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Performance of sodium iodide based ¹⁸F-fluorodeoxyglucose positron emission tomography in the characterization of indeterminate pulmonary nodules or masses

Departments of ¹Diagnostic Imaging and ²Radiation Oncology, Peter MacCallum Cancer Institute, St Andrews Place, East Melbourne, Victoria 3002, Australia

Correspondence: Dr Alex G Pitman, Peter MacCallum Cancer Institute, Locked bag 1, A'Beckett Street, Melbourne, Victoria 3000, Australia

	Abstract

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The purpose of this study was to document the accuracy of ¹⁸F-fluorodeoxyglucose (¹⁸F-FDG) positron emission tomography (PET) with sodium iodide detectors in characterizing indeterminate lung nodules or masses and in identifying additional extralesional findings. 50 consecutive patients without a confident diagnosis of malignancy on CT underwent ¹⁸FDG PET with and without attenuation correction. The diagnosis of malignancy was made using visual diagnostic criteria, and tumour-to-blood pool ratios were calculated. The final diagnosis was established by surgery, biopsy or long-term follow-up. Any additional findings made at PET were recorded and similarly verified. Using blinded visual diagnostic criteria for the differentiation of malignant from benign nodules, sodium iodide PET achieved a sensitivity of 91% (30 of 33 cases), a specificity of 88% (15 of 17 cases), a positive predictive value for malignancy of 94% (30 of 32 cases) and a negative predictive value of 83% (15 of 18 cases). False positives occurred with active tuberculosis and sarcoidosis. False negatives were a 3 cm bronchoalveolar carcinoma, a 1.3 cm sarcoma metastasis and a 1 cm carcinoma. Use of tumour-to-blood pool ratios did not improve performance. PET suggested the presence of nodal or distant metastases in 13 of 33 patients with a malignant pulmonary lesion. These PET findings were confirmed in 11 patients. These results indicate that sodium iodide PET is an accurate tool for the characterization of indeterminate pulmonary masses or nodules and simultaneously provides non-invasive staging information that can alter patient management in up to one-third of such patients. Performance of sodium iodide PET is comparable with reported results for PET scanners using other detector materials.

	Introduction

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The solitary pulmonary nodule or mass remains a diagnostic problem despite continuing application of different diagnostic procedures and work-up protocols. In most cases radiological features are not sufficiently specific to avoid biopsy [1, 2]. The need for accurate and expeditious characterization arises from the high prevalence of primary lung carcinoma first presenting as a solitary pulmonary nodule or mass, in the order of 30–50% of all solitary pulmonary nodules in the USA and which is likely to be higher in other parts of the world where asymptomatic granulomatous and fungal foci are less prevalent.

Considerable work on the evaluation of solitary pulmonary nodules using ¹⁸F-fluorodeoxyglucose (¹⁸F-FDG) positron emission tomography (PET) has already been performed, mainly in centres in the USA. The bulk of this work used bismuth germanate (BGO) detector technology [3–8].

PET systems using sodium iodide (NaI) detector technology are generally less expensive to purchase than BGO based systems. Because of the higher sensitivity of the NaI detector compared with BGO detectors (even though count rate performance is lower) and the three-dimensional acquisition mode, typical ¹⁸F-FDG doses are lower than with BGO systems, leading to lower radiation exposure to patients and staff and poten<1?show=[fo]>tially reduced radionuclide costs. Assuming that clinical accuracy of NaI and BGO based PET is comparable, NaI based systems become particularly attractive where access to capital or operating funds is limited.

The purpose of this work was to document the accuracy of PET using NaI detectors in the characterization of indeterminate pulmonary lesions as well as the prevalence and significance of extralesional findings made with this technology. It is our hypothesis that diagnostic accuracy of PET in indeterminate pulmonary lesions should be similar for NaI and BGO technology.

	Materials and methods

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In this paper a pulmonary "nodule" is defined as a non-calcified, soft tissue lung parenchymal mass 3 cm or less in diameter [9]. A soft tissue mass exceeding 3 cm in diameter shall be referred to as a lung "mass". To be indeterminate, a mass or nodule has to have no pathognomonic imaging signs (such as arteriovenous malformation enhancement, popcorn calcification or fat), and no imaging evidence strongly indicative of malignancy, which is conventionally taken to be (a) distant metastases, (b) unequivocal local invasion of mediastinal structures or chest wall, or (c) a central mass with bronchial invasion or distal collapse, extensive locoregional lymphadenopathy and/or cavitation of the primary lesion.

Patient population
The initial patient population comprised 50 consecutive patients referred for characterization of indeterminate pulmonary nodules or masses as part of their clinical work-up and who did not have a past history of lung cancer or prior biopsy confirmation of malignancy.

36 of these 50 patients had a solitary pulmonary nodule that was indeterminate as defined above. Five patients had two or more indeterminate nodules 3 cm or less in diameter. Nine patients had indeterminate masses over 3 cm in diameter. All attempts at non-surgical tissue diagnosis were either unsuccessful or had an indeterminate result in five of these nine patients. Tissue diagnosis was ultimately achieved in the remaining four patients. One of the nine patients had three separate masses.

5 of the 50 patients were considered clinically to have evidence of active extrapulmonary malignancy at the time of PET (lymphoma, leukaemia, uterine sarcoma, thyroid carcinoma and melanoma). The lung nodule in all of these cases was indeterminate on imaging criteria, there was no evidence of widespread metastatic disease and PET was performed to determine whether the nodule could be a solitary metastatic deposit.

Evaluation of data
All available conventional pre-PET imaging was reviewed at the time of the PET scan, and either copies of the radiographs were made for later analysis or a copy of the final radiology report was filed. The size of the index lesion was directly measured on CT, or taken from the CT report, in all but three cases. Of these three cases, one had pre-PET chest radiography only, and in the other two the films were unavailable and the outside radiology report did not quote a measurement so the size was estimated from the description to be between 1.5 cm and 3 cm.

All patients underwent an ¹⁸F-FDG scan of the chest and upper abdomen at our institution using a UGM Penn-PET 300 H (UGM Medical Systems, Philadelphia, PA) dedicated full ring scanner. This scanner uses NaI detectors arranged in a hexagonal ring array, has a z-axis field of view of 25 cm and an intrinsic in-plane resolution of approximately 6 mm full width at half maximum height (FWHM) [10].

The administered activity was 2–3 mCi (74–111 MBq) of ¹⁸F-FDG for each patient. 1 h later, emission and transmission data were acquired (three 5 min emission steps each followed by a 3 min transmission step) and processed with iterative reconstruction using the ordered subset expectation maximization (OSEM) algorithm [11]. The scanner used a caesium-137 single transmisson attenuation correction system. Both the attenuation corrected and non-corrected images were independently reviewed blindly by two experienced PET readers (RJH and REW). The readers were told which lung and lobe contained the lesion. If there was more than one lesion, the largest was taken to be the index lesion. Readers graded ¹⁸F-FDG activity within the lesion (Table 1) and recorded any additional findings.

Diagnostic criteria
We applied visual interpretation of solitary pulmonary nodules or masses where activity in the index lesion was graded against activity in the mediastinal blood pool on the attenuation corrected images (Table 1). Mediastinal blood pool activity was defined to be ¹⁸F-FDG activity within the contours of the aorta and pulmonary arteries. All lesions with activity greater than that of the mediastinal blood pool (Grade 3) were considered malignant, while lesser grades (Grade 0–2) were considered benign (Table 1). A lesion was graded 0 (no visible activity) only if no increased ¹⁸F-FDG activity was seen on both the non-attenuation corrected and the attenuation corrected images. A lesion not seen on the attenuation corrected images but visible on the non-attenuation corrected images was Graded 1.

The attenuation corrected images were used in a non-blinded manner to derive tumour-to-blood pool ratios (TBPRs) for all patients with visualized nodules or masses, using the mediastinal blood pool and the ipsilateral lung as controls. The region of interest contour was placed around the index lesion on all the axial slices where it was visible, and the highest voxel activity was obtained. A large region of interest area was placed completely within the mediastinal blood pool contour, usually within the contours of the aortic arch, and mean voxel activity was calculated. TBPR was thus the ratio between the highest lesion voxel activity and the mean blood pool voxel activity.

The final diagnosis
The final diagnosis was established as follows. Where available, copies of histopathology reports were obtained and reviewed. Only positive histological or cytological diagnoses, whether for malignancy or for specific benign conditions such as hamartoma, were accepted as final. Non-specific or inconclusive diagnoses were not considered sufficient to exclude malignancy.

Serial imaging (n=15) was taken to represent the final diagnosis where no conclusive histology was available, and was treated as follows.

Malignant
The index lesion had unequivocally grown over an appropriate time interval, commensurate with growth rates of malignancy, without curative treatment, or the index lesion had unequivocally shrunk over an appropriate time interval with appropriate treatment, for instance radical radiotherapy.

Benign
The index lesion had shrunk or disappeared without any treatment, or the index lesion had remained stable over time without evidence of growth (n=7, mean follow-up 535 days, range 368–757 days).

Clinical follow-up was used as the final diagnostic criterion in those patients where no serial imaging was available (n=3).

	Results

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The final diagnoses for the 50 patients and the means by which they were established are presented in Table 2. There were 33 malignancies and 17 cases of benign disease. Lesion ¹⁸F-FDG activity grade vs final diagnosis for all 50 patients is presented in Table 3, which also shows lesion sizes for Grade 1 and Grade 2 lesions.

The 14 patients with indeterminate masses or multiple pulmonary nodules appeared to form a different population. The incidence of malignancy was higher in this group (12 of 14 cases compared with 21 of 36 cases, p<0.07), but did not reach statistical significance. The two benign conditions were multifocal aspergillosis (true negative on PET) and sarcoidosis (PET false positive on grade but recognized as likely granulomatous disease on overall PET appearance). The last false negative was a 1.3 cm sarcoma metastasis (Grade 1 uptake) in a patient with a coexistent benign nodule (Grade 0 uptake).

Two of the five patients with active extrapulmonary malignancy at the time of PET imaging had non-malignant pulmonary nodules, which were correctly identified as benign by PET.

Figure 1 plots lesion TBPR, using mediastinum as the background, against the final diagnosis and lesion size. As expected, perfect separation of the benign and malignant lesions on the basis of ¹⁸F-FDG activity alone is not possible. However, very good practical separation is still achieved, with a malignant lesion mean TBPR (relative to mediastinum, ±1 SD) of 3.32±1.78 and a benign lesion mean TBPR (relative to mediastinum, ±one SD) of 0.75±0.65 (p-value <0.001). Using tumour-to-background ratios, with surrounding lung as background, had no advantage over using TBPRs.

View larger version (11K): [in this window] [in a new window]   Figure 1. Graph showing the correlation between tumour-to-blood pool ratio (TBPR) lesion size in millimetres and final diagnosis (, benign; , malignant) of the lesions for 50 indeterminate pulmonary masses or nodules examined with positron emission tomography.

Additional findings on FDG PET
On consensus reading, additional PET findings were made in 16 (32%) of 50 patients (Table 5). The methods of verification of the findings were surgical histology (n=4), serial imaging (n=6) and final clinical outcome (n=6).

View larger version (45K): [in this window] [in a new window]   Figure 2. 18F-fluorodeoxyglucose (18F-FDG) positron emission tomography (PET) of an 82-year-old female with a newly identified asymptomatic 2.5 cm right upper lobe nodule. PET characterized the nodule as malignant, but in addition identified previously unsuspected metastases in the left iliac crest and lumbar subcutaneous tissues. Despite the PET findings, the patient underwent thoracotomy, which confirmed squamous cell carcinoma. The patient died of widespread metastases 2 months following the thoracotomy. (a) Axial image through the nodule (arrow) showing intense 18F-FDG uptake, consistent with malignancy. (b) Coronal image through the nodule (thin arrow), also showing focal increased 18F-FDG uptake in the left iliac crest (thick arrow) consistent with a metastasis. (c) Mid sagittal image showing a subcutaneous focus of markedly elevated 18F-FDG uptake (arrow) subsequently proven to be a subcutaneous metastasis.

	Discussion

Top Abstract Introduction Materials and methods Results Discussion References

 
Our study shows that NaI PET using routine iterative (OSEM) reconstruction and measured attenuation correction is an accurate technique for characterizing indeterminate pulmonary lesions as benign or malignant.

Comparison of the results of this study with six other studies (total n=339) performed after 1996 using a range of dedicated PET cameras and different image processing methods [3–8] is favourable (Table 6). In particular, not all of these studies routinely used attenuation correction and most did not use iterative reconstruction. Only one of these studies was carried out using NaI technology [7], with a series size and PET performance comparable with our results. This study does not appear to have utilized routine attenuation correction.

NaI detector technology is less expensive than BGO technology and requires substantially lower doses of ¹⁸F-FDG than BGO systems operating in two-dimensional mode, and slightly lower doses than BGO systems operating in three-dimensional mode. This reduces running costs and radiation exposure to both patients and staff [12].

Lower noise-equivalent count ratios for NaI systems may potentially reduce lesion contrast and therefore lesion sensitivity [13]. On the other hand, the improved energy discrimination characteristics of NaI allows use of a single photon transmission source and yields a transmission scan of higher statistical quality than is generally achieved with a positron source [11].

There are no direct comparative studies of dedicated NaI and BGO scanning of the same patient. Accordingly, studies confirming the accuracy of NaI systems rather than extrapolating from data derived using BGO systems are important. Assuming similar diagnostic accuracy between NaI and BGO, NaI based systems can offer an economic and radiation dosimetry advantage, particularly in healthcare systems with limited PET funding or where access to capital funding for equipment is an issue.

Comparison with other PET studies (Table 5) shows no appreciable difference in PET diagnostic accuracy based on the country of origin, despite what might be expected from different incidences of fungal lung disease. There is also no appreciable difference between the two NaI based studies and the BGO studies, despite use of a range of different equipment and processing methods. The comparison suggests instead that PET is a robust and reproducible technique for characterization of indeterminate pulmonary masses or nodules, irrespective of the incidence of granulomatous lung disease or the detector technology used.

Small pulmonary nodules present a frequent problem. The incidence of malignancy is lower, tissue diagnosis is more difficult to obtain and they are subject to partial volume artefact on imaging. As the nodule diameter falls below two FWHM diameters of the PET camera, it can no longer be completely resolved on its own, and its activity becomes averaged with counts from the surrounding lung parenchyma.

There were nine patients in our patient population with Grade 1 or Grade 2 ¹⁸F-FDG activity, where partial volume effects could have been relevant to final interpretation. The three false negatives encountered in our series were included in these nine (see Table 3). Partial volume effect may account for the low uptake in the confirmed malignant nodules of 1 cm (a primary non-small cell lung cancer) and 1.3 cm (a metastatic sarcoma) diameter, but not in the falsely negative bronchoalveolar cancer that was 3 cm in diameter. Low intrinsic metabolic activity is a more likely explanation for the false negative result, as this type of cancer has previously been documented to have low FDG avidity [14, 15]. Better sensitivity could be obtained by diagnosing all nodules of Grade 1 or 2 as malignant if they fall below a certain cut-off size. Theoretical considerations suggest that this cut-off should be determined by two FWHM diameters of the PET camera. For our camera, such a cut-off value is approximately 1.5 cm.

Lowe et al [3] found that all of the small cancerous lesions in their study were detected by visual analysis, and also recommend visual analysis for small nodules of 1.5 cm in diameter or smaller.

The use of quantitation, more specifically standardized uptake values, is widespread in the literature but there has been no conclusive demonstration of its superiority over qualitative assessment in clinical work [3, 5, 14, 16–18]. A previous study [19] compared standardized uptake values, tumour-to-background ratios and visual criteria in PET characterization of solitary pulmonary nodules and found no statistically significant differences. Use of quantitation has not yielded any advantage over visual assessment in our patient population.

There is ample evidence of PET's superior accuracy over CT in staging lung cancer [20–26]. A contemporary meta-analysis of CT and PET in non-small cell lung cancer staging has convincingly demonstrated the better sensitivity and specificity of PET (sensitivity 79±0.03%, specificity 91±0.02%) vs CT (sensitivity 60±0.02%, specificity 77±0.02%) [27].

A recent series of 102 patients [28] compared BGO based PET with conventional pre-operative staging for resectable lung cancer [28]. In that study, PET correctly identified 29 patients with mediastinal lymph node metastases and 11 patients with distant metastases invisible with conventional staging. In our series PET correctly found that 9 of 33 patients with confirmed malignancy had mediastinal nodal metastases and that 2 of 33 patients had distant tumour. The proportions are very similar despite different detector technologies. These results are also in keeping with our findings in a cohort of patients undergoing primary staging for newly diagnosed lung cancer [29].

Furthermore, our results imply that in one-third of patients with malignancy presenting as an indeterminate pulmonary lesion, PET will produce a finding that may alter subsequent patient management and outcome. In those patients where malignancy first presents as a solitary pulmonary nodule, the proportion of such patients is still considerable at nearly one-fifth.

In conclusion, NaI PET is an accurate tool for characterization of indeterminate pulmonary masses or nodules, and provides accuracy similar to BGO instruments. Masses or nodules that are negative on PET can avoid percutaneous biopsy, but in these cases we recommend follow-up with CT or PET. Because of partial volume effect, small nodules with faint but visible FDG activity (Grade 1–2) should be considered potentially malignant and may warrant more aggressive investigation than larger nodules of similar intensity. All masses or nodules positive for malignancy on PET (Grade 3 uptake) should be considered malignant once active tuberculosis and sarcoidosis have been excluded. Active therapies are available for non-cancerous conditions that cause false positive ¹⁸F-FDG scans, so that a positive PET scan is a highly useful clinical finding, even if false positive for malignancy. In our study, PET correctly identified additional nodal metastases or distant tumour in one-third of patients with malignant lung lesions presenting as an indeterminate mass or nodule. PET findings of nodal or distant metastases in a PET positive indeterminate lung mass or solitary pulmonary nodule will usually turn out to be true positive, and so should be incorporated into management planning.

Received for publication April 10, 2001. Revision received September 11, 2001. Accepted for publication September 18, 2001.

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