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Nuclear Medicine |
1 From the Division of Nuclear Medicine, Johns Hopkins University, 601 N Caroline St, Rm 3223A, Baltimore, MD 21287-0817. From the 2002 RSNA Annual Meeting. Received February 23, 2003; revision requested May 16; final revision received April 12, 2004; accepted May 26. R.L.W. supported by research grant from GE Medical Systems. Address correspondence to R.L.W. (e-mail: rwahl@jhmi.edu).
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ABSTRACT |
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 TOP ABSTRACT INTRODUCTIONMATERIALS AND METHODSRESULTSDISCUSSIONREFERENCES |
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MATERIALS AND METHODS: The institutional review board allowed a retrospective review of PET/CT images obtained in 78 patients with non–head and neck cancer and waived the requirement for informed consent. The accumulation of FDG in 11 normal head and neck structures was visually and quantitatively assessed retrospectively. Positive rate percentage (PRP) was defined as the sum of the percentages of patients with grade 2 and grade 3 tracer uptake intensity. Standardized uptake values (SUVs) were calculated for quantitative analysis. Mean SUVs were compared between the male and female patients by using the unpaired t test, and the correlation between FDG uptake and patient age was assessed by using the Pearson correlation coefficient test.
RESULTS: Intense tracer uptake was usually seen in the palatine tonsils (PRP, 98%; mean SUV, 3.48), soft palate (PRP, 96%; mean SUV, 3.13), and lingual tonsils (PRP, 96%; mean SUV, 3.11). In the inferior concha (PRP, 4%; mean SUV, 1.56), thyroid gland (PRP, 3%; mean SUV, 1.31), and tongue (PRP, 1%; mean SUV, 1.39), uptake was typically minimal. FDG accumulation was variable in the sublingual glands (PRP, 72%; mean SUV, 2.93), spinal cord (PRP, 64%; mean SUV, 2.12), submandibular glands (PRP, 53%; mean SUV, 2.11), parotid glands (PRP, 51%; mean SUV, 1.90), and vocal cords (PRP, 19%; mean SUV, 1.77). The mean normal-tissue SUV in the soft palate was higher in male than in female patients (P < .01). A negative correlation between age and physiologic FDG uptake was seen in the palatine tonsils (r = –0.51, P < .001) and sublingual glands (r = –0.70, P < .001).
CONCLUSION: Intense FDG uptake was usually observed in the palatine tonsils, lingual tonsils, and soft palate, whereas uptake in the major salivary glands was variable.
© RSNA, 2005
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INTRODUCTION |
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TOPABSTRACTINTRODUCTIONMATERIALS AND METHODSRESULTSDISCUSSIONREFERENCES |
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To interpret PET images accurately, it is essential to be fully familiar with the normal patterns, intensities, and frequencies of FDG distribution in the head and neck area. PET evaluation of physiologic tracer uptake in the head and neck region, with or without image fusion techniques involving the use of conventional cross-sectional modalities to assist in locating structures and lesions seen on PET images, has been described (8–12). The normal patterns and the variability in the extent of tracer uptake need to be characterized in a broad population of patients.
Combined PET/CT scanners that enable highly precise localization of the metabolic abnormalities seen on PET and high-spatial-resolution CT images have been developed (13–15). We believed that the evaluation of normal tracer uptake in the head and neck region would be easier and more precise and reliable with PET/CT, enabling us to investigate normal imaging characteristics more effectively. The purpose of this study was to retrospectively evaluate FDG distribution in the head and neck region by using a combined PET/CT system in patients with no known abnormality in this anatomic area.
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MATERIALS AND METHODS |
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TOPABSTRACTINTRODUCTIONMATERIALS AND METHODSRESULTSDISCUSSIONREFERENCES |
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Patients
The study population (identified in the database) comprised 78 patients—36 male and 42 female patients aged 10–83 years (mean ages of all, male, and female patients, 54, 53, and 55 years, respectively; nonsignificant difference between male and female groups, unpaired t test)—who had been referred for evaluation of known or suspected cancer. These patients had had no history of malignancy in the head and neck, no symptoms in this region, and no known clinically suspicious diseases, such as thyroiditis, in the neck region. Also, when abnormal foci seen on PET images were suspected of being tumors in the head and neck region, as described in a clinical PET/CT report by two experienced nuclear medicine physicians (C.C. with 3 years of experience with PET, M.M.O. with 8 years of experience with PET), or when any clinical abnormalities in the head and neck became apparent during the follow-up period, the patient data were excluded from our investigation. All CT, PET, and fused PET/CT images were retrospectively examined.
PET/CT Scanning
For whole-body imaging, PET had been performed by using a PET/CT scanner (Discovery LS; GE Medical Systems, Waukesha, Wis). The imaging system enabled the simultaneous acquisition of 35 transverse PET images per field of view, with intersection spacing of 4.25 mm. The field of view and pixel size of the PET images reconstructed for fusion were 50 cm and 3.91 mm, respectively, with a matrix size of 128 x 128. This PET/CT system also includes a four–detector row helical CT scanner. The technical parameters used for CT imaging were as follows: a detector row configuration of 4 x 5 mm, a pitch of 6:1 (high-speed mode), a gantry rotation speed of 0.8 second, a table speed of 30 mm per gantry rotation, 140 kVp, and 80 mA.
The patients had fasted for at least 4 hours before FDG was administered. Blood glucose levels were checked before the injection, and if they were lower than 11.1 mmol/L, the patients received an intravenous injection of 555–740 MBq of FDG, which was synthesized by using the Hamacher et al method (16). A tracer uptake phase lasting about 60 minutes was implemented; during this phase, the patients were instructed to sit in a quiet room without talking or chewing. After the uptake phase, CT image acquisition in the region of the meatus of the ear to the middle portion of the thigh was performed for approximately 35 seconds without patient breath holding, and whole-body emission scanning of the same transverse plane was performed, with a 5-minute acquisition period at each bed position.
The CT images had been used not only for image fusion but also to generate the attenuation map with use of measured attenuation correction. PET images were reconstructed by using an ordered-subset expectation maximization iterative reconstruction algorithm (two iterations, 28 subsets).
Image Analysis
Two physicians (Y.N. with 11 years of experience with CT and 7 years of experience with PET, M.T. with 8 years of experience with CT and 6 years of experience with PET) in consensus retrospectively evaluated the following 11 structures for FDG uptake visually and quantitatively by using the transverse images: (a) the inferior concha in the nasal cavity, (b) the spinal cord at the C1 level, (c) the parotid glands bilaterally, (d) the soft palate, (e) the palatine tonsils bilaterally, (f) the tongue, (g) the lingual tonsils bilaterally, (h) the submandibular glands bilaterally, (i) the sublingual glands bilaterally, (j) the vocal cords bilaterally, and (k) both lobes of the thyroid gland. For visual analysis, a four-point grading system was used: Grade 0 indicated no or faint uptake; grade 1, uptake comparable to that in the blood pool; grade 2, moderate update—that is, greater than that in the blood pool; and grade 3, intense uptake. Positive rate percentage was defined as the quotient of the number of cases with a visual grade 2 or 3 divided by the total number of cases, times 100.
For quantitative analysis, first an author (Y.N.) and a co-author (M.T.) drew 8–10-pixel circular regions of interest in the central portion of each structure depicted on the CT images. Then, quantitative uptake values in the corresponding regions of interest on the PET images were determined by using a computer workstation (eNTEGRA; ELGEMS, Haifa, Israel). When the locations of organs were not definitely determined on the CT image for FDG-avid structures, the region of interest was placed on the PET image first. In the parotid and submandibular glands, the CT attenuation values (in Hounsfield units) in the regions of interest also were measured. In addition, a region of interest was placed over the blood activity in the aorta at the level of the arch to estimate the blood pool activity.
The standardized uptake value (SUV) was calculated by using the following formula: SUV = cdc/(di/w), where cdc is the decay-corrected tracer tissue concentration (in becquerels per gram); di, the injected dose (in becquerels); and w, the patient’s body weight (in grams). For bilateral structures such as the major salivary glands, palatine and lingual tonsils, thyroid gland lobes, and vocal cords, the mean of the values measured on both sides was calculated.
Statistical Analyses
We compared the degree of tracer uptake between the male and female patients by using the unpaired t test. To assess the relationship between tracer uptake and smoking history, we first divided the imaging data for 66 patients whose smoking histories were available into three groups: nonsmoker, past smoker, and current smoker data. Then, the mean SUVs were compared among the three data groups according to sex by using the Scheffé test. In addition, correlations between SUV and patient characteristics such as age and plasma glucose levels and between SUV and CT attenuation values (in Hounsfield units), as determined for the same region in the parotid and submandibular glands, were assessed (by Y.N.) by using the Pearson correlation coefficient test and were plotted by using a linear regression equation. Correlations among the three major salivary glands (parotid, submandibular, and sublingual glands) and between the two tonsils (palatine and lingual tonsils) were evaluated in the same manner. The significance of the correlations was assessed with the Fisher z test. P < .05 was considered to indicate a significant difference.
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RESULTS |
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TOPABSTRACTINTRODUCTIONMATERIALS AND METHODSRESULTSDISCUSSIONREFERENCES |
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Oropharynx Level
The soft palate showed intense FDG uptake in 72% of the patients (Fig 1a); the mean SUV was 3.13 ± 0.78. The palatine and lingual tonsils also commonly showed intense FDG uptake, which was seen in 80% and 74% of the patients, respectively. The mean SUV was 3.48 ± 1.30 for the palatine tonsils (Fig 1b) and 3.11 ± 1.06 for the lingual tonsils (Fig 1c). In contrast, the tongue had no or mild accumulation of FDG in 99% of the patients.
Hypopharynx Level
At the level below the lower margin of the epiglottic vallecula, FDG uptake in the submandibular (Fig 1d) and sublingual (Fig 1e) glands was variable, with positive rates of 53% and 72%, respectively. The mean SUV was 2.11 ± 0.57 for the submandibular glands and 2.93 ± 1.39 for the sublingual glands. The vocal cords showed no or mild uptake in 81% of the patients (Fig 1f); the mean SUV was 1.77 ± 0.69. The thyroid gland showed no or low uptake in 97% of the patients; the mean SUV was 1.31 ± 0.30 (Fig 1g).
Correlation
Generally, there were no major differences in the SUV for most tissues between the male and female patients (Table 2). In the soft palate (mean SUV, 3.39 ± 0.83 vs 2.90 ± 0.66, P < .01) and thyroid gland (mean SUV, 1.39 ± 0.31 vs 1.23 ± 0.27, P = .02), the mean SUV was slightly higher in the male patients than in the female patients. Smoking history did not appear to make any significant difference in uptake among the evaluated structures (Table 3).
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DISCUSSION |
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TOPABSTRACTINTRODUCTIONMATERIALS AND METHODSRESULTSDISCUSSIONREFERENCES |
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Jabour et al (8) previously reported intense uptake in the nasal turbinates, but no patients had intense uptake in this area in our series. Furthermore, in our series, the thyroid gland usually demonstrated low or mild FDG uptake. When bilateral intense uptake in the thyroid gland is noted, it might suggest the presence of an inflammatory condition, such as chronic thyroiditis (18), even if this inflammation was not suspected clinically.
In terms of normal FDG uptake in the head and neck region, we observed no correlation between tissue accumulation and plasma glucose level; however, most patients had normal plasma glucose levels before undergoing the scanning examinations. An age-related negative correlation was observed in the palatine tonsils and sublingual glands only. The palatine tonsils are usually largest in individuals aged 5–7 years; then they typically become smaller with age. Thus, for the palatine tonsils, the time course of involution of physiologic tonsilar size may partly explain the results.
There was a positive correlation between tracer uptake in the palatine tonsils and that in the lingual tonsils (r = 0.74, P < .01), but the expected negative correlation between uptake in the lingual tonsils and age was somewhat weaker (r = –0.31, P < .01). Because of tracer accumulation in inflammatory cells, inflammatory processes, especially during the acute phase, can cause increased attenuation at CT (19). Thus, a weak but definitely positive correlation between CT attenuation and FDG uptake was observed in the parotid and submandibular glands.
In this study, we performed qualitative assessments of FDG uptake and quantitative evaluations of SUV, as measured with CT attenuation–corrected PET images. Compared with the uptake values measured with PET images that were attenuation corrected by using an external source of combined germanium 68–gallium 68 in a previous study (20), the values that we observed were slightly higher. Dental metallic implants can also affect quantitative uptake values. Moreover, the iterative reconstruction that has been widely accepted for use in clinical FDG PET has been reported to yield quantitative values that are slightly different from those created by using the filtered back projection method, depending on the transmission scanning time and the emission scanning time (21). Therefore, the SUVs measured in this study could have been slightly different from the values measured only by using PET with germanium attenuation correction and filtered back projection reconstruction. Nonetheless, our qualitative and quantitative PET/CT results should accurately reflect relative FDG concentrations in tissue.
There were limitations in this study. Although a combined PET/CT scanner was effectively used, there may have been some tissue averaging of the measured values at evaluation of the soft palate because the posterior third of the tongue was in direct contact with the soft palate when the patient was supine. In addition, although we included only the cases of patients in whom no apparent disease (in the head and neck region) had been detected on the basis of other clinical information, a clinically disease-free status does not always mean a histologically normal status. We excluded the data on patients who had had any symptoms in the head and neck area on the basis of the results of brief clinical examinations and medical records, but if patients with symptoms did not reveal them, these individuals may have been included in our study population.
Similarly, although we found no abnormalities in the head and neck region in our study group at PET/CT, after scanning some patients may have developed head and neck abnormalities that had not yet been recognized owing to limited follow-up. Moreover, because we had examined predominantly patients who were clinically suspected of having a malignancy in the thoracic, abdominal, or pelvic region (not in the head and neck region), this study population comprised patients who generally were middle aged or older, and this may have affected the frequency of certain physiologic parameters. Yet, we believe this population was quite representative of patients who are referred for clinical PET.
In conclusion, PET/CT commonly depicted intense FDG uptake in several normal head and neck structures; such uptake must be recognized to avoid mistaking it for malignant involvement. The soft palate and tonsils almost always had intense FDG uptake, which was seen as a normal physiologic finding, and intense tracer accumulation in the major salivary glands was variable but also quite frequent.
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ACKNOWLEDGMENTS |
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FOOTNOTES |
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R.L.W. received honoraria from GE Medical Systems, CPS, Philips, and Cardinal Health.
Author contributions: Guarantor of integrity of entire study, Y.N.; study concepts and design, R.L.W., Y.N.; literature research, Y.N.; clinical studies, C.C., M.O., D.H.; data acquisition, M.T., D.H.; data analysis/interpretation, Y.N., M.T., D.H.; statistical analysis, Y.N., R.L.W.; manuscript preparation, Y.N.; manuscript definition of intellectual content, Y.N., R.L.W.; manuscript editing, Y.N., D.H., R.L.W.; manuscript revision/review, D.H., R.L.W.; manuscript final version approval, R.L.W.
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REFERENCES |
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TOPABSTRACTINTRODUCTIONMATERIALS AND METHODSRESULTSDISCUSSIONREFERENCES |
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