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DOI:10.2214/AJR.07.2652
AJR 2007; 189:1407-1413
© American Roentgen Ray Society

Clinical Observations

Integrated PET/CT of Salivary Gland Type Carcinoma of the Lung in 12 Patients

Sun Young Jeong1, Kyung Soo Lee1, Joungho Han2, Byung-Tae Kim3, Tae Sung Kim1, Young Mog Shim4 and Jhingook Kim4

1 Department of Radiology and Center for Imaging Science, Samsung Medical Center, Sungkyunkwan University School of Medicine, 50, Ilwon-Dong, Kangnam-Ku, Seoul 135-710, Korea.
2 Department of Diagnostic Pathology, Samsung Medical Center, Sungkyunkwan University School of Medicine, Seoul 135-710, Korea.
3 Department of Nuclear Medicine, Samsung Medical Center, Sungkyunkwan University School of Medicine, Seoul 135-710, Korea.
4 Department of Thoracic Surgery, Samsung Medical Center, Sungkyunkwan University School of Medicine, Seoul 135-710, Korea.

Received May 30, 2007; accepted after revision June 29, 2007.

 
Address correspondence to K. S. Lee (kyungs.lee{at}samsung.com).


Abstract
Top
 Abstract
Introduction
 Materials and Methods
 Results
 Discussion
 References
 
OBJECTIVE. The purpose of our study was to show the integrated 18F-FDG PET/CT findings of salivary gland type carcinomas of the lung.

CONCLUSION. Salivary gland type carcinomas of the lung appear as airway tumors with variable CT morphologies and show different patterns and extents of FDG uptake on PET images according to their grades of differentiation.

Keywords: CT • lung • lung neoplasms • PET • PET/CT • salivary gland • salivary gland type carcinoma


Introduction
Top
 Abstract
 Introduction
Materials and Methods
 Results
 Discussion
 References
 
Lung carcinomas of the salivary gland type occur primarily in central airways and presumably originate from submucosal glands. Overall, they account for 1–2% of all lung carcinomas. These tumors include adenoid cystic carcinoma (ACC), mucoepidermoid carcinoma (MEC), and epithelial–myoepithelial carcinoma [1]. Of the subtypes of salivary gland type carcinomas, ACC is the most common (75% of reported cases), followed by MEC (5–10%). ACC has an equal sex distribution and preferentially occurs in the fourth and fifth decades. Although MEC has been reported in patients ranging from 4 to 78 years old, nearly half of those affected are younger than 30 years old [2–4].

Most ACCs in the lung arise in the lower trachea or mainstem bronchi, and a peripheral or segmental location is uncommon (10% of the cases). These tumors have a striking tendency toward submucosal extension that manifests on CT images as an intraluminal mass with soft-tissue attenuation and extension through the tracheal wall, diffuse or circumferential wall thickening, a soft-tissue mass filling the airway, or a homogeneous mass encircling the trachea with wall thickening [5, 6]. MECs are more commonly observed in the segmental bronchus than in the trachea or main bronchus and appear as sharply marginated, ovoid or lobulated, intraluminal nodules that adapt to the branching features of airways [7].

Integrated 18F-FDG PET/CT offers both morphologic and metabolic information on neoplastic conditions of the lungs and airways, and PET/CT metabolic information on salivary gland type carcinomas of the lung is expected to provide underlying histopathologic information on tumors regarding numbers of malignant cells and their proliferative activity. However, few case reports are available on the integrated PET/CT findings of lung salivary gland type carcinomas [8, 9]. Thus, the purpose of this study was to characterize the integrated PET/CT findings of salivary gland type carcinomas of the lung and to compare these with pathologic findings.


Materials and Methods
Top
 Abstract
 Introduction
 Materials and Methods
Results
 Discussion
 References
 
Patient Enrollment
Our institutional review board approved this retrospective study and waived the requirement for informed consent. For the period between December 2003 and May 2007, we reviewed all recorded surgical biopsy files and selected patients with a pathologic diagnosis of salivary gland type carcinoma of the lung (ACC, MEC, or epithelial–myoepithelial carcinoma). In total, 16 patients were identified and, of these, 12 underwent integrated PET/CT and subsequent tissue confirmation or surgical resection. Five of the 12 had ACC and seven, MEC. Thus, we enrolled 12 patients with histopathologically proven salivary gland type carcinoma of the lung.

Demographic Data
Histories of cigarette smoking and symptoms and signs were assessed. Treatments administered for each salivary gland type carcinoma of the lung were recorded, as were treatment results.

Integrated PET/CT Acquisition
PET/CT was performed as previously described [10–12]. Briefly, patients fasted for at least 6 hours before undergoing PET/CT. After ensuring a normal blood glucose level in the peripheral blood (≤ 150 mg/dL), an IV injection of 370 MBq (10 mCi) of FDG was administered to the patient approximately 45 minutes before scanning. Scans were acquired using a PET/CT device (Discovery LS, GE Healthcare). CT was performed using a standard protocol with the following settings: 140 kV; 80 mA; tube rotation time, 0.5 second per rotation; pitch, 6; and section thickness, 5 mm (to match the PET section thickness). Immediately after unenhanced CT, PET was performed in an identical transverse field of view. CT data were resized from a 512 x 512 matrix to a 128 x 128 matrix to match the PET data so that scans could be fused and CT-based transmission maps generated. PET data sets were reconstructed iteratively using an ordered subset expectation maximization algorithm with segmented attenuation correction (two iterations, 28 subsets) using CT data.

Interpretation of the CT Component of PET/CT Images
Integrated PET/CT images were interpreted jointly by one chest radiologist and one nuclear medicine physician and decisions on findings were reached by consensus.

The CT analysis included the determination of tumor airway location, size, and morphology. Tumors were subcategorized by location as tracheal or as main, lobar, segmental, or subsegmental bronchial. Tumor long-axis diameters were measured, and tumors were also subcategorized by morphology as intraluminal nodules, iceberg tumors, or infiltrative lesions. Intraluminal nodules were defined as a tumor located exclusively within the airway with a well-defined smooth margin; iceberg tumors were defined as a tumor with intraluminal and extraluminal components with a smooth or lobulated margin; and infiltrative tumors were defined as a tumor manifested as circumferential airway wall thickening with surrounding mediastinal fat or extraluminal tissue invasion. The presence of postobstructive pneumonia or atelectasis was also recorded.

Interpretation of the PET Component of PET/CT Images
Maximum standardized uptake values (SUVs) of tumors were recorded. Patterns of uptake were described as heterogeneous or homogeneous. Heterogeneous uptake was considered present when a tumor showed spotted or mottled FDG uptake, and homogeneous uptake was considered present when the whole of a tumor showed homogeneous uptake, irrespective of the presence of a tumor necrotic area (an uptake void area). Lymph node (hilar or mediastinal) and distant metastases were also recorded with their maximum SUVs.

Integrated PET/CT–Pathology Comparisons
A lung pathologist with 14 years of experience reviewed the pathologic specimens. Histopathologic tumor grade and the presence of necrosis and an extraluminal tumor component were evaluated. In ACCs, three histologic grades were defined: grade 1, tumor composed of completely glandular lesions; grade 2, tumor containing a solid area < 30%; and grade 3, tumor containing a solid portion ≥ 30% [13]. Also in MECs, three histologic grades (grades 1–3) were defined by modifying the grading system of the Armed Forces Institute of Pathology (AFIP) [14, 15]. Maximum SUVs of tumors were compared with histologic grades for both ACCs and MECs.


Results
Top
 Abstract
 Introduction
 Materials and Methods
 Results
Discussion
 References
 
Demographic and Clinical Features
For ACCs (Figs. 1A, 1B, 1C, 1D, 1E, 1F, 2A, 2B, 2C, 2D, 2E, and 2F), the patients were four men and one woman (age range, 30–60 years; mean age, 45 years; median, 45 years). Tumors were located in main (n = 2, 40%), lobar (n = 2, 40%), or segmental (n = 1, 20%) bronchi. Tumor lesions observed on CT images were 43–59 mm (mean ± SD, 51 ± 7 mm; median, 50 mm) in longest diameter.


Figure 1
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  		Fig. 1A —Adenoid cystic carcinoma in 30-year-old man (patient 1 in Table 1). Transverse lung window CT scan (5-mm section thickness) obtained at level of right middle lobar bronchus shows lobulated mass obliterating superior segmental bronchus of left lower lobe.

 

Figure 2
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  		Fig. 1B —Adenoid cystic carcinoma in 30-year-old man (patient 1 in Table 1). CT (B), PET (C), and PET/CT (D) images obtained at left upper divisional bronchus show tumor has inhomogeneous mild 18F-FDG uptake (arrows, C and D). Maximum standardized uptake value was 5.0.

 

Figure 3
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  		Fig. 1C —Adenoid cystic carcinoma in 30-year-old man (patient 1 in Table 1). CT (B), PET (C), and PET/CT (D) images obtained at left upper divisional bronchus show tumor has inhomogeneous mild 18F-FDG uptake (arrows, C and D). Maximum standardized uptake value was 5.0.

 

Figure 4
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  		Fig. 1D —Adenoid cystic carcinoma in 30-year-old man (patient 1 in Table 1). CT (B), PET (C), and PET/CT (D) images obtained at left upper divisional bronchus show tumor has inhomogeneous mild 18F-FDG uptake (arrows, C and D). Maximum standardized uptake value was 5.0.

 

Figure 5
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  		Fig. 1E —Adenoid cystic carcinoma in 30-year-old man (patient 1 in Table 1). Gross pathologic specimen shows gray–tan mass consisting of intraluminal (arrows, superior segmental bronchus) and extraluminal (arrowheads) components of lesion. LLB = left lower lobar bronchus.

 

Figure 6
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  		Fig. 1F —Adenoid cystic carcinoma in 30-year-old man (patient 1 in Table 1). High-magnification photomicrograph shows that tumor consists of monotonous compact cells of cribriform (glandular) pattern with little atypism or mitotic activity. (H and E, x200)

 

Figure 7
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  		Fig. 2A —Adenoid cystic carcinoma in 45-year-old man (patient 3 in Table 1). Transverse lung window CT scan (5-mm section thickness) obtained at level of bronchus intermedius shows lobulated mass (arrows) obliterating lingular divisional bronchus of left upper lobe. Also note areas of obstructive pneumonia (arrowhead).

 

Figure 8
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  		Fig. 2B —Adenoid cystic carcinoma in 45-year-old man (patient 3 in Table 1). CT (B), PET (C), and PET/CT (D) images obtained at similar level to A show tumor has homogeneous high 18F-FDG uptake (arrows, C and D). Maximum standardized uptake value (SUV) is 8.3. Also note FDG uptake in hilar node (arrowheads, C and D; maximum SUV is 5.7), which proved to be metastatic in surgical specimen.

 

Figure 9
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  		Fig. 2C —Adenoid cystic carcinoma in 45-year-old man (patient 3 in Table 1). CT (B), PET (C), and PET/CT (D) images obtained at similar level to A show tumor has homogeneous high 18F-FDG uptake (arrows, C and D). Maximum standardized uptake value (SUV) is 8.3. Also note FDG uptake in hilar node (arrowheads, C and D; maximum SUV is 5.7), which proved to be metastatic in surgical specimen.

 

Figure 10
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  		Fig. 2D —Adenoid cystic carcinoma in 45-year-old man (patient 3 in Table 1). CT (B), PET (C), and PET/CT (D) images obtained at similar level to A show tumor has homogeneous high 18F-FDG uptake (arrows, C and D). Maximum standardized uptake value (SUV) is 8.3. Also note FDG uptake in hilar node (arrowheads, C and D; maximum SUV is 5.7), which proved to be metastatic in surgical specimen.

 

Figure 11
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  		Fig. 2E —Adenoid cystic carcinoma in 45-year-old man (patient 3 in Table 1). Gross pathologic specimen shows firm yellow–tan tumor with infiltrative intraluminal and extraluminal components of lesion (straight arrows) encircling lingular divisional bronchus of left upper lobe. Also note enlarged intrapulmonary node (curved arrow) and area of obstructive pneumonia (arrowhead). Li = lingular divisional bronchus.

 

Figure 12
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  		Fig. 2F —Adenoid cystic carcinoma in 45-year-old man (patient 3 in Table 1). High-magnification photomicrograph shows that tumor consists of solid (white arrows) and glandular (large black arrows) areas. Solid area contains cells having less cribriform pattern (small arrows), whereas glandular area contains cells having more cribriform pattern (arrowheads). Also note moderate to high cellular atypism in solid area. (H and E, x100)

 
For MECs (Figs. 3A, 3B, 3C, 3D, 3E, 3F, 4A, 4B, 4C, 4D, 4E, and 4F), the patients were five men and two women (age range, 23–63 years; mean age, 44 years; median, 46 years). Tumors were located in lobar (n = 3, 43%) or segmental (n = 4, 57%) bronchi. Tumor lesions observed on CT images were 10–45 mm (33 ± 13 mm; median, 36 mm) in longest diameter.


Figure 13
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  		Fig. 3A —Low-grade mucoepidermoid carcinoma in 63-year-old woman (patient 10 in Table 1). Transverse lung window CT scan (5-mm section thickness) obtained at level of suprahepatic inferior vena cava shows lobulated mass (arrows) in left lower lobe. Also note postobstructive mucus plugging (arrowhead).

 

Figure 14
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  		Fig. 3B —Low-grade mucoepidermoid carcinoma in 63-year-old woman (patient 10 in Table 1). CT (B), PET (C), and PET/CT (D) images obtained at similar level to A show tumor has little 18F-FDG uptake (arrows, C and D). Maximum standardized uptake value is 1.5.

 

Figure 15
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  		Fig. 3C —Low-grade mucoepidermoid carcinoma in 63-year-old woman (patient 10 in Table 1). CT (B), PET (C), and PET/CT (D) images obtained at similar level to A show tumor has little 18F-FDG uptake (arrows, C and D). Maximum standardized uptake value is 1.5.

 

Figure 16
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  		Fig. 3D —Low-grade mucoepidermoid carcinoma in 63-year-old woman (patient 10 in Table 1). CT (B), PET (C), and PET/CT (D) images obtained at similar level to A show tumor has little 18F-FDG uptake (arrows, C and D). Maximum standardized uptake value is 1.5.

 

Figure 17
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  		Fig. 3E —Low-grade mucoepidermoid carcinoma in 63-year-old woman (patient 10 in Table 1). Gross pathologic specimen shows yellow–tan tumor (arrows) occupying posterior basal segmental bronchus of left lower lobe. M = mucus within dilated bronchi distal to tumor nodule.

 

Figure 18
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  		Fig. 3F —Low-grade mucoepidermoid carcinoma in 63-year-old woman (patient 10 in Table 1). High-magnification photomicrograph shows tumor composed of mixture of glands, cysts, and solid areas. These areas show little mitotic activity, nuclear pleomorphism, or necrosis (low-grade malignancy). (H and E, x100)

 

Figure 19
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  		Fig. 4A —High-grade mucoepidermoid carcinoma in 48-year-old man (patient 6 in Table 1). Transverse mediastinal window CT scan (5-mm section thickness) obtained at level of right middle lobar bronchus shows mass (arrows) obliterating lingular divisional bronchus of left upper lobe. Left lower lobe (arrowhead) is partly atelectatic due to extraluminal extension of tumor.

 

Figure 20
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  		Fig. 4B —High-grade mucoepidermoid carcinoma in 48-year-old man (patient 6 in Table 1). CT (B), PET (C) and PET/CT (D) images obtained at similar level to A show tumor has avid and homogeneous 18F-FDG uptake (arrows, C and D). Maximum standardized uptake value is 23.4.

 

Figure 21
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  		Fig. 4C —High-grade mucoepidermoid carcinoma in 48-year-old man (patient 6 in Table 1). CT (B), PET (C) and PET/CT (D) images obtained at similar level to A show tumor has avid and homogeneous 18F-FDG uptake (arrows, C and D). Maximum standardized uptake value is 23.4.

 

Figure 22
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  		Fig. 4D —High-grade mucoepidermoid carcinoma in 48-year-old man (patient 6 in Table 1). CT (B), PET (C) and PET/CT (D) images obtained at similar level to A show tumor has avid and homogeneous 18F-FDG uptake (arrows, C and D). Maximum standardized uptake value is 23.4.

 

Figure 23
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  		Fig. 4E —High-grade mucoepidermoid carcinoma in 48-year-old man (patient 6 in Table 1). Gross pathologic specimen shows yellow–tan mass containing intraluminal (arrow) and extraluminal (arrowheads) components of lesion. LLB = left lower lobar bronchus, ULB = left upper lobar bronchus.

 

Figure 24
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  		Fig. 4F —High-grade mucoepidermoid carcinoma in 48-year-old man (patient 6 in Table 1). High-magnification photomicrograph shows tumor composed mainly of squamous and intermediate cells with few mucin-secreting cells. There is nuclear pleomorphism and hyperchromatism (high-grade malignancy). (H and E, x100)

 
Six patients (three with ACC and another three with MEC) were symptomatic. Symptoms included cough (n = 6), sputum (n = 3), and fever (n = 1). Four men (two with ACC and two with MEC) were smokers (mean, 15.6 pack-years; range, 2.5–30 pack-years), but the remaining eight (five men and three women) were nonsmokers.

For ACCs (n = 5), the treatments were as follows: lobectomy in one patient, sleeve lobectomy in two, pneumonectomy in one, and sleeve pneumonectomy in one. For MECs (n = 7), treatments were lobectomy in five patients, sleeve lobectomy in one, and pneumonectomy in one. On follow-up CT (n = 12) and bronchoscopy (n = 4) (mean follow-up period, 22 months; range, 4–39 months; median, 20 months), one patient with ACC (who had undergone sleeve left upper lobectomy previously) had recurrence at the ipsilateral hilar nodes 26 months after surgery. In this patient, completion pneumonectomy was performed without recurrence over the following 13 months. In the remaining 11 patients, no evidence of recurrence was seen.

CT Component Findings
ACCs (n = 5) manifested as an iceberg tumor in four patients (Figs. 1A, 1B, 1C, 1D, 1E, 1F, 2A, 2B, 2C, 2D, 2E, and 2F) and as an infiltrative tumor (intraluminal nodule with diffuse bronchial wall thickening) in one. Obstructive pneumonia, atelectasis, or mucus plugging was observed in three patients with a tumor nodule located in a main (n = 2) or lobar (n = 1) bronchus.

MECs (n = 7) presented on CT scans as an airway intraluminal nodule in five patients or as an iceberg tumor in two (Figs. 4A, 4B, 4C, 4D, 4E, and 4F). Obstructive pneumonia, atelectasis, or mucus plugging was observed in four patients with a tumor nodule located in segmental (n = 4) bronchi.

PET Component Findings
In ACCs (n = 5), tumors showed heterogeneous (Figs. 1A, 1B, 1C, 1D, 1E, and 1F) FDG uptake in four patients and homogeneous uptake in one (Figs. 2A, 2B, 2C, 2D, 2E, and 2F). Maximum SUVs ranged from 3.7 to 8.3 (5.5 ± 1.6). MECs (n = 7) showed heterogeneous (Figs. 3A, 3B, 3C, 3D, 3E, and 3F) uptake in five patients and homogeneous uptake (Figs. 4A, 4B, 4C, 4D, 4E, and 4F) in two, with maximum SUVs ranging from 1.5 to 23.4 (7.2 ± 7.4). In one ACC and one MEC (patients 3 and 6, respectively), hilar nodal metastasis was detected on PET (maximum SUV, 5.7 and 2.7, respectively) and nodes were confirmed to contain malignant cells histopathologically (Figs. 2A, 2B, 2C, 2D, 2E, and 2F). In the remaining 10 patients, neither hilar nor mediastinal nodal metastasis was found by integrated PET/CT or by histopathology.

PET/CT–Pathologic Comparisons
In ACCs (n = 5), a grade 1 tumor was present in four patients and a grade 2 tumor in one. In MECs (n = 7), a grade 1 tumor was present in four patients, a grade 2 in one, and a grade 3 in two. For both ACCs and MECs, high-grade tumors tended to have high FDG uptake and a homogeneous pattern (Figs. 2A, 2B, 2C, 2D, 2E, 2F, 4A, 4B, 4C, 4D, 4E, and 4F). High-grade tumors (grade 2 or more in both ACCs and MECs) had maximum SUVs of > 6 (Table 1). Tumor necrosis was observed in one patient with ACC and in another patient with MEC. In both of these patients, tumor necrosis accounted for < 5% of the entire tumor lesion.


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  		TABLE 1: PET/CT and Pathologic Findings in 12 Patients with Salivary Gland Type Carcinomas of the Lung

 


Discussion
Top
 Abstract
 Introduction
 Materials and Methods
 Results
 Discussion
References
 
Few articles have been published on the PET findings of salivary gland type carcinomas of the lung [8]. However, for neck salivary gland tumors, it has been reported that higher-grade malignancy had higher mean maximum SUVs than low- and intermediate-grade malignancies [16]. In our study, ACCs and MECs showed variable amounts and patterns (homogeneous vs heterogeneous) of FDG uptake within tumors, but tumors of high or intermediate grades (grades 2 or 3) in both types had avid (maximum SUV > 6) homogeneous FDG uptake. In one case of ACC in which tumor recurrence was noticed in an ipsilateral hilar node, the initial tumor had a high maximum SUV of 8.3 and showed grade 2 histopathologic differentiation. In one case of grade 3 MEC, the primary tumor had a maximum SUV of 23.4 and hilar nodal metastasis (maximum SUV, 2.7). Therefore, when salivary gland type cancer of the lung shows high and homogeneous FDG uptake suggestive of high-grade malignancy, more aggressive surgery should be planned.

In our study, ACCs occurred in larger airways (mostly in main or lobar bronchi) than did MECs (mostly in lobar or segmental bronchi) [5–7]. Locations of tumors observed in our study concur with previous reports. The morphologic features of ACCs and MECs on CT component images of PET/CT scans were also identical to those described previously [5–7]. Most ACCs manifested as iceberg tumors or tumors showing circumferential and infiltrative growth, whereas most MECs presented as an intraluminal nodule.

Because most salivary gland type carcinomas of the lung appear as airway tumors, they should be differentiated from bronchogenic carcinomas (squamous cell carcinoma or, less frequently, large cell neuroendocrine carcinoma or adenocarcinoma of the lung), carcinoids, and airway mesenchymal tumors (such as leiomyomas or neurogenic tumors). When ACCs and MECs are located in the central airways with avid FDG uptake, differential diagnosis of these tumors from above-mentioned carcinomas, especially squamous cell carcinomas, seems to be difficult. Although carcinoids or airway mesenchymal tumors present as airway tumors with intraluminal nodule or iceberg tumor morphologies, they may show less FDG uptake than salivary gland type carcinomas [11, 17, 18].

Our study is inherently limited by its retrospective design. In addition, we included a small number of salivary gland type carcinomas of the lung. A further correlative study on histopathologic grades and FDG PET/CT findings in a large number of salivary gland type carcinomas of the lung is warranted.

In conclusion, salivary gland type carcinomas in the lung manifest as airway tumors with or without lung parenchymal invasion on CT images and show different patterns and extents of FDG uptake on PET images. In addition, FDG uptake values and patterns of uptake are found to reflect underlying histopathologic tumor differentiation. Thus, we believe that analyses of the integrated PET/CT findings of these tumors may enable us to predict patient prognoses.


References
Top
 Abstract
 Introduction
 Materials and Methods
 Results
 Discussion
 References
 

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  17. Kim YK, Kim H, Lee KS, et al. Airway leiomyoma: imaging findings and histopathologic comparisons in 13 patients. AJR2007; 189:393 -399[Abstract/Free Full Text]
  18. Chong S, Lee KS, Chung MJ, Han J, Kwon OJ, Kim TS. Neuroendocrine tumors of the lung: clinical, pathologic, and imaging findings. RadioGraphics 2006;26 : 41-45[Abstract/Free Full Text]

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