adult patient. The internal diameters of the spheres were 4.4, 6.0, 7.7, and 9.8 mm. The wall thickness of each sphere was 1.2 mm. The centers of the two smallest and the two largest spheres were located in approximately the same transverse plane. The centers of the remaining four spheres were located in a different transverse plane. The phantom and spheres were filled with FDG solution, with the concentrations adjusted to provide a sphere-to-background (S/B) activity ratio of 8:1 to simulate typical ratios obtained in clinical studies of head and neck cancer. FDG activity in the background solution was 5700 Bq/mL, similar to the background activity in the neck during a typical acquisition. A CT image of the phantom was acquired, followed by a 2-, 3-, and 4-minute PET emission acquisition (standard protocol) or an 8-minute PET emission acquisition (dedicated protocol). The coincidence count rate during the PET emission scans was approximately 26 kilocounts per second.

A physician (Y.Y., with 12 years of experience with CT and 4 years of experience with PET) evaluated the phantom data by using a workstation (Xeleris; GE Medical Systems). For visual analysis, the following three-point grading system was used: Grade 0 indicated no increased uptake above the intensity of the surrounding activity; grade 1, faint uptake; and grade 2, clear uptake. For quantitative analysis, a circular region of interest (ROI) that was the same size as the spheres was placed over each visualized sphere. A 3-cm-diameter background ROI was placed in the center of the phantom. The maximal radioactivity concentration values in the spheres and the mean radioactivity concentration values in the background were obtained, and contrast ratios of measured sphere counts to background counts (S/B ratios) were calculated. The percentage difference between the radioactivity concentration obtained by using the dedicated image compared with the standard image was calculated with the following formula: [C_DP – (C_SP/C_DP)]·100, where C_DP is the ROI radioactivity concentration value determined from the dedicated image and C_SP is the corresponding radioactivity concentration value determined from the standard image.

Clinical Study
Institutional review board approval and informed consent were obtained. The study was compliant with the Health Insurance Portability and Accountability Act.

Fifty-five consecutive patients suspected of having head and neck malignancy (28 men, 27 women; mean age, 57.9 years; age range, 21–79 years) who underwent dedicated head and neck PET/CT and standard whole-body PET/CT between October 2004 and July 2005 were retrospectively selected. Patients were referred for staging of known malignancies (n = 13), for detecting recurrence of treated malignancies (n = 41), or for identifying unknown primary lesions in the setting of nodal enlargement (n = 1). Fifteen patients had thyroid carcinoma, nine had laryngeal carcinoma, seven had nasopharyngeal carcinoma, seven had tongue carcinoma, six had unknown primary carcinoma, two had salivary gland carcinoma, two had oral floor carcinoma, two had paranasal sinus carcinoma, two had skin carcinoma, one had malignant lymphoma, one had breast carcinoma, and one had multiple enlarged lymph nodes.

Patients were instructed to have no caloric intake for at least 4 hours before intravenous administration of FDG (5.18 MBq per kilogram of body weight, with a minimum of 370 and maximum of 740 MBq). Serum glucose concentrations were obtained before the injection and were less than 200 mg/dL (11.1 mmol/L) (normal range, 70–115 mg/dL [3.9–6.4 mmol/L]) in all patients. A tracer uptake phase of approximately 120 minutes was used, and, during this phase, patients were instructed to sit in a quiet room. After the uptake phase, the patient was placed on the PET/CT scanner table. A nonenhanced CT image acquisition from the midcranium to the proximal thighs was performed first for approximately 15.8 seconds. The patients were instructed to hold their breath at end tidal volume. The images were acquired with the arms positioned at the side of the body. After the CT image acquisition was completed, dedicated PET emission scanning of the head and neck with an 8-minute acquisition of one bed position was performed. This acquisition was immediately followed by a standard whole-body emission scan of the same transverse planes used at CT that started at the proximal thighs and typically required five to seven bed positions.

CT and standard and dedicated PET images were reviewed on the Xeleris workstation in transverse, coronal, and sagittal planes, along with maximum intensity projection images. Two physicians (Y.Y. and T.Z.W. [who had 4 years of experience with CT and 8 years of experience with PET]) independently evaluated the FDG uptake. The images obtained with the standard protocol were read before those obtained with the dedicated protocol, with an interval of several days between interpretations. The evaluating physicians were blinded to the patient's clinical history and to any other imaging procedures used, except the CT component of the PET/CT study. Any difference of opinion was resolved by consensus.

For visual analysis, pathologic FDG accumulation was identified by tracer uptake greater than that in the surrounding normal soft tissue. For semiquantitative analysis, a circular ROI was placed over the identified head and neck lesion and the normal neck muscle on the transverse PET image. For lesions visualized at PET, ROIs were placed over the entire FDG-avid lesion to include the largest amount of radioactivity. When little or no lesion-related radioactivity was discernible at visual analysis, the ROI was positioned by using the lesion on CT. For the muscle ROI, a circular 2-cm ROI was placed on a posterior neck muscle, avoiding areas of increased muscle uptake. The tumor sizes were obtained from CT images. The standardized uptake value (SUV) was calculated by using the following formula: SUV = c_dc/(d_i/w), where c_dc is the decay-corrected tracer tissue concentration (in becquerels per gram), d_i is the injected dose (in becquerels), and w is the patient's body weight (in grams). The maximal SUV value in the lesion ROI and the mean SUV value in the muscle ROI were calculated for each patient. The percentage difference between the SUV on the dedicated image and the SUV on the standard image was calculated, as previously defined. As a contrast value, the lesion-to-muscle (L/M) SUV ratio was calculated by dividing the lesion SUV by the muscle SUV.

Lymph nodes that were larger than 5 mm in short-axis diameter at CT and/or showed abnormal uptake at standard or dedicated PET imaging were evaluated. At CT, lymph nodes were considered malignant if their short-axis diameter was more than 1 cm or if either central necrosis or an irregular border was present.

Reference Standard for Clinical Study
The CT and standard and dedicated PET findings were compared with the results of biopsy and/or clinical-radiologic follow-up as the reference standards. A hypermetabolic FDG lesion was considered to be true-positive for malignant involvement if this was proved by biopsy or if the lesion resolved after therapy or progressed at follow-up PET/CT or other imaging. An FDG-negative CT lesion was considered true-negative if it showed stability in size at conventional imaging follow-up for least 6 months or remained negative at repeat PET/CT.

Statistical Analysis
We compared the SUV or L/M SUV ratio between standard PET and dedicated PET and between benign and malignant lymph nodes by using a t test modified for clustered sampling (22,23). Receiver operating characteristic (ROC) curves and areas under the curves were generated for the likelihood of metastases in each lesion to determine the differences in accuracy between the standard and dedicated PET protocols. A two-tailed P value was used to compare standard PET with dedicated PET. Statistical analyses were performed by using software (SPSS, version 11.0 for Windows; SPSS, Chicago, Ill). Decision thresholds were considered optimal when the sum of paired values for sensitivity and specificity reached the maximum. The sensitivity and specificity of standard PET, dedicated PET, and CT for depicting metastatic lymph nodes were calculated by using biopsy and follow-up results as reference standards. For statistical comparison of dedicated and standard PET and CT, a ² test modified for clustered sampling (23) was used. A P value of .05 or less was considered to indicate a statistically significant difference.

	RESULTS

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Phantom Study
The 6.0-, 7.7-, and 9.8-mm spheres were clearly observed (grade 2) on the standard and dedicated PET images, although the 4.4-mm sphere was faintly visualized (grade 1) (Fig 1). The visualized spheres on the dedicated PET image had greater contrast and clearer borders than did the spheres on the standard PET image.

View larger version (85K): [in this window] [in a new window] [Download PPT slide]   Figure 1: Images from phantom study. A, B, C, Diagrams show sizes (in millimeters, shown by numbers) and positions of "hot" spheres. D, E, F, Three-minute emission scan images obtained with standard protocol. G, H, I, Eight-minute emission scan images obtained with dedicated protocol.

View larger version (9K): [in this window] [in a new window] [Download PPT slide]   Figure 2: Graph shows S/B ratios with each standard and the dedicated PET image plotted against sphere diameter. For all spheres, the S/B ratio on the dedicated PET image was higher than that on each standard PET image.

View larger version (8K): [in this window] [in a new window] [Download PPT slide]   Figure 3: Graph shows percentage differences between S/B ratios obtained with dedicated PET image and those obtained with each standard PET image, plotted against sphere diameters. A larger percentage difference between the S/B ratios obtained with the dedicated PET image and those obtained with each standard PET image was observed for the 6.0–9.8-mm spheres compared with the 4.4-mm sphere.

Both SUV and L/M SUV ratios derived from the dedicated PET images were significantly higher than those derived from the standard PET images (P < .003) (Table 1).

View larger version (11K): [in this window] [in a new window] [Download PPT slide]   Figure 4a: Flow diagrams of study on diagnostic accuracy of (a) PET visual analysis. Flow diagrams of study on diagnostic accuracy of (b) PET SUV analysis and (c) CT analysis.

View larger version (11K): [in this window] [in a new window] [Download PPT slide]   Figure 4b: Flow diagrams of study on diagnostic accuracy of (a) PET visual analysis. Flow diagrams of study on diagnostic accuracy of (b) PET SUV analysis and (c) CT analysis.

View larger version (15K): [in this window] [in a new window] [Download PPT slide]   Figure 4c: Flow diagrams of study on diagnostic accuracy of (a) PET visual analysis. Flow diagrams of study on diagnostic accuracy of (b) PET SUV analysis and (c) CT analysis.

The ROC curves are shown in Figure 5. The areas under the curve of standard PET and dedicated PET were 0.92 and 0.94, respectively. Although the ROC curves and areas under the curve showed dedicated PET to be marginally better than standard PET in depicting metastases, the difference did not reach statistical significance in our population (P = .56). When an SUV of 4.1 was used as the cutoff for positive dedicated PET results, the ROC analysis showed 96% sensitivity and 84% specificity. On the other hand, when an SUV of 2.9 was used as the cutoff for positive standard PET results, the ROC analysis showed 93% sensitivity and 83% specificity. The sensitivity of standard and dedicated PET in SUV analysis was significantly higher than that of CT (P < .001) (Table 2).

View larger version (9K): [in this window] [in a new window] [Download PPT slide]   Figure 5: ROC curves for presence of malignancy in a lesion (n = 149) show that dedicated PET is marginally better than standard PET (area under the curve, 0.94 vs 0.92), although the difference does not reach statistical significance (P = .56).

View larger version (101K): [in this window] [in a new window] [Download PPT slide]   Figure 6a: Images in 59-year-old man with thyroid cancer with submandibular lymph node metastasis. (a) Transverse nonenhanced CT image shows normal-sized lymph node (arrow) (area, 10 x 7 mm) in left submandibular region. (b) Transverse standard protocol FDG PET image shows no FDG uptake in the node. (c) Transverse FDG PET and (d) FDG PET/CT fusion images (both obtained with dedicated FDG PET protocol) show increased and clearly visible FDG uptake in the node (arrow).

View larger version (75K): [in this window] [in a new window] [Download PPT slide]   Figure 6b: Images in 59-year-old man with thyroid cancer with submandibular lymph node metastasis. (a) Transverse nonenhanced CT image shows normal-sized lymph node (arrow) (area, 10 x 7 mm) in left submandibular region. (b) Transverse standard protocol FDG PET image shows no FDG uptake in the node. (c) Transverse FDG PET and (d) FDG PET/CT fusion images (both obtained with dedicated FDG PET protocol) show increased and clearly visible FDG uptake in the node (arrow).

View larger version (76K): [in this window] [in a new window] [Download PPT slide]   Figure 6c: Images in 59-year-old man with thyroid cancer with submandibular lymph node metastasis. (a) Transverse nonenhanced CT image shows normal-sized lymph node (arrow) (area, 10 x 7 mm) in left submandibular region. (b) Transverse standard protocol FDG PET image shows no FDG uptake in the node. (c) Transverse FDG PET and (d) FDG PET/CT fusion images (both obtained with dedicated FDG PET protocol) show increased and clearly visible FDG uptake in the node (arrow).

View larger version (53K): [in this window] [in a new window] [Download PPT slide]   Figure 6d: Images in 59-year-old man with thyroid cancer with submandibular lymph node metastasis. (a) Transverse nonenhanced CT image shows normal-sized lymph node (arrow) (area, 10 x 7 mm) in left submandibular region. (b) Transverse standard protocol FDG PET image shows no FDG uptake in the node. (c) Transverse FDG PET and (d) FDG PET/CT fusion images (both obtained with dedicated FDG PET protocol) show increased and clearly visible FDG uptake in the node (arrow).

	DISCUSSION

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Although dedicated PET showed higher sensitivity for the detection of lymph node metastases, it resulted in a lower specificity, owing to visualization of lymph nodes without metastasis. FDG accumulates in inflammatory cells such as activated granulocytes and macrophages (25). Di Martino et al (26) reported a 13.4% false-positive PET result rate owing to inflammation of cervical lymph nodes. Distinguishing a lymph node metastasis from a reactive lymph node remains a problem with FDG PET.

Dedicated PET showed higher sensitivity for the detection of small lymph node metastases, but some false-negative findings were also found. Four malignant lymph nodes 5–10 mm in diameter were not visualized, even with dedicated PET imaging. In our phantom studies, spheres less than 1 cm in size were detected, although the smallest sphere (4.4 mm) was faintly visualized. The sizes of the lesions detected in the phantom and clinical studies were different. This discrepancy was explained by some differences between the phantom and patients. In the phantom study, the lesion and background radionuclide concentrations were uniform, whereas in patients, radionuclide accumulation was frequently nonuniform in the lesion and background. Patients frequently move—for example, swallow—during the emission acquisition, which decreases lesion detection. In addition, the patient may move between the emission scan and CT transmission scan, and this may result in less than perfect registration.

There were limitations in our study. We did not perform standard and dedicated PET emission scanning at exactly the same time after administration of FDG. Dedicated PET emission scanning was always performed first. This difference of time between dedicated and standard PET imaging was 10–28 minutes, depending on the emission acquisition time and bed positions of standard PET imaging. The FDG uptake ratio of tumor to background tissue has been reported to increase over time (27). Therefore, this study protocol might have given standard PET imaging an advantage over dedicated PET imaging. This effect is minimized, though, because of the relatively slow changes in distribution after the 2-hour uptake time used for this study. There was also the possibility of standard PET image degradation because of patient motion, which is known to increase with time during long examinations. We may have underestimated the true value of the CT portion of the examination by virtue of its having been performed without intravenous contrast material.

We did not attempt to optimize the image processing for the standard and dedicated protocols. Beyond the reduction in pixel size, fairly standard reconstruction parameters were used. It is possible that the sensitivity in lesion detection and lesion characterization could be improved for either the standard or dedicated protocol with the use of modified reconstruction parameters. It is highly unlikely, however, that any changes to the reconstruction methods would reverse the rankings of the two imaging protocols.

In conclusion, our evaluation of the detectability of head and neck metastatic adenopathy with a dedicated neck FDG PET/CT protocol and a standard FDG PET/CT protocol suggests improved detection of smaller nodes with the dedicated protocol.

	ADVANCE IN KNOWLEDGE

TOP ABSTRACT INTRODUCTION MATERIALS AND METHODS RESULTS DISCUSSION ADVANCE IN KNOWLEDGE References

 

• A dedicated fluorine 18 fluorodeoxyglucose (FDG) PET/CT protocol allowed the detection of smaller lymph nodes than did a standard FDG PET/CT protocol.
  

	FOOTNOTES

 

Abbreviations: FDG = fluorodeoxyglucose • L/M = lesion to muscle • ROC = receiver operating characteristic • ROI = region of interest • S/B = sphere to background • SUV = standardized uptake value

Authors stated no financial relationship to disclose.

Author contributions: Guarantors of integrity of entire study, Y.Y., T.Z.W., R.E.C.; study concepts/study design or data acquisition or data analysis/interpretation, all authors; manuscript drafting or manuscript revision for important intellectual content, all authors; manuscript final version approval, all authors; literature research, R.E.C.; clinical studies, Y.Y., T.Z.W., T.G.T., R.E.C.; experimental studies, Y.Y., T.G.T., T.C.H., R.E.C.; statistical analysis, Y.Y., R.E.C.; and manuscript editing, all authors

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TOP ABSTRACT INTRODUCTION MATERIALS AND METHODS RESULTS DISCUSSION ADVANCE IN KNOWLEDGE References

 

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