Oncological diagnosis using positron coincidence ... - BIR Publications

The British Journal of Radiology, 75 (2002), 409–416

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2002 The British Institute of Radiology

Oncological diagnosis using positron coincidence gamma camera with fluorodeoxyglucose in comparison with dedicated PET 1,2

H ZHANG, DMSc, 1M TIAN, MD, 1N ORIUCHI, MD, 1T HIGUCHI, MD, 2S TANADA, MD and 1 K ENDO, MD 1

Department of Nuclear Medicine and Diagnostic Radiology, Gunma University School of Medicine, Showa-machi 3-39-22, Maebashi, Gunma 371-8511 and 2Department of Medical Imaging, National Institute of Radiological Sciences, 9-1, Anagawa-4, Inage-ku, Chiba 263-8555, Japan

Abstract. The purpose of this study was to compare the utility of a dual-head positron coincidence detection gamma camera (PCD) with that of dedicated positron emission tomography (PET) in the imaging of various malignancies using 18F-fluorodeoxyglucose (FDG). 25 patients with known or suspected malignancies at various sites underwent imaging with both methods, and diagnostic performance on a lesion basis was compared. Tumour lesions were analyzed visually and semi-quantitatively using the ratio of tumour-to-background counts (T/B ratio). FDG PCD and FDG PET visually detected 34 (72.3%) lesions and 37 (78.7%) lesions, respectively. The mean T/B ratio and standard deviation (SD) of FDG PCD was 3.5¡3.3, significantly lower than that of FDG PET (8.4¡7.1, p,0.001). When tumour lesions were less than 2.0 cm in diameter, the sensitivity of FDG PCD was 37.5%, significantly inferior to that of FDG PET (50.0%, p,0.01). Sensitivity between FDG PCD and FDG PET in lesions of more than 2.0 cm diameter showed no statistically significant difference. This study indicates that FDG imaging with a dual-head coincidence detection gamma camera can provide suitable diagnostic performance for lesions greater than 2.0 cm diameter, but performed significantly worse than dedicated PET for lesions smaller than this. The potential value of positron emission tomography (PET) with 18F-fluorodeoxyglucose (FDG) for the detection of malignant tumours has been demonstrated [1]. In recent years, numerous studies have shown that FDG PET is a valuable, non-invasive method for tumour detection [2–5]. However, the high cost of implementation owing to the expense of a dedicated PET scanner, cyclotron, support laboratories, maintenance and operation has hindered the widespread use of FDG PET. Studies of FDG imaging with single-photon emission tomography (SPECT) equipped with 511 keV ultra-high energy collimators have been performed to investigate its role in oncology. Results were limited due to its lower sensitivity and lower spatial resolution compared with dedicated PET [6]. Recently, Received 12 November 2001 and in revised form 18 January 2002, accepted 6 February 2002. Address correspondence to Hong Zhang, DMSc, Department of Nuclear Medicine and Diagnostic Radiology, Gunma University School of Medicine, Showa-machi 3-39-22, Maebashi, Gunma 371-8511, Japan. Dr Hong Zhang was supported by a Japan Society for the Promotion of Science Postdoctoral Fellowship. The British Journal of Radiology, May 2002

Muehllehner et al [7] introduced a dual-head gamma camera modified for coincidence detection, which provided spatial resolution and system sensitivity higher than with SPECT systems and comparable with dedicated PET [8, 9]. Dual-head gamma cameras modified for coincidence detection have become available for oncological FDG imaging, making FDG studies potentially available to most nuclear medicine departments [10]. So far, the clinical utility of FDG imaging using a coincidence gamma camera in the detection of lung cancer has been reported [11–13], but studies of FDG imaging in the detection of other kinds of malignancies are still limited. The purpose of this study was to compare the performance of FDG imaging with a dual-head coincidence detection gamma camera with that of dedicated PET in patients with known or suspected malignancies.

Materials and methods Imaging equipment A dual-head positron coincidence detection gamma camera (PCD) (Picker, Cleveland, OH), equipped with 0.75 inch thick NaI (TI) crystals 409

H Zhang, M Tian, N Oriuchi et al

and rectangular field of view (FOV) detectors with a FOV of 50 cm638 cm, was used for FDG imaging. Two detectors were oppositely positioned at 180 ˚ with the capability of simultaneously detecting one annihilation photon in each detector resulting from the same positron emitter. A 15 ns timing window was applied to identify coincidence events and a dual window technique was used to accept the coincidences between photopeak–photopeak events and photopeak– Compton scatter events. Slit collimators were used to reduce the single rate from activity outside the FOV and reduce effects of low energy scattered radiation in two-dimensional (2D) acquisition mode. The pre-windows were adjusted to 511 keV¡30% of photopeak. Dedicated PET (SET-2400W; Shimadzu Corporation, Kyoto, Japan) was used for FDG PET imaging. This PET has a 20 cm axial FOV and 59.5 cm transaxial FOV, and consists of 32 rings of 21 504 bismuth germanate (BGO) crystals, giving 63 2D imaging planes. Signals from the photomultiplier tubes are processed to the position of the crystal which the gamma photon hits by using a coincidence time window of 15 ns. Position non-linearity and energy non-uniformity of the detector unit are corrected in real time. In the 2D mode, axial coincidence path acceptance can be controlled from 1 to 8 to optimize sensitivity and axial resolution. The system has 1 mm thick and 55 mm long content septa for the 2D mode. 63 sinograms are stored in a large scale acquisition memory (1 GB) in the 2D mode. A dead time correction and physical decay correction of radioisotope can be performed in real time in the memory. A 68Ge–68Ga external rod source of 185 MBq can be orbited in a 640 mm radius to measure blank scan and transmission scan data. Simultaneous transmission–emission scans can be performed in the SET-2400W PET scanner [14]. The performance of PCD and PET are summarized in Table 1.

Patient population 47 lesions in 25 patients (7 females, 18 males; age range 33–80 years; mean age 59 years) with

known or suspected malignancies were included in this study. A variety of pathologies were encountered, namely oesophageal carcinoma (n54), head and neck carcinoma (n51); bronchial carcinoma (n513), malignant lymphoma (n521), soft tissue tumours (n54), and uterine carcinoma (n51). 22 lesions were histologically confirmed from surgical or biopsy specimens and the other 25 lesions were diagnosed based on follow-up CT or MRI. Patients underwent both PET and PCD imaging on the same day after the same administration of FDG. All patients fasted for more than 4 h prior to imaging in order to minimize glucose utilization by normal tissue and to ensure standardized glucose metabolism. The study was approved by the local ethical committee of Gunma University, and written informed consent was obtained from all patients.

Imaging with dedicated PET A simultaneous transmission–emission scan technique was used in the FDG PET study, which has the same semiquantification and detectability with the separate transmission and emission scan in 2D mode [15]. 40–50 min after iv administration of approximately 185–370 MBq FDG, simultaneous transmission–emission scans were performed for 8 min per bed position. The order subsets expectation maximization (OSEM) algorithm was used to reconstruct attenuationcorrected PET emission data. The OSEM algorithm with 16 subsets and 1 iteration was used for 2D image reconstruction. Images were reconstructed in a 1286128 matrix using a Butterworth filter with a cutoff of 12 and order of 2. Decay and dead time correction were automatically performed during the acquisition step.

Imaging with PCD PCD imaging was performed 2 h after completion of FDG PET, due to the count rate limitation of PCD (singles count rate of approximately 1.1 counts per second). A 15 ns timing window was employed to identify the coincidence events using the combination of photopeak–photopeak

Table 1. Performance of dual-head positron coincidence detection gamma camera (PCD) and dedicated positron emission tomography (PET) camera in two-dimensional mode Camera PCDb PET

Resolutiona (FWHM:mm)

Sensitivity (kcps kBq21 m21)

Scatter fraction (%)

(kcps

NECR kBq ml21)

5.7 4.4

1.8 7.98

22 13.1

3.9 73.0

0.2 28.0

NECR, noise equivalent count rate; FWHM, full width at half maximum. a Reconstructed transaxial resolution at the center of the field of view. b PCD data were measured within combinations of coincidence events identified by 30% photopeak–Compton scatter window.

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The British Journal of Radiology, May 2002

Oncological diagnosis using FDG coincidence gamma camera

events and photopeak–Compton scatter events. No Compton–Compton counts were accepted. Energy windows were set at 511 keV¡30% for the 18 F photopeak and 280–340 keV for the Compton scatter events in the crystals. Random coincidence events were not corrected. PCD images were acquired with a 180 ˚ rotation with 32 steps pre-set at 30 s each, for a total of 16.9 min at one bed position. Decay and dead time correction were performed before image reconstruction. Emission data was corrected by Chang’s attenuation correction method with an attenuation coefficient of 0.095 cm21. The OSEM algorithm with 32 subsets and 1 iteration was used for 2D image reconstruction. Data were rebinned into 96 projections and images reconstructed in a 1286128 matrix using a Butterworth filter with a cutoff of 12 and an order of 2.

Image and data analysis FDG PCD and FDG PET images with 9.8 mm slice thicknesses were separately and blindly interpreted by three experienced nuclear medicine physicians until consensus was reached. Clinical information and conventional images such as radiographs, ultrasound scans, CT scans and MR images were available at the time of image interpretation. Increased FDG uptake relative to the surrounding background radioactivity was considered a positive result for tumour. For the semiquantitative analysis, a regions of interest (ROIs) method was used to evaluate FDG uptake of tumour. The focal area of FDG uptake of tumour included maximal point of activity. 1 cm diameter ROIs for background radioactivity measurement were drawn on the homologous contralateral normal lung, the right lower lung field for the thoracic region, the lateral intraabdominal cavity below the right kidney for the abdominal pelvic region and the right lateral cervical region for the head and neck region. ROIs of non-visualized lesions on FDG PCD and FDG PET images were defined corresponding to CT or MRI findings. Mean counts per pixel were used to calculate tumour-to-background counts (T/B ratio). In the PET studies, mean standardized uptake values (SUVs) were also determined for all lesions.

Statistical analysis The data are expressed as mean¡standard deviation. Statistical analysis of difference in FDG uptake was performed by paired Student’s t-test. The difference in sensitivity of FDG PCD and FDG PET was estimated with McNemar’s test. Probability values of less than 0.05 were considered statistically significant. The British Journal of Radiology, May 2002

Results A total of 25 patients with known or suspected malignancies were included in this study. Table 2 summarizes the results of FDG PET and FDG PCD studies. Of 47 lesions in 25 patients, 37 (78.7%) lesions were detected on FDG PET images and 34 (72.3%) lesions were correctly identified on FDG PCD images (Figures 1–3). On CT, the diameter of these lesions ranged from 1.0 cm to 8.0 cm. Three lesions of 1.8 cm (SUV5 1.8), 2.0 cm (SUV51.7) and 4.0 cm (SUV50.9) in three patients showed positive results on FDG PET images but were missed on FDG PCD images. In addition, 10 lesions with false-negative results on both FDG PET and FDG PCD images ranged from less than 1.0 cm to 8.0 cm with a mean SUV of 0.84¡0.69. The sensitivity of FDG PET and FDG PCD for small lesions ((2.0 cm) was lower than the sensitivity for large lesions (.2.0 cm) (p,0.01). In small lesions, sensitivity of FDG PET (50.0%) was higher than that of FDG PCD (37.5%), whereas the similar sensitivity (93.5% PET, and 90.3% PCD) was observed in large lesions. Sensitivity of FDG PCD, regardless of lesion size, was 72.3% compared with 78.7% for FDG PET (Figure 4). No correlation was observed between lesion size and T/B ratio on either FDG PET or FDG PCD (Figure 5). The T/B ratio of FDG PET was 8.4¡7.1 (range 0.7–25.8), and that of FDG PCD was 3.5¡3.3 (range 0.4–15.2), which was significantly lower (p,0.001) (Figure 6). However, there was a significant positive correlation between the T/B ratio of FDG PET and FDG PCD (Figure 7). The SUV of lesions on FDG PET was 3.3¡2.5 (range 0.1–11.9). Significant positive correlations were observed between SUV and the T/B ratio of FDG PET (r50.87, p,0.001) and between SUV and the T/B ratio of FDG PCD (r50.58, p,0.01).

Discussion Although our previous phantom study indicated that PCD performance was inferior to that of dedicated PET (Table 1) [16], FDG PCD showed comparable lesion basis sensitivity in the detection of tumours in comparison with FDG PET in this study (Figure 4). Also, the T/B ratio of FDG PCD was significantly lower than that of FDG PET (Figure 6). On the basis of visual analysis, 10 false-negative results in FDG PET and 13 false-negative results in FDG PCD were observed mostly in lesions less than or equal to 2.0 cm diameter. Among them, five regional lymph node metastatic lesions, two kidney lesions and three lung tumours showed false-negative 411

H Zhang, M Tian, N Oriuchi et al Table 2. Patient characteristics and results of 18F-fluorodeoxyglucose (FDG) positron emission tomography (PET) and FDG dual-head positron coincidence detection gamma camera (PCD) Patient No.

Lesion

Sit at CT or MRI

Size at CT or MRI (cm)

SUV-PET

T/B-PET

T/B-PCD

Tumour

1 2

1 2 3 4 5 6 7 8 9 10 11 12 13 14 15 16 17 18 19 20 21 22 23 24 25 26 27 28 29 30 31 32 33 34 35 36 37 38 39 40 41 42 43 44 45 46 47

Im Im Mediastinal LN Ei Regional LN Im Regional LN Regional LN Parotid Kidney Kidney Hilar LN Hilar LN Paraaortic LN Paraaortic LN Liver Lower lobe Mediastinal LN Upper lobe Upper lobe Lower lobe Lingula Lingula Mediastinal LN Upper lobe Upper lobe Upper lobe Upper lobe Mediastinal LN Rib Spine Upper lobe Lower lobe Mediastinal LN Mediastinal LN Mediastinal LN Mediastinal LN Upper lobe Upper lobe Upper lobe Upper lobe Lower lobe Thigh Knee Leg Knee Paraaortic LN

5.8 5.0 3.0 5.6 1.0, 7.0 1.0 1.0 3.5 8.0 2.5 2.0 2.0 1.0 1.0 6.0 1.0 3.0 6.0 1.8 3.0 2.0 6.0 2.5 2.0 1.8 3.0 3.0 4.0 4.0 3.0 2.0 2.5 3.0 3.0 2.5 3.0 2.0 3.0 3.0 8.0 1.7 8.0 4.0 3.5 2.0 2.5

1.8 3.7 3.5 8.6 0.3 11.9 2.8 2.5 5.8 2.0 1.1 0.1 0.1 1.0 1.0 4.5 0.3 4.5 6.6 5.0 4.3 0.8 8.3 1.9 2.8 1.2 3.2 3.8 4.5 4.9 3.2 1.7 3.4 5.6 6.7 4.3 4.5 3.1 5.9 4.5 2.3 0.3 1.9 0.9 1.1 1.8 3.1

3.1 5.6 6.4 14.9 0.7 25.8 6.1 5.3 5.6 1.0 0.9 1.2 1.0 1.0 1.0 6.1 0.9 14.0 16.4 17.2 14.5 1.3 18.8 4.3 5.9 3.0 4.8 15.9 18.7 19.1 9.7 4.7 11.0 18.0 21.5 13.7 14.5 9.9 19.2 14.5 4.9 0.7 2.2 1.6 2.0 4.6 3.6

2.4 4.7 3.7 1.7 0.4 7.2 2.1 1.8 3.5 0.9 0.8 0.9 0.9 1.0 0.9 2.9 0.9 3.2 4.1 3.9 3.1 1.0 3.6 2.3 2.6 1.2 1.8 3.2 5.1 3.5 3.5 0.9 6.1 7.2 13.1 8.6 9.9 5.3 15.2 9.2 1.7 0.4 1.9 1.2 2.2 2.5 2.2

Oesophageal cancer Oesophageal cancer

3 4 5 6

7 8 9 10 11 12 13 14 15 16 17

18 19

20 21 22 23 24 25

(N)

(N) (N) (N) (N) (N) (N) (N)

(N)

(N)

Oesophageal cancer (N) Oesophageal cancer

(N) (N) (N) (N) (N) (N) (N)

(N)

(N)

(N)

Head and neck tumour Malignant lymphoma

Malignant lymphoma Lung cancer Lung Lung Lung Lung Lung

cancer cancer cancer cancer cancer

Lung Lung Lung Lung

cancer cancer cancer cancer

Lung cancer Lung cancer

Lung nodule (N) (N)

Soft tissue tumour Soft tissue tumour Soft tissue tumour Soft tissue tumour Uterine cancer

Im, middle portion of intrathoracic oesophagus; LN, lymph node; Ei, inferior portion of intrathoracic oesophagus; SUV, standardized uptake value determined from PET; T/B-PET, tumour-to-background ratio in PET study; T/B-PCD, tumor-tobackground ratio in PCD study; N, not identified on image

results on both FDG PET and FDG PCD. Two lung cancer lesions (1.8 cm diameter with 1.2 SUV and 2.0 cm (diameter with 1.7 SUV) and one soft tissue tumour (4.0 cm diameter with 0.9 SUV) of the knee were detected by FDG PET but were not visualized by FDG PCD. The results of lesion basis sensitivity showed that FDG PCD was problematic in the detection of tumours less than 2.0 cm diameter with less than 1.7 SUV. Mean lesion diameter in this study was 3.3 cm 412

(range 1.0–8.0 cm) and the mean T/B ratio of FDG PCD and FDG PET was 3.5¡3.3 (range 0.4–15.2) and 8.4¡7.1 (range 0.7–25.8), respectively. Although no statistical correlation was observed between tumour size and T/B ratio in both FDG PET and FDG PCD in this study, lesion size should influence tumour detectability of FDG PCD and FDG PET [17]. Previously reported sensitivities for detection of pulmonary lesions with FDG coincidence gamma The British Journal of Radiology, May 2002


Figure 1. Patient 2, oesophageal cancer with mediastinal lymph node metastases. (A) Chest CT image shows the primary lesion (arrow). Coronal views of (B) 18F-fluorodeoxyglucose (FDG) positron emission tomography and (C) FDG dual-head positron coincidence determination gamma camera detection show increased uptake in the node (upper arrows) and the primary lesion (lower arrows).

camera ranged from 80% to 97% [11–13], which were relatively higher than 72% in detection of various tumour lesions in this study. This may be owing to different lesion size, lesion location and FDG tumour uptake in this study, since our patients were not selected on the basis of any criteria for size or number of tumour lesions. Owing to limitations in contrast resolution and the uniform attenuation correction, sensitivity for tumour lesions was relatively lower in the

abdomen and elsewhere compared with that in lung, especially for lesions smaller than 2.0 cm. In this study, PCD imaging was performed more than 2 h after FDG injection to allow acquisition with PET and PCD in the same day. As previously pointed out [8], FDG accumulation in tumours tends to rise with time, while accumulation in most normal tissues imaged decreases. This turns out to be advantageous in detecting lesions by PCD imaging because of the

Figure 2. Patient 23, soft tissue tumour (neurinoma), 3.5 cm greatest diameter. (A) MRI image shows tumour in leg (arrow). Coronal views of (B) 18F-fluorodeoxyglucose (FDG) positron emission tomography and (C) FDG dual-head positron coincidence determination gamma camera detection show tumour uptake (arrows).

Figure 3. Patient 25, uterine cancer with paraaortic lymph node metastases. (A) Abdominal CT image shows enlarged paraaortic lymph node (arrow). Coronal views of (B) 18F-fluorodeoxyglucose (FDG) positron emission tomography and (C) FDG dual-head positron coincidence determination gamma camera detection show metastatic lymph node (arrows). The British Journal of Radiology, May 2002

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Figure 4. Percentage of lesion detected by 18F-fluorodeoxyglucose (FDG) positron emission tomography (&) and FDG dual-head positron coincidence determination gamma camera detection (H) imaging with respect to size using CT or histopathologic confirmation as the gold standard.

Figure 5. Relationship between lesion size and tumour-to-background ratio (T/B ratio) obtained by 18F-fluorodeoxyglucose (FDG) positron emission tomography (PET) (a) and FDG dual-head positron coincidence determination gamma camera detection (PCD) (b). No correlation is observed between lesion size and T/B ratio by either FDG PCD or FDG PET.

Figure 6. Comparison of tumourto-background ratio (T/B ratio) of 18 F-fluorodeoxyglucose (FDG) positron emission tomography (PET) and FDG dual-head positron coincidence determination gamma camera detection (PCD). T/B ratio of FDG PCD (3.5¡3.3) is significantly lower than obtained by FDG PET (8.4¡7.1, p,0.001). 414



Figure 7. Relationship between tumour-to-background ratio (T/B ratio) of 18F-fluorodeoxyglucose (FDG) PET and FDG dual-head positron coincidence determination gamma camera detection (PCD). Significant positive correlation is observed between T/B ratios obtained by FDG PET and FDG PCD.

improvement of the tumour-to-background ratio [18, 19]. This study focused on the utility of FDG PCD imaging in detecting various tumours. The data indicated that sensitivity of FDG PCD for tumours was comparable to that of FDG PET on visual analysis. However, FDG PCD has certain limitations that diminish image quality and semi-quantification compared with dedicated PET. The percentage of scatter and random events is considerably higher than that of a dedicated PET in 2D mode. In our previous phantom study, scatter and random fraction of a 20 cm cylinder filled with 18F solution was 22% in PCD and 13.1% in dedicated PET [16]. In this study, a higher percentage of scatter and random fraction in PCD imaging could be expected. Conversely, pulse pile-up in the detector system limited the single count rate of PCD imaging. These factors resulted in poor image quality of FDG PCD when the single count rate exceeded approximately 26106 s21. The lower number of coincidence events, and the higher fraction of scatter and random fraction illustrated the reason why T/B ratio was significantly lower in PCD studies compared with dedicated PET. In this study, uniform attenuation correction was employed for PCD imaging and the effect of scatter on FDG images was not corrected in either PCD or PET. Better results might be achieved if the attenuation correction of PCD and the scatter correction of PCD and PET were performed by measured attenuation correction and scatter correction methods. The British Journal of Radiology, May 2002

Conclusion This study indicates that FDG imaging with a dual-head PCD can provide suitable diagnostic performance for lesions greater than 2.0 cm diameter, but performed significantly worse than dedicated PET for lesions smaller than this.

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